Hojun Song 2018

Insect Systematics and Diversity, (2018) 2(4): 3; 1–25
doi: 10.1093/isd/ixy008
Research
Molecular Phylogenetics, Phylogenomics, and Phylogeography
Evolution, Diversification, and Biogeography of

Grasshoppers (Orthoptera: Acrididae)
Downloaded from https://academic.oup.com/isd/article/2/4/3/5052737 by Universidad Nacional de Colombia user on 06 August 2021

Hojun Song,1,4 Ricardo Mariño-Pérez,1 Derek A. Woller,1,2 and Maria Marta Cigliano3
Department of Entomology, Texas A&M University, 2475 TAMU, College Station, TX 77843-2475, 2Rangeland Grasshopper and
1
Mormon Cricket Management Team, USDA: APHIS-PPQ-S&T-CPHST Phoenix Lab, Phoenix, AZ, 3División Entomología, Museo La
Plata, CEPAVE-CONICET, La Plata, Argentina, and 4Corresponding author, e-mail: hsong@tamu.edu
Subject Editor: Jessica Ware
Received 6 March 2018; Editorial decision 31 May 2018
Abstract
The grasshopper family Acrididae is one of the most diverse lineages within Orthoptera, including more than 6,700
valid species distributed worldwide. Grasshoppers are dominant herbivores, which have diversified into grassland,
desert, semi-aquatic, alpine, and tropical forest habitats, and exhibit a wide array of morphological, ecological, and
behavioral diversity. Nevertheless, the phylogeny of Acrididae as a whole has never been proposed. In this study,
we present the first comprehensive phylogeny of Acrididae based on mitochondrial genomes and nuclear genes
to test monophyly of the family and different subfamilies as well as to understand the evolutionary relationships
among them. We recovered the monophyletic Acrididae and identified four major clades as well as several well-
characterized subfamilies, but we also found that paraphyly is rampant across many subfamilies, highlighting the
need for a taxonomic revision of the family. We found that Acrididae originated in the Paleocene of the Cenozoic
period (59.3 million years ago) and, because the separation of South America and Africa predates the origin of the
family, we hypothesize that the current cosmopolitan distribution of Acrididae was largely achieved by dispersal.
We also inferred that the common ancestor of modern grasshoppers originated in South America, contrary to a
popular belief that they originated in Africa, based on a biogeographical analysis. We estimate that there have been
a number of colonization and recolonization events between the New World and the Old World throughout the
diversification of Acrididae, and, thus, the current diversity in any given region is a reflection of this complex history.
Key words: Acrididae, grasshopper, phylogeny, biogeography
Grasshoppers (Orthoptera: Acrididae) are among the most recog- 1982). Some of the most important insect pests around the world
nizable and familiar insects in terrestrial habitats around the world. are locusts, which are grasshoppers that can form dense migrating
They are dominant herbivores and represent a ubiquitous component swarms and exhibit density-dependent phase polyphenism (Uvarov
of grasslands around the world (Uvarov 1966, Mitchell and Pfadt 1966, Pener 1983, Pener and Simpson 2009, Cullen et al. 2017).
1974, Gangwere et al. 1997, Cigliano et al. 2000, Guo et al. 2006). In While many grasshopper species are pests, some species are bene-
grassland ecosystems, grasshoppers contribute to more than half of ficial, such as Cornops aquaticum (Bruner, 1906) (Leptysiminae),
the total arthropod biomass in the above ground grass layer (Gillon which has been used as a successful biocontrol agent of water hya-
1983). They exert a significant ecological impact in grasslands in cinth in South Africa (Bownes et al. 2011, Coetzee et al. 2011), and
terms of nutrient cycling (Mitchell and Pfadt 1974, Belovsky and Hesperotettix viridis (Thomas, 1872) (Melanoplinae), which prefers
Slade 1993, Gangwere et al. 1997) and provide an important source to feed on noxious snakeweeds that can harm cattle and other live-
of nutrition for both invertebrates (Joern et al. 2006) and vertebrates stock (Thompson and Richman 1993).
(Gandar 1982), thus supporting other biological components of the Although grasshoppers are often thought to be associated with
ecosystem (Belovsky and Slade 1993). Grasshoppers can also be grasslands, many species are actually found in tropical forests, shrub-
excellent monitors of landscape use as they are ecologically sensitive lands, deserts, wetlands, and alpine regions around the world. For
and yet sufficiently mobile and abundant to serve as bioindicators example, Urnisiella rubropunctata Sjöstedt, 1930 (Catantopinae)
(Samways and Sergeev 1997, Gebeyehu and Samways 2002, Bazelet is highly adapted to the sandy habitat in the Australian outback,
and Samways 2014). Several species of grasshoppers are considered where it can withstand high temperatures and uses its long middle
major pests, especially when they periodically develop into local and legs to sweep sand over its body to bury itself when it is threat-
large-scale outbreaks, causing enormous economic damage (COPR ened (Rentz 1996). An aquatic grasshopper from South America,
© The Author(s) 2018. Published by Oxford University Press on behalf of Entomological Society of America. 1
All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
2 Insect Systematics and Diversity, 2018, Vol. 2, No. 4
Marellia remipes Uvarov, 1929 (Marelliinae), lives on broad, float- Rocky Mountains of the United States (Knowles 2001, Knowles
ing leaves of aquatic plants and its hind tibiae are modified and and Richards 2005), and Orotettix Ronderos & Carbonell, 1994,
expanded to be oar-like, which help it swim underwater (Carbonell Jivarus Giglio-Tos, 1898, and Maeacris Ronderos, 1983 in the
1957). Many specialized grasshopper species in the subfamilies Andes in South America (Cigliano and Amédégnato 2010, Cigliano
Proctolabinae and Ommatolampidinae (= Ommatolampinae) live in et al. 2011, Pocco et al. 2015), which are typically characterized by
the canopies of tropical rainforests in the Amazon (Descamps 1976, short-wings and have limited dispersal abilities. Indeed, grasshop-
Amédégnato and Descamps 1978, Descamps 1978). A number of pers are extremely diverse in terms of size, body shape, feeding biol-
alpine grasshoppers in the subfamily Melanoplinae have diversified ogy, ecology, and life-history traits (Fig. 1) (Uvarov 1977, Chapman
in isolated mountain ranges, such as Melanoplus Stål, 1873 in the and Joern 1990).
Fig. 1. Diversity of Acrididae: (A) Anacridium aegyptium (Linnaeus, 1764) (Cyrtacanthacridinae), France; (B) Dactylotum bicolor Charpentier, 1845 (Melanoplinae),
Mexico; (C) Kosciuscola tristis Sjöstedt, 1934 (Oxyinae), Australia; (D) Adimantus ornatissimus (Burmeister, 1838) (Copiocerinae), Argentina; (E) Calliptamus italicus
(Linnaeus, 1758) (Calliptaminae), France; (F) Proctolabus mexicanus (Saussure, 1859) (Proctolabinae), Mexico; (G) Marellia remipes Uvarov, 1929 (Marelliinae),
Colombia; (H) Paulinia acuminata (De Geer, 1773) (Pauliniinae), Colombia; (I) Acrida sp. (Acridinae), Vietnam; (J) Hylopedetes surdus Descamps & Rowell, 1978
(Rhytidochrotinae), Costa Rica; (K) Trimerotropis pallidipennis (Burmeister, 1838) (Oedipodinae), Mexico; (L) Stenopola puncticeps (Stål, 1861) (Leptysminae),
Argentina; (M) Rhammatocerus pictus (Bruner, 1900) (Gomphocerinae), Argentina; (N) Abracris flavolineata (De Geer, 1773) (Ommatolampidinae), Costa Rica;
(O) Hemiacris fervens Walker, 1870 (Hemiacridinae), Mozambique. Photo credits. A, E, I, N: Ruben Foquet; B, O: Ricardo Mariño-Pérez; C, J: Hojun Song; D, L, M:
Maria Marta Cigliano; F, K: Paolo Fontana; G, H: Juan Manuel Cardona.
Insect Systematics and Diversity, 2018, Vol. 2, No. 4 3
The family Acrididae includes more than 6,700 valid species and structures, prosternal process (a short spine located ventrally on
represents the most diverse lineage within the orthopteran suborder the prosternum between the two front coxae), sculpting patterns on
Caelifera (Cigliano et al. 2018). It is hypothesized to have originated in head and pronotum, hind legs, and wings for classifying grasshop-
the early Cenozoic Era and diversified through the mid to late Cenozoic pers (Rehn and Grant 1961, Bei-Bienko and Mishchenko 1963),
(Song et al. 2015). By this time, major continents had already separated, later authors regarded male phallic structures as the single most
which suggests that dispersal might have played an important role in important characters for higher-level classification (Dirsh 1973,
forming current biogeographical patterns. There are currently 26 recog- Amedegnato 1976, Eades 2000). However, too much reliance on
nized subfamilies within Acrididae (Table 1), of which only five subfam- these phallic structures led to over-splitting of taxonomic concepts,
ilies (Acridinae, Cyrtacanthacridinae, Gomphocerinae, Melanoplinae, especially when Dirsh (1975) elevated several subfamilies to family
and Oedipodinae) have a cosmopolitan distribution, while others have level, resulting in four families and 40 subfamilies.

more restricted distributions (Cigliano et al. 2018). Of the remain- Initially, taxonomic research on grasshopper diversity focused
ing subfamilies, 14 are found exclusively in the Old World, while on faunas in Europe, Africa, Eurasia, and North America, and,
seven are only found in the New World, mostly in Central and South thus, earlier classification schemes were established based on the
America. To explain this pattern, Carbonell (1977), Amédégnato and specimens collected from these regions (Rehn and Grant 1961,
Descamps (1979), Jago (1979), Rowell (1987), (Vickery 1987, 1989), Bei-Bienko and Mishchenko 1963, Dirsh 1965). During 1960s and
and Amedegnato (1993) proposed various biogeographic hypotheses 1970s, taxonomists began exploring South America and discovered
regarding the origin and diversification of different acridid lineages, but previously unknown grasshopper lineages, which led to the erection
these hypotheses have never been formally tested. of several new subfamilies (Amedegnato 1974, Amédégnato and
The taxonomy of Acrididae has had a tumultuous history (Song Descamps 1978). In fact, the faunas in Southeast Asia and Australia
2010). Throughout much of the 19th and 20th centuries, there was no still have not been fully explored (Key 1992, Rentz 1996, Song
clear definition of what should constitute Acrididae, and the family 2010). While many of the debates on how to classify different grass-
was used as a taxonomic dumping ground for groups when authors hopper groups have been made by European and North American
did not know where to place them (Eades 2000). For example, taxonomists, Chinese taxonomists have adopted a different classi-
Robert’s (1941) comparative study of male genitalia treated the cur- fication scheme (Zheng 1993, Xia 1994, Zheng and Xia 1998, Yin
rent families Pyrgomorphidae, Pamphagidae, Ommexechidae, and and Xia 2003) based on the species found in China, which they
Romaleidae as subfamilies of Acrididae, but they have since been continue to use currently. In an effort to produce a unified classi-
shown to be quite distinct families from Acrididae. Likewise Dirsh’s fication scheme, Otte (1995a,b) published the Orthoptera Species
(1961) preliminary revision of Acrididae included the currently File (OSF), which later became the basis for an electronic version
recognized families Dericorythidae, Tristiridae, Romaleidae, and (Cigliano et al. 2018), which most orthopterists accept. Currently,
Lithidiidae as subfamilies of Acrididae. Although early taxonomists the OSF recognizes 26 subfamilies (Table 1) and some unplaced
relied on external morphological characters, such as stridulatory tribes and genera for Acrididae.
Table 1. The 26 currently recognized subfamilies within Acrididae, number of genera and species, and distribution
Subfamily Number of genera Number of species Distribution
Acridinae 141 483 Cosmopolitan

Calliptaminae 12 92 Africa, Europe, Middle East, Central Asia, India
Catantopinae 341 1,077 Africa, Middle East, Asia, Australia
Copiocerinae 21 90 Central and South America, Caribbean
Coptacrinae 20 116 Sub-Saharan Africa, India, Southeast Asia
Cyrtacanthacridinae 36 162 Cosmopolitan
Egnatiinae* 9 36 North Africa, Middle East, Central Asia
Eremogryllinae* 2 5 Northwestern Africa
Euryphyminae 23 87 Southern Africa
Eyprepocnemidinae 26 159 Africa, Middle East, Southern Asia, Southeast Asia, Eastern Asia
Gomphocerinae 192 1,274 Cosmopolitan
Habrocneminae* 2 3 Southeast Asia
Hemiacridinae 38 122 Sub-Saharan Africa, Southern Asia, Southeast Asia
Leptysminae 21 79 North, Central, and South America, Caribbean
Marelliinae 1 1 South America
Melanoplinae 145 1,173 North, Central, and South America, Asia, Europe
Oedipodinae 137 792 Cosmopolitan
Ommatolampidinae 114 292 Central and South America, Caribbean
Oxyinae 37 307 Sub-Saharan Africa, Asia, Australia
Pauliniinae 1 1 Central and South America
Pezotettiginae* 2 10 Europe, Northwestern Africa
Proctolabinae 29 215 Central and South America
Rhytidochrotinae 20 47 Northern South America
Spathosterninae 3 12 Sub-Saharan Africa, Southern Asia, Southeast Asia, Australia
Teratodinae* 8 24 India, Middle East, Central eastern Africa
Tropidopolinae 11 34 Africa, Middle East, Southeast Asia
The numbers of genera and species are from OSF (Cigliano et al. 2018). Asterisks indicate those subfamilies not included in the present study due to
unavailability of DNA-grade specimens.
There has never been a comprehensive phylogeny proposed for a total of 142 taxa, including 8 outgroup and 134 ingroup taxa cover-
Acrididae, although several studies have focused on the phylogen- ing the phylogenetic diversity within Acrididae (Table 2, Supplementary
etic relationships at subfamily level using either morphology or Table 1). The outgroups included seven representative families within
molecular data (Chapco et al. 2001, Litzenberger and Chapco 2001, Acridoidea based on our previous findings on the higher-level relation-
Amédégnato et al. 2003, Litzenberger and Chapco 2003, Rowell and ships (Leavitt et al. 2013, Song et al. 2015). Of these outgroup taxa, four
Flook 2004, Bugrov et al. 2006, Contreras and Chapco 2006, Fries are Old World families: Pamphagidae, Pamphagodidae, Lithidiidae,
et al. 2007, Song and Wenzel 2008, Chapco and Contreras 2011, and Lentulidae, and three are endemic to the New World: Tristiridae,
Chintauan-Marquier et al. 2011, Li et al. 2011, Nattier et al. 2011, Romaleidae (two representatives included), and Ommexechidae. For
Chintauan-Marquier et al. 2014). Flook and Rowell (1997) pre- ingroup sampling, we included 21 of the 26 currently recognized acridid
sented the first molecular phylogeny of Caelifera based on fragments subfamilies. Due to the difficulty in obtaining DNA-grade specimens,

of mitochondrial ribosomal RNA genes, which included 12 acridids we did not include these five subfamilies in our analysis: Egnatiinae,
belonging to four subfamilies, but they did not recover monophyly Eremogryllinae, Habrocneminae, Pezotettiginae, and Teratodinae. We
of Acrididae because Pamphagidae was nested within Acrididae. included multiple representatives of each subfamily to test monophyly
Based on the investigation of male genitalia across Acridoidea, except Spathosterninae, Tropidopolinae, Marelliinae, and Pauliniinae,
Eades (2000) proposed that all acridids have a strongly developed the latter two of which are monotypic. For 58 terminals, which rep-
arch sclerite in the male phallic complex, which is not found in resented key taxa for understanding higher-level relationships, we
other families within the Acridoidea except the Pamphagodidae included partial or complete mtgenome data, 24 of which were newly
(= Charilaidae), apparently having evolved a similar structure inde- sequenced for this study. The remaining mtgenomes were either previ-
pendently. Liu et al. (2008) proposed a phylogeny of Acrididae ously generated by us (Fenn et al. 2008, Sheffield et al. 2010, Leavitt
using 24 Chinese species based on two mitochondrial ribosomal et al. 2013, Song et al. 2015) or obtained from GenBank (Table 2). For
genes and found that Acridinae and Catantopinae were paraphy- all taxa, we generated complete sequences of 18S and 28S ribosomal
letic, while Cyrtacanthacridinae, Oxyinae, and Oedipodinae were RNA genes and histone 3 (H3) genes, as well as full-length sequences of
monophyletic. Li et al. (2011) published a morphological phylogeny mitochondrial cytochrome c oxidase 1 and 2 (COI and COII). For the
of Catantopidae, which Chinese authors recognize as a valid fam- 19 taxa for which we obtained mtgenome sequences from GenBank, we
ily that includes grasshoppers with the prosternal process, based were unable to generate the three nuclear genes due to an obvious lack
on an analysis of 87 genera and 88 characters. They recovered of access to specimens.
monophyletic Catantopidae, but because they did not include any DNA-grade tissue samples used for this study were either collected
grasshoppers without the prosternal process (such as Acridinae, by the authors or provided by collaborators. They were preserved in
Gomphocerinae, and Oedipodinae) or the New World endemic 100% ethanol and vouchered in the −80°C freezer in the Texas A&M
groups that possess this structure (such as Ommatolampidinae, University Insect Collection’s Insect Genomic Collection (TAMUIC-
Leptysminae, Rhytidochrotinae, Copiocerinae, and Proctolabinae), IGC). To generate 18S, 28S, H3, COI, and COII sequences, we followed
their inferences need to be viewed with caution. Leavitt et al. (2013) standard protocols for DNA extraction, PCR, and Sanger sequencing,
tested the monophyly of Acrididae using complete mitochondrial which we described in detail elsewhere (Mugleston et al. 2013, Song
genome (mtgenome) sequences and 34 caeliferan taxa (including 16 et al. 2015). To generate mtgenome sequences, we performed shotgun
acridid species) and recovered strong monophyly of the family, but sequencing of genomic DNA using the Illumina platform. To extract
only eight subfamilies were included, none of which were from South high molecular weight DNA required for Illumina sequencing, we
America. Most recently, Song et al. (2015) published a phylogeny of used a Gentra Puregene Tissue Kit (Qiagen) following the manufactur-
Orthoptera based on 254 taxa and four nuclear genes (18S and 28S er’s guidelines. The quality and concentration of DNA extracts were
rRNA, histone 3, and wingless) and complete mtgenome sequences initially measured using either Qubit Fluorometer (Thermo Fisher) or
for 69 backbone terminals, which included 87 acridid taxa cover- DeNovix Spectrophotometer, and more thoroughly analyzed using
ing the phylogenetic and geographic diversity of the family. While Fragment Analyzer (Advanced Analytical Technologies). We used a
they recovered monophyletic Acrididae with strong support based Nextera XT DNA Library Prep Kit for library preparation and per-
only on mtgenome data, the family was rendered paraphyletic in a formed either 150bp paired-end (PE) sequencing using NextSeq500 or
total evidence analysis. They noted that branch lengths were very 125bp PE sequencing using HiSeq2500.
short within Acrididae, suggesting that the nuclear genes used in the Library preparation and next-generation sequencing (NGS)
analysis were too conserved and did not have enough phylogenetic were conducted at either Georgia Genomic Facility (NextSeq500)
signal to accurately resolve the phylogeny of Acrididae. or Texas A&M Genomics and Bioinformatics Service (HiSeq2500).
The two primary objectives of this study are 1) to present the first The resulting raw reads were quality-trimmed in CLC Genomics
large-scale molecular phylogeny of Acrididae to test monophyly of Workbench 8 (Qiagen). We used the MITObim pipeline (Hahn
the family and different subfamilies, as well as 2) to understand the et al. 2013) to assemble mtgenomes de novo from the NGS reads.
evolutionary relationships among these groups. Based on the resulting All newly assembled mtgenomes were first uploaded as raw fasta
phylogeny and divergence time estimates, we also propose a novel bio- files to MITOS (Bernt et al. 2013) to identify open reading frames
geographical hypothesis regarding the origin and diversification of dif- (ORFs) and tRNAs. The initial MITOS annotation was used as a
ferent lineages of Acrididae. This will provide a framework for future guideline to delimit gene boundaries, and start and stop codons
phylogeny-based classification of Acrididae and a reference for study- of each protein-coding gene were manually identified in Geneious
ing interesting biology and evolutionary patterns within this family. 10.0.9 (Biomatters), following the recommendation by Cameron
(2014). DNA sequence data generated for this study were deposited
in Genbank with accession numbers presented in Table 2.
Materials and Methods
Taxon and Character Sampling Phylogenetic Analyses
We followed the classification scheme adopted by the OSF (Cigliano For both mitochondrial and nuclear protein-coding genes, we aligned
et al. 2018) in order to test it with our phylogenetic analysis. We sampled based on the conservation of reading frames by first translating into
Table 2. Taxonomic information and Genbank accession numbers for 142 taxa used in total evidence analysis
Voucher #
Family Subfamily Species (TAMUIC-IGC-#) mtgenome 18S 28S H3 COI COII
Acrididae Acridinae Acrida willemsei OR059 NC_011303 KM853177 KM853512 KM853687 mtgenome mtgenome
Calephorus compressicornis OR192 N/A KM853192 KM853498 KM853673 MG888076 MG888143
Coryphosima stenoptera OR512 N/A MG888284 MG888333 MG888241 MG888120 MG888187
Gymnobothrus sp OR511 N/A MG888283 MG888332 MG888240 MG888119 MG888186
Hyalopteryx rufipennis OR240 N/A KM853210 KM853480 KM853655 MG888088 MG888155
Keya capicola OR514 N/A MG888286 MG888335 MG888243 MG888122 MG888189
Orthochtha sp OR513 N/A MG888285 MG888334 MG888242 MG888121 MG888188
Phlaeoba albonema N/A NC_011827 N/A N/A N/A mtgenome mtgenome
Truxalis sp OR510 N/A KM853325 KM853367 KM853543 MG888118 N/A
Calliptaminae Acorypha sp OR195 N/A MG888254 MG888300 MG888208 MG888078 MG888145
Calliptamus italicus OR193 NC_011305 KM853193 KM853497 KM853672 mtgenome mtgenome
Paracaloptenus caloptenoides OR194 N/A KM853194 KM853496 KM853671 MG888077 MG888144
Catantopinae Apotropis vittata OR493 N/A MG888277 MG888325 MG888233 MG888106 MG888173
Buforania sp OR500 N/A MG888278 MG888327 MG888235 MG888113 MG888180
Catantops sp OR237 N/A KM853209 KM853481 KM853656 MG888086 MG888153
Insect Systematics and Diversity, 2018, Vol. 2, No. 4
Cedarinia sp OR490 N/A MG888274 MG888322 MG888230 MG888103 MG888170

Coryphistes ruricola OR503 MG993389, MG993390, MG888281 MG888330 MG888238 mtgenome mtgenome
MG993403, MG993406
Ecphantus quadrilobus OR495 N/A MG888295 MG888326 MG888234 MG888108 MG888175
Gen nov. 46 sp. 1 OR491 N/A MG888275 MG888323 MG888231 MG888104 MG888171
Gen nov. 64 sp. 1 OR489 N/A MG888273 MG888321 MG888229 MG888102 MG888169
Goniaea vocans OR502 N/A MG888280 MG888329 MG888237 MG888115 MG888182
Kinangopa jeanneli OR574 N/A KM853345 KM853348 KM853523 N/A MG888205
Macrolopholia sp OR235 N/A KM853208 KM853482 KM853657 MG888085 MG888152
Macrotona sp OR488 N/A MG888272 MG888320 MG888228 MG888101 MG888168
Pezocatantops sp OR505 N/A KM853321 KM853372 KM853548 MG888117 MG888184
Phaeocatantops sp OR504 N/A MG888282 MG888331 MG888239 MG888116 MG888183
Porraxia sp OR494 N/A KM853316 KM853377 KM853553 MG888107 MG888174
Retuspia validicornis OR496 N/A KM853317 KM853376 KM853552 MG888109 MG888176
Rusurplia tristis OR497 N/A KM853318 KM853375 KM853551 MG888110 MG888177
Stenocatantops vitripennis OR498 N/A KM853319 KM853374 KM853550 MG888111 MG888178
Traulia szetschuanensis N/A NC_013826 N/A N/A N/A mtgenome mtgenome
Typaya semicristata OR492 N/A MG888276 MG888324 MG888232 MG888105 MG888172
Urnisa guttulosa OR501 N/A MG888279 MG888328 MG888236 MG888114 MG888181
Urnisiella rubropunctata OR499 N/A KM853320 KM853373 KM853549 MG888112 MG888179
Xenocatantops brachycerus OR236 NC_021609 MG888296 MG888303 MG888211 mtgenome mtgenome
Copiocerinae Copiocera sp OR333 MG993384 KM853250 KM853440 KM853616 mtgenome mtgenome
Cyphacris sp OR334 N/A KM853251 KM853439 KM853615 MG888096 MG888163
Coptacrinae Eucoptacra sp OR509 MG993445 KM853324 KM853368 KM853544 mtgenome mtgenome
Parepistaurus deses OR508 N/A KM853323 KM853369 KM853545 N/A MG888185
Cyrtacanthacridinae Acanthacris ruficornis OR183 N/A MG888253 MG888299 MG888207 MG888071 MG888138
Acridoderes sp OR546 N/A MG888293 MG888342 MG888250 MG888137 MG888203
Anacridium incisum OR184 N/A KM853185 KM853505 KM853680 MG888072 MG888139
5

6
Table 2. Continued
Voucher #
Acrididae Cyrtacanthacridinae Austracris guttulosa OR182 MG993415 MG888252 MG888298 MG888206 mtgenome mtgenome
Chondracris rosea N/A NC_019993 N/A N/A N/A mtgenome mtgenome
Cyrtacanthacris tatarica OR181 MG993444 KM853184 KM853506 KM853681 mtgenome mtgenome
Nomadacris septemfasciata OR545 N/A KM853340 KM853352 KM853528 MG888136 N/A
Ornithacris sp OR544 N/A KM853339 KM853353 KM853529 MG888135 MG888202
Rhadinacris schistocercoides OR547 N/A KM853341 KM853351 KM853527 N/A MG888204
Schistocerca gregaria OR185 NC_013240 KM853186 KM853504 KM853679 mtgenome mtgenome
Euryphyminae Calliptamicus sp OR313 N/A MG888261 MG888308 MG888216 N/A N/A
Calliptamulus sp OR311 N/A KM853241 KM853449 KM853625 MG888094 MG888161
Euryphymus sp OR314 MG993388, MG993422, KM853243 KM853447 KM853623 mtgenome mtgenome
MG993436
Pachyphymus sp OR308 N/A MG888260 MG888307 MG888215 MG888092 MG888159
Rhachitopis sp OR312 N/A KM853242 KM853448 KM853624 N/A N/A
Eyprepocnemidinae Cataloipus sp OR218 N/A KM853201 KM853489 KM853664 MG888079 MG888146
Eyprepocnemis plorans OR309 MG993386, KM853239 KM853451 KM853627 mtgenome mtgenome
MG993418,MG993424,
MG993425,MG993427,
MG993433,MG993437,
MG993450
Heteracris sp OR310 N/A KM853240 KM853450 KM853626 MG888093 MG888160
Shirakiacris shirakii N/A NC_021610 N/A N/A N/A mtgenome mtgenome
Tylotropidius sp OR219 N/A MG888255 MG888301 MG888209 MG888080 MG888147
Gomphocerinae Arcyptera coreana N/A NC_013805 N/A N/A N/A mtgenome mtgenome
Aulocara elliotii OR521 N/A KM853329 KM853363 KM853539 MG888129 MG888196
Dichromorpha viridis OR226 N/A KM853205 KM853485 KM853660 MG888083 MG888150
Euchorthippus fusigeniculatus N/A NC_014449 N/A N/A N/A mtgenome mtgenome
Gomphocerus sibiricus N/A NC_015478 N/A N/A N/A mtgenome mtgenome
Mermiria intertexta OR520 N/A KM853328 KM853364 KM853540 MG888128 MG888195
Mesopsis sp OR239 N/A MG888257 MG888304 MG888212 MG888087 MG888154
Orinhippus tibetanus N/A NC_023467 N/A N/A N/A mtgenome mtgenome
Pacris xizangensis N/A NC_023919 N/A N/A N/A mtgenome mtgenome
Prorocorypha snowi OR214 MG993438, KM853199 KM853491 KM853666 mtgenome mtgenome
MG993452,
MG993453
Pseudogmothela sp OR519 N/A MG888289 MG888338 MG888246 MG888127 MG888194
Rhammatocerus OR346 N/A KM853258 KM853432 KM853608 MG888098 MG888164
schistocercoides
Rhaphotittha sp OR518 N/A MG888288 MG888337 MG888245 MG888126 MG888193
Silvitettix sp OR343 N/A MG888267 MG888314 MG888222 N/A N/A
Syrbula montezuma OR227 N/A KM853206 KM853484 KM853659 MG888084 MG888151

Table 2. Continued
Voucher #
Acrididae Hemiacridinae Dirshacris aridus OR305 MG993398, MG888259 MG888306 MG888214 mtgenome mtgenome
MG993399,
MG993410,
MG993417,
MG993420,
MG993434,
MG993435,
MG993451
Euroryma sp OR302 N/A KM853236 KM853454 KM853630 MG888090 MG888157
Hieroglyphus tonkinensis N/A NC_030587 N/A N/A N/A mtgenome mtgenome
Leptacris sp OR304 MG993429 KM853238 KM853452 KM853628 mtgenome mtgenome
Paulianiobia hirsuta OR301 N/A MG888258 MG888305 MG888213 MG888089 MG888156
Pristocorypha sp OR303 N/A KM853237 KM853453 KM853629 MG888091 MG888158
Leptysminae Stenacris sp OR342 N/A KM853255 KM853435 KM853611 N/A N/A
Stenopola sp OR220 N/A MG888256 MG888302 MG888210 MG888081 MG888148

Tetrataenia surinama OR338 MG993385, KM853254 KM853436 KM853612 mtgenome mtgenome
MG993395,
MG993396,
MG993404,
MG993407,
MG993409,
MG993432,
MG993448
Marelliinae Marellia remipes OR344 MG993387, KM853256 KM853434 KM853610 mtgenome mtgenome
MG993423,
MG993442,
MG993447
Melanoplinae Anapodisma miramae OR356 N/A KM853265 KM853425 KM853601 MG888100 MG888166
Aptenopedes sphenarioides OR516 N/A MG888287 MG888336 MG888244 MG888124 MG888191
Bradynotes obesa OR515 N/A KM853326 KM853366 KM853542 MG888123 MG888190
Dichroplus sp OR325 N/A KM853248 KM853442 KM853618 MG888095 MG888162
Fruhstorferiola kulinga N/A NC_026716 N/A N/A N/A mtgenome mtgenome
Hesperotettix viridis OR517 N/A KM853327 KM853365 KM853541 MG888125 MG888192
Jivarus ronderosi OR328 MG993400, KM853249 KM853441 KM853617 mtgenome mtgenome
MG993405
Kingdonella bicollina N/A NC_023920 N/A N/A N/A mtgenome mtgenome
Maeacris aptera OR329 N/A MG888266 MG888313 MG888221 N/A N/A
Melanoplus bivittatus OR245 MG993426 KM853211 KM853479 KM853654 mtgenome mtgenome
Ognevia longipennis OR394 NC_013701 MG888297 MG888319 MG888227 mtgenome mtgenome
Ponderacris peruvianus OR324 N/A MG888265 MG888312 MG888220 N/A N/A
Prumna arctica OR395 NC_013835 KM853277 KM853412 KM853589 mtgenome mtgenome
Qinlingacris taibaiensis N/A NC_027187 N/A N/A N/A mtgenome mtgenome
Oedipodinae Acrotylus patruelis OR190 N/A KM853190 KM853500 KM853675 MG888075 MG888142
7

8
Table 2. Continued
Voucher #
Acrididae Oedipodinae Angaracris barabensis N/A NC_025946 N/A N/A N/A mtgenome mtgenome
Bryodema miramae miramae N/A KP889242 N/A N/A N/A mtgenome mtgenome
Ceracris kiangsu N/A NC_019994 N/A N/A N/A mtgenome mtgenome
Chortoicetes terminifera OR524 N/A MG888290 MG888339 MG888247 MG888132 MG888199
Gastrimargus marmoratus N/A NC_011114 N/A N/A N/A mtgenome mtgenome
Heteropternis sp OR225 N/A KM853204 KM853486 KM853661 MG888082 MG888149
Locusta migratoria OR191 NC_001712 KM853191 KM853499 KM853674 mtgenome mtgenome
Psinidia fenestralis OR522 N/A KM853330 KM853362 KM853538 MG888130 MG888197
Pycnostictus seriatus OR525 N/A MG888291 MG888340 MG888248 MG888133 MG888200
Qualetta maculata OR526 N/A MG888292 MG888341 MG888249 MG888134 MG888201
Tomonotus ferruginosus OR523 N/A KM853331 KM853361 KM853537 MG888131 MG888198
Trilophidia annulata N/A NC_027179 N/A N/A N/A mtgenome mtgenome
Trimerotropis sp OR186 N/A KM853187 KM853503 KM853678 MG888073 MG888140
Xanthippus sp OR187 N/A KM853188 KM853502 KM853677 MG888074 MG888141
Ommatolampidinae Abracris sp OR222 MG993440 KM853202 KM853488 KM853663 mtgenome mtgenome
Anablysis teres OR362 N/A MG888269 MG888316 MG888224 N/A N/A
Kyphiacris sp OR363 N/A MG888270 MG888317 MG888225 N/A N/A
Locheuma brunneri OR366 N/A KM853268 KM853422 KM853598 N/A N/A
Lysacris festae OR365 N/A MG888271 MG888318 MG888226 N/A N/A
Ommatolampis OR364 MG993443 KM853267 KM853423 KM853599 mtgenome mtgenome
quadrimaculata
Pollostacris sp OR322 MG993391, MG888263 MG888310 MG888218 mtgenome mtgenome
MG993411,
MG993413
Psiloscirtus sp OR348 N/A MG888268 MG888315 MG888223 MG888099 MG888165
Syntomacrella sp OR323 N/A MG888264 MG888311 MG888219 N/A N/A
Vilerna sp OR336 N/A KM853252 KM853438 KM853614 MG888097 N/A
Xiphidiopteron sp OR321 N/A MG888262 MG888309 MG888217 N/A N/A
Oxyinae Kosciuscola tristis OR396 MG993402, KM853278 KM853411 KM853588 mtgenome mtgenome
MG993408,
MG993414
Oxya chinensis OR315 NC_010219 KM853244 KM853446 KM853622 mtgenome mtgenome
Pseudoxya diminuta N/A NC_025765 N/A N/A N/A mtgenome mtgenome
Pauliniinae Paulinia acuminata OR345 MG993401, KM853257 KM853433 KM853609 mtgenome mtgenome
MG993416,
MG993419,
MG993430,
MG993431,
MG993446
Proctolabinae Coscineuta sp OR249 MG993441 KM853212 KM853478 KM853653 mtgenome mtgenome
Poecilocloeus napoana OR368 N/A KM853270 KM853420 KM853596 N/A N/A
Rhytidochrotinae Galidacris variabilis OR371 N/A KM853271 KM853419 KM853595 N/A MG888167

Table 2. Continued
Voucher #
Acrididae Rhytidochrotinae Paropaon sp OR337 MG993393, KM853253 KM853437 KM853613 mtgenome mtgenome
MG993397,
MG993421,
MG993428,
MG993449
Spathosterninae Spathosternum nigrotaeniatum OR224 MG993439 KM853203 KM853487 KM853662 mtgenome mtgenome
Tropidopolinae Petamella prosternalis OR560 MG993412 KM853343 KM853349 KM853525 mtgenome mtgenome
Lentulidae Lentulinae Lentula callani OR295 NC_020774 KM853234 KM853456 KM853632 mtgenome mtgenome
Lithidiidae Lithidiinae Lithidiopsis carinatus OR316 NC_020775 KM853245 KM853445 KM853621 mtgenome mtgenome
Ommexechidae Ommexechinae Ommexecha virens OR367 NC_020778 KM853269 KM853421 KM853597 mtgenome mtgenome
Pamphagidae Thrinchinae Prionotropis hystrix OR151 JX913764 KM853180 KM853509 KM853684 mtgenome mtgenome
Pamphagodidae Unplaced Hemicharilaus monomorphus OR540 JX913773 KM853337 KM853355 KM853531 mtgenome mtgenome
Romaleidae Romaleinae Romalea microptera OR1000 MG993392, MG888294 MG888343 MG888251 mtgenome mtgenome
MG993394,
MG993454,
MG993455,
MG993456, MG993457
Xyleus modestus OR265 NC_014490 KM853221 KM853469 KM853644 mtgenome mtgenome
Tristiridae Tristirinae Tristira magellanica OR204 NC_020773 KM853197 KM853493 KM853668 mtgenome mtgenome
‘N/A’ means that the sequence data were not available. ‘mtgenome’ means that the corresponding sequences were derived from the available mtgenome data. For some taxa, multiple Genbank accession numbers are assigned
for mtgenome, which indicates partial mtgenomes consisting of several fragments.
9

amino acids and aligning individually in MUSCLE (Edgar 2004) fossil was Tyrbula russelli Scudder, 1885, known from the Florissant
using default parameters in Geneious. All other genes were individu- Formation of the Eocene of the United States (37.2 to 33.9 MYA).
ally aligned in MUSCLE using default parameters, also in Geneious. A number of fragmentary fossils of Acrididae have been found in this
All these individual alignments were concatenated into a single mat- formation and the one we chose is the most completely preserved
rix using SequenceMatrix (Vaidya et al. 2011). We divided the data specimen known, which characteristically resembles the North
into a total of 66 data blocks (13 mitochondrial protein-coding American gomphocerine Syrbula (Scudder 1890). In our analyses,
genes divided into individual codon positions, 22 tRNAs, 2 mito- Gomphocerinae was paraphyletic with Acridinae and Oedipodinae,
chondrial rRNAs, 2 nuclear rRNAs, and 1 nuclear protein-coding although these three subfamilies as a whole formed a clade. In fact,
gene). We then used PartitionFinder v.1.1.1 (Lanfear et al. 2012) they have been considered paraphyletic grades in previous studies
using the ‘greedy’ algorithm (heuristic search) with branch lengths (Chapco and Contreras 2011). Thus, we used T. russelli to calibrate

estimated as ‘linked’ to search for the best-fit scheme as well as to the clade consisting of these three subfamilies. The final fossil was
estimate the model of nucleotide evolution for each partition using Menatacridium eocenicum Piton 1936 of the Paleocene of France
the Bayesian Information Criterion (BIC). (58.7 to 55.8 MYA), which is the oldest known fossil of Acrididae.
We performed maximum likelihood (ML) and Bayesian (BA) However, we did not use this to calibrate the node at the base of
analyses on two datasets that include both mitochondrial and Acrididae, but at a node of an internal clade consisting of clades B,
nuclear loci: a backbone dataset (20,425 aligned bp and 58 taxa) C, and D (Fig. 3). The rationale for this is as follows: in all of the
and a total evidence dataset (20,425 aligned bp and 142 taxa). The phylogenetic analyses, the earliest diverging clade (A in Fig. 3) within
backbone dataset had 11.1% missing data due to those 19 taxa Acrididae consisted of subfamilies restricted to the Neotropics, sug-
that we obtained from Genbank without nuclear gene data, and the gesting a South American origin for Acrididae. Since this fossil is
total evidence dataset had 46.2% missing data due to 83 taxa with- from France, which in the Paleocene was not far from its present-day
out sequenced mtgenomes. We compared the resulting topologies location, we considered that it could not be the stem Acrididae, but
to examine the effect of missing data in phylogenetic reconstruc- the stem of the group that colonized the Old World. Therefore, we
tion in the total evidence dataset. For the ML analyses, we used the used it to calibrate this node.
best-fit partitioning scheme recommended by PartitionFinder with For this analysis, we used the total evidence dataset following
the GTRCAT model applied to each partition and analyzed using the partitioning scheme and the models of nucleotide evolution rec-
RAxML 7.2.8 (Stamatakis et al. 2008) on XSEDE (Extreme Science ommended by PartitionFinder. We created an XML file in BEAUti
and Engineering Discovery Environment, https://www.xsede.org) from the BEAST2 package, specifying the fossil priors and mono-
through the CIPRES Science Gateway (Miller et al. 2011). Nodal phyly constraints. We used the relaxed clock lognormal model for
support was evaluated using 1,000 replications of rapid bootstrap- the clock model, the birth-death model with a uniform distribution
ping implemented in RAxML. For the BA analyses, we used the best- as a tree prior, and a lognormal distribution as a distribution prior
fit partitioning scheme and partition-specific models recommended for fossil calibration points following a general guideline discussed
by PartitionFinder and analyzed using MrBayes 3.2.6 (Ronquist in Ho and Phillips (2009). To assess convergence across independ-
et al. 2012) also on CIPRES. We used default priors and ran four ent runs, we conducted two separate analyses each for 100 million
runs with four chains each for 100 million generations, sampling generations, sampling every 2,500 generations. We inspected the
every 5,000 generations. We plotted the likelihood trace for each run results using Tracer (Rambaut and Drummond 2003–2009), dis-
to assess convergence in Tracer (Rambaut and Drummond 2003– carded 25% of each run as burn-in, and combined the trees using
2009), and discarded an average of 25% of each run as burn-in. LogCombiner (Rambaut and Drummond 2002–2013a). A max-
The resulting trees were visualized using FigTree (Rambaut 2006– imum clade credibility tree was summarized in TreeAnnotator
2009). Our aligned datasets and the resulting trees were deposited to (Rambaut and Drummond 2002–2013b) and visualized in FigTree.
Mendeley (doi:10.17632/3cgttymztk.1).
Biogeographic Analysis
Divergence Time Estimate Analysis We used the package BioGeoBEARS (Biogeography with Bayesian
In order to estimate timing and rates of divergence across major [and Likelihood] Evolutionary Analysis in R Scripts) (Matzke 2013)
grasshopper lineages using fossil records, we performed a divergence within R (R Core Team 2017) to infer biogeographical patterns
time estimate analysis in a Bayesian framework using the BEAST2 during the diversification of different lineages within Acrididae.
package (Bouckaert et al. 2014). We used the Fossilworks data- BioGeoBEARS performs different models of ancestral range esti-
base (Behrensmeyer and Turner 2013) to search for known fossils mation because different ancestral-area reconstructions have dif-
of Acrididae. Although there are more than 50 fossil acridid speci- ferent assumptions. The input files were: 1) a dated phylogeny
mens, many of them were discovered from the same deposits, and, inferred from the BEAST analysis and 2) a file of geographical
so, there were only a small number of calibration points available to ranges indicating presence/absence of each taxon in each discrete
use for the analysis. Furthermore, many of the known fossils repre- area in the analysis. We defined six areas: Neotropical, Nearctic,
sented either crown groups or extant species. As a result, we selected Palearctic, Ethiopian, Oriental, and Australian following the most
three fossil species representing stem groups of different lineages commonly used divisions of the biogeographical realms. We iden-
within Acrididae. The first fossil was Proschistocerca oligocaenica tified a distribution range for each terminal (treated at the genus
Zeuner 1937, known from the Eocene of the United Kingdom (37.2 level) from the distribution maps available from the OSF (Cigliano
to 33.9 million years ago [MYA]). This is the oldest definitive fos- et al. 2018). Although this information from the OSF was not based
sil of the subfamily Cyrtacanthacridinae and we used it to calibrate on specimen-level databases, we were able to identify the distribu-
this monophyletic group (Song and Wenzel 2008). Although there tion ranges with confidence. To cope with those genera with broad
is no modern lineage of Cyrtacanthacridinae occurring in northern geographical distributions, we allowed a maximum of five areas
Europe, the fossil deposition site suggests that this Old World sub- for a given genus to occur within. We tested six models imple-
family (except for Schistocerca, which is discussed later) must have mented in the program: 1) DEC (dispersal-extinction-cladogenesis)
had a broader distribution in the Eocene than today. The second (Ree et al. 2005); 2) DEC+J (including founder-event speciation);
3) DIVALIKE, a likelihood version of DIVA (dispersal-vicariance) (Fig. 2). For the total evidence dataset, the resulting relationships
(Ronquist 1997); 4) DIVALIKE+J (including founder-event specia- were also largely congruent between the two analyses, but in the
tion); 5) BAYAREALIKE, a likelihood version of the Bayesian infer- Bayesian tree (not shown, available at Mendeley), the positions of
ence of historical biogeography for discrete areas (BayArea) (Landis some of the smaller clades, which had low bootstrap support (<50)
et al. 2013); and, 6) BAYAREALIKE+J (including founder-event in the ML tree (Fig. 3), were not fully resolved. Between the back-
speciation). These six models included two parameters: d = dispersal bone trees and the total evidence trees in both inference methods,
and e = extinction. Likelihood values of these models were compared the majority of backbone relationships were preserved in the total
using a likelihood ratio test and we used the Akaike Information evidence trees and the taxa with lots of missing data (those with-
Criterion (AIC) to directly compare how well the different models fit out mtgenome sequenced) were placed in the expected positions
the data (Matzke 2013, 2014). in the backbone topology. The clade that had different positions

between the inference methods in the backbone trees grouped with
Melanoplinae in the total evidence trees. The relationships among
Results
major lineages, including the placement of Acrididae in relation to
Phylogeny of Acrididae the outgroups, as well as the early divergence of the New World
We recovered monophyletic Acrididae with strong nodal support in endemic subfamilies within Acrididae, were consistent among all
both ML and BA analyses of the backbone dataset and the total analyses. In other words, there seemed to be no negative effect of
evidence dataset. For the backbone dataset, the topologies recovered missing data in this data combination strategy. Because the ML
from both analyses were mostly congruent except the clade consist- analysis resulted in a single fully resolved topology with the best
ing of Copiocera Burmeister, 1838 (Copiocerinae) and Coscineuta likelihood score (Fig. 3), even though some of the relationships were
Stål, 1873 (Proctolabinae) (Fig. 2). This clade grouped closely with supported with low bootstrap values, we base the following discus-
Oxyinae and Spathosterninae in the ML tree, but with the earliest sion on the relationships resolved by the ML total evidence analysis.
diverging lineage in the Bayesian tree. However, the nodal support In terms of outgroup relationships, we found Acrididae to be
values for the placements of this lineage were low in both analyses most closely related to Ommexechidae, Romaleidae, and Tristiridae,
Fig. 2. Phylogeny of Acrididae based on the backbone dataset inferred in ML (a) and Bayesian (b) framework. Shown in red is the relationships that are different
between ML and Bayesian analyses. Green circles on the nodes represent 100% bootstrap values in the ML tree and 100% posterior probability values in the
Bayesian tree. Values lower than 100 are shown.
Fig. 3. Phylogeny of Acrididae inferred from ML analysis. The numbers on nodes indicate bootstrap support values. Values lower than 50 are not known. Asterisk
indicates a paraphyletic group.
all of which are the New World families. These three New World of Lentulidae and Lithidiidae. Within Acrididae, we recovered four
endemic families and Acrididae collectively formed a monophyletic major clades, which we tentatively refer to as clades A, B, C, and
group, which was sister to the South African endemic clade consisting D, although the nodal support values for these clades were low
(Fig. 3). Across all analyses, the placement of clade A at the base of well-characterized subfamilies with strong support, we found that
the Acrididae phylogeny was consistent, but the relationships among paraphyly is rampant across many subfamilies. This finding high-
the remaining three clades were unclear. The earliest diverging clade lights that the current classification has been affected by inadequate
(clade A, green in Fig. 3) consisted of the Central and South American subfamily definitions and calls for the urgent need to revise the tax-
endemic subfamilies: Marelliinae, Pauliniinae, Ommatolampidinae, onomy of Acrididae as a whole.
Leptysminae, and Rhytidochrotinae. Ommatolampidinae was Although the family concept of Acrididae has been used since
found to be largely paraphyletic. The two monotypic subfamilies, the 19th century, the formal definition of what constitutes the fam-
Marelliinae and Pauliniinae, formed a clade, which represented the ily has never been clearly made because different authors relied on
earliest diverging lineage within clade A. The second clade (clade different characters for recognizing the family (Dirsh 1975, Xia
B, red in Fig. 3) consisted of the Old World subfamilies (one rep- 1994, Eades 2000). In fact, there are no external characters whose

resentative each of Hemiacridinae, Tropidopolinae, Coptacrinae [= presence define the family (Rowell 2013). As mentioned previously,
Coptacridinae], one representative of Catantopinae) and the cosmo- the only morphological character that has been suggested to unite
politan subfamilies (Acridinae, Gomphocerinae, and Oedipodinae). all family members is the presence of a well-developed arch scler-
Hemiacridinae and Catantopinae were paraphyletic because other ite in the male phallic complex (Eades 2000), which is a difficult
members of these subfamilies were found in other clades. Acridinae, character to observe for untrained eyes and without careful dissec-
Gomphocerinae, and Oedipodinae collectively formed a monophy- tion. Nevertheless, the fact that we have recovered the monophy-
letic group, which was consistently found in all analyses, but each letic Acrididae strongly suggests that this obscure genital character
subfamily was paraphyletic within. may indeed be a synapomorphy for the family. Amedegnato (1977)
The third clade (clade C, blue in Fig. 3) consisted of three Old also suggested the preapical diverticulum of the female spermatheca
World subfamilies (Hemiacridinae, Oxyinae, and Spathosterninae), could be a diagnostic feature for Acrididae, but because her work
two Neotropical subfamilies (Copiocerinae and Proctolabinae), focused only on the Neotropical taxa, it is not clear how applicable
and one cosmopolitan subfamily (Melanoplinae). Hemiacridinae this trait might be to other Old World taxa.
and Copiocerinae were paraphyletic. Spathosterninae was nested Due to the lack of obvious morphological characters that can be
within Oxyinae, rendering Oxyinae paraphyletic. Proctolabinae used to distinguish Acrididae from other related families, several cur-
and Melanoplinae were the only monophyletic groups in this rently recognized families were previously considered as members of
clade and Melanoplinae was found to be closely related to Proctolabine Acrididae. For example, Dirsh (1975) considered the South American
and Copiocerinae. The fourth clade (clade D, orange in Fig. 3) endemic Tristiridae and the South African endemic Lithidiidae
consisted of the Old World subfamilies (Eyprepocnemidinae, to be closely related to the acridid subfamily Hemiacridinae
Calliptaminae, Euryphyminae, and Catantopinae) and one cosmo- (Hemiacrididae in his concept). These two families, however, have
politan subfamily (Cyrtacantharidinae). Of these, Catantopinae since been shown to be quite divergent from Acrididae and repre-
was the only paraphyletic group, and all other subfamilies were sent lineages that diverged much earlier than Acrididae (Leavitt et al.
found to be monophyletic. Eyprepocnemidinae, Calliptaminae, and 2013, Song et al. 2015). The family Romaleidae is still sometimes
Euryphyminae collectively formed a strongly supported clade. regarded as part of Acrididae (Capinera et al. 2004, Johnson and
Triplehorn 2005), but our study finds that it is a closely related but
Divergence Time Estimate and Biogeography distinctly different family. Romaleidae can be morphologically dis-
The time-calibrated tree estimated from the BEAST analysis tinguished from Acrididae by the sclerites of the aedeagus, which
(Fig. 4) indicated that Acrididae originated in the Paleocene are derived from posterior prolongations of the endophallic plates,
of the Cenozoic period (59.3 MYA). The BioGeoBEARS ana- and the absence of the arch sclerite of the male phallic complex
lysis suggested BAYAREALIKE+J to be the best-fit model for our (Amedegnato 1977, Eades 2000, Rowell 2013).
data (LnL = −307.0228), allowing us to infer that the diversi- The two most recent studies that investigated the phylogenetic
fication of the family can be characterized as a series of founder relationships of Acrididae to other families used mtgenome data
events with subsequent radiation (Fig. 5). We found that the com- (Leavitt et al. 2013, Song et al. 2015) and our present phylogeny
mon ancestor of the South American endemic families (Tristiridae, essentially used the same outgroup taxon sampling. Regardless of
Romaleidae, and Ommexechidae) and Acrididae diverged from their the scope of each study, the consistent pattern resulting from the
African relatives (Pamphagidae, Pamphagodidae, Lentulidae, and mtgenome data is that Acrididae forms a monophyletic group
Lithidiidae) in the late Cretaceous. Soon after the K/T boundary, with Ommexechidae and Romaleidae, which in turn is sister to
Acrididae diverged from Ommexechidae and started to diversify Tristiridae. This relationship is significant because the closest liv-
in northern South America, giving rise to Marelliinae, Pauliniinae, ing relatives of Acrididae are all endemic to South America, which
Ommatolampidinae, Leptysminae, and Rhytidochrotinae (clade supports the possibility of Acrididae originating in this region. We
A). The analysis also suggested that the common ancestor of the expand on this finding in the next section on biogeography. The
remaining subfamilies colonized Africa in the late Paleocene, radi- common ancestor of Acrididae, Ommexechidae, and Romaleidae
ated throughout Africa and progressively colonized the Palearctic diverged from the ancestral Tristiridae in the late Cretaceous period.
and Oriental regions. Subsequently, several lineages recolonized the The common ancestor of these four families diverged from the Old
New World multiple times. World endemic lineage, including Lentulidae and Lithidiidae, prob-
ably due to variance.
Discussion
Major Clades Within the Phylogeny of Acrididae
Phylogenetic Relationships of Acrididae to Other Although there have been several phylogenetic hypotheses of acridid
Families grasshoppers at the subfamily level (Chapco et al. 2001, Litzenberger
Our study represents the first modern phylogenetic hypothesis of and Chapco 2001, Amédégnato et al. 2003, Litzenberger and Chapco
Acrididae based on a large taxon and molecular character sampling. 2003, Rowell and Flook 2004, Bugrov et al. 2006, Contreras and
While we recovered the monophyly of Acrididae as well as several Chapco 2006, Fries et al. 2007, Song and Wenzel 2008, Chapco and
Fig. 4. A time-calibrated phylogeny of Acrididae based on three fossil calibration points using BEAST. Posterior probability values are shown as colored circles
(yellow: 96–100%, orange: 90–95%, red: 80–89%, below 79% not shown). Green bar indicates 95% HPD for a time estimate. Asterisk indicates a paraphyletic
group. (a) Marellia remipes Uvarov, 1929 (Marelliinae); (b) Paulinia acuminata (De Geer, 1773) (Pauliniinae); (c) Tucayaca parvula Roberts, 1977 (Leptysminae);
(d) Trichopaon tatei (Hebard, 1924) (Rhytidochrotinae); (e) Ommatolampis perspicillata (Johannson, 1763) (Ommatolampidinae); (f) Homoxyrrhepes punctipennis
(Walker, 1870) (Tropidopolinae); (g) Eucoptacra anguliflava (Karsch, 1893) (Coptacrinae); (h) Acanthoxia gladiator (Westwood, 1841) (Hemiacridinae);
(i) Uvarovium dirshi Uvarov, 1933 (Hemiacridinae); (j) Truxalis robusta (Uvarov, 1916) (Acridinae); (k) Mermiria picta (Walker, 1870) (Gomphocerinae);
(l) Amblytropidia mysteca (Saussure, 1861) (Gomphocerinae); (m) Oedipoda miniata (Pallas, 1771) (Oedipodinae); (n) Oxya japonica (Thunberg, 1815) (Oxyinae);
(o) Spathosternum pygmaeum Karsch, 1893 (Spathosterninae); (p) Adimantus ornatissimus (Burmeister, 1838) (Copiocerinae); (q) Proctolabus brachypterus
Bruner, 1908 (Proctolabinae); (r) Melanoplus sanguinipes (Fabricius, 1798) (Melanoplinae); (s) Eyprepocnemis plorans (Charpentier, 1825) (Eyprepocneminae);
(t) Calliptamus italicus (Linnaeus, 1758) (Calliptaminae); (u) Euryphymus haematopus (Linnaeus, 1758) (Euryphyminae); (v) Oxycatantops spissus (Walker,
1870) (Catantopinae); (w) Cyrtacanthacris tatarica (Linnaeus, 1758) (Cyrtacanthacridinae); (x) Eumecistes gratiosus Brančik, 1896 (Catantopinae).
Fig. 5. Biogeographical histories of different lineages of Acrididae as inferred by BioGeoBEARS. Each terminal is a genus, and the colored squares indicate
where the species in the genus are currently distributed, as defined by six biogeographical realms. The colored circles on the nodes represent the probabilities
of each possible geographical range just before and after each speciation event. Some of the colored circles do not match with one of the six pre-defined colors
for the six biogeographical realms, which show ambiguity in the ancestral distribution. Orange represents either Ethiopian (yellow) or Oriental (red), and olive
green represents either Ethiopian (yellow), Oriental (red), or Palearctic (green). Major biogeographical events are indicated by the arrows on specific nodes, and
the recolonization of the New World (NW) from the Old World (OW) by various lineages is indicated by OW→NW. The colored maps next to each clade show
general hypothesized patterns of dispersals and colonization events for the subfamilies within each clade. A star represents the origin of Acrididae in South
America. Black circles represent a likely area where the most recent common ancestor of each clade could have originated. Thick arrows indicate likely paths of
colonization by major lineages, and thin arrows represent likely paths of colonization by lower taxonomic units (e.g., genus). Dotted arrows indicate possible
dispersal events between the Old World and the New World.
Contreras 2011, Chintauan-Marquier et al. 2011, Li et al. 2011, acridid lineages has remained unclear. Our study found that Paulinia
Nattier et al. 2011), our study represents the first attempt to eluci- and Marellia form a well-supported clade, which instead suggests
date phylogenetic relationships among major subfamilies across the that their similar external morphology and unusual biology are, in
entire family. We found eight out of 21 subfamilies included in this fact, due to shared ancestry. However, we also found that the two
analysis to be paraphyletic: Acridinae, Catantopinae, Copiocerinae, lineages diverged in the Eocene, which means that there was ample
Gomphocerinae, Hemiacridinae, Oedipodinae, Ommatolampidinae, time for each lineage to accumulate species-specific traits that might
and Oxyinae. Most of these paraphyletic groupings are to be have confused earlier taxonomists.
expected because these subfamilies have either not been clearly Prior to 1974, all grasshopper species with the prosternal pro-
defined or used as taxonomic dumping grounds by previous tax- cess were artificially grouped into Catantopinae, which was occa-
onomists (Dirsh 1975, Grunshaw 1996, Eades 2000, Chapco and sionally elevated to the level of family (Dirsh 1961). This structure

Contreras 2011, Rowell and Hemp 2017). Although more than one- is, however, present in all known subfamilies except Acridinae,
third of the acridid subfamilies are paraphyletic, we have neverthe- Gomphocerinae, and Oedipodinae, and also present in Romaleidae,
less recovered four major clades, which we tentatively call clades Ommexechidae, and Tristiridae, as well as other Old World fami-
A, B, C, and D (Figs. 3 and 4). The relationships within each of lies. This suggests that it is a plesiomorphic character and cannot be
these clades corroborate well with morphology and previous stud- used as a diagnostic character for any one group within Acrididae.
ies focusing on subfamilies (Amedegnato 1977, Eades 2000). One Amedegnato (1974) reclassified Neotropical grasshoppers based on
caveat is that the nodal support values for clades B, C, and D, espe- a detailed examination of male and female genitalia and recognized
cially the bootstrap support values from the ML analysis, are not six subfamilies that used to be classified as Catantopinae. Of these
strong (below 50), which we think is related to our character sam- six subfamilies, she considered Leptysminae, Rhytidochrotinae,
pling that included a large number of missing data for those taxa and Ommatolampidinae to form a clade (Amedegnato 1977),
without sequenced mtgenomes, although this did not have any effect and our study also recovered these three subfamilies as a clade,
on phylogenetic reconstruction. Thus, we discuss the higher relation- although Ommatolampidinae was found to be paraphyletic. While
ships among these clades very little, and the following discussions Leptysminae and Rhytidochrotinae are defined by vertically hooked
should be viewed with some caution. Below, we present an in-depth male cerci (Roberts and Carbonell 1980) and by a short pronotum
discussion of the recovered relationships, along with commentary and reduced aedeagus, respectively (Descamps and Amédégnato
about our study’s implications for the evolution of grasshoppers in 1972), Ommatolampidinae is only defined as one of the Neotropical
light of our phylogenetic analyses (Fig. 3) and the time-calibrated Acrididae with the prosternal process and a simple spermatheca
tree (Fig. 4). Because many of the subfamilies may be unfamiliar to (both of which the other two subfamilies have too), and without
the average readers, we also take this opportunity to highlight the the defining features of Leptysminae and Rhytidochrotinae (Rowell
diverse biology and ecology of each subfamily. 2013). Therefore, without any unique morphological characters of
its own, it is not surprising that Ommatolampidinae was rendered
Clade A paraphyletic in our phylogeny.
The earliest diverging lineage within Acrididae is clade A (green Leptysminae is a relatively small group with 21 genera and 79
in Figs. 3 and 4), which consists of members of two monotypic valid species, well-characterized by the vertically hooked male cerci,
subfamilies, Marelliinae and Pauliniinae, two monophyletic sub- angular lower external lobe of the hind knee, very short second tar-
families, Leptysminae, and Rhytidochrotinae, and the paraphyletic sal segment of the hind legs, and the distal portion of the endophallic
Ommatolampidinae. This clade represents the first radiation within apodemes of the aedeagus that lies in the horizontal plane (Rowell
the Neotropical region, although a few species of Leptysminae have 2013). A series of revisionary work by Roberts and Carbonell in the
reached the southern United States (such as Leptysma marginicollis 1970s placed Leptysminae as one of the best-studied Neotropical
(Serville, 1838) and Stenacris vitreipennis (Marschall, 1836)). The acridid subfamilies (Roberts 1975, 1978; Roberts and Carbonell
members of this clade are ecologically diverse and quite aberrant 1979, 1980). We included members of two major tribes, Leptysmini
compared to typical grasshoppers. The most unusual case can be and Tetrataeniini, in our taxon sampling, and recovered the subfam-
demonstrated with two aquatic species in Marelliinae (Marellia ily as monophyletic, which suggests the taxonomic stability of this
remipes Uvarov, 1929) and Pauliniinae (Paulinia acuminata (De group. Leptysmines are highly adapted to semi-aquatic habitats,
Geer, 1773)). These species live on broad, floating leaves of aquatic preferring marshes or swampy areas, and feed on grasses, sedges,
plants, feeding and ovipositing on them, and their entire life cycle or broad-leaved monocots that thrive in these habitats (Rowell
takes place on these plants. Their hind femora are flat and dilated, 2013). Like many grass-feeding grasshoppers, these insects have
which help them swim underwater (Carbonell 1957). As reviewed evolved an elongated body form (Rowell 2013) and many species
in Carbonell (2000), the literature on Paulinia and Marellia suggests even have the ability to swim. Unlike typical grasshoppers that lay
an uncertainty by authors regarding their relationships with other eggs underground, leptysmines are known to engage in endophytic
acridids and their taxonomic placement. Initially, these two taxa oviposition, in which the female first bites a hole in the surface of a
were treated as the only members of the family Pauliniidae, which stem and then inserts the toothed ovipositor to oviposit inside the
Dirsh (1956) considered to be sufficiently different from Acrididae plant (Braker 1989).
based on the male phallic complex. However, Dirsh (1961) later Rhytidochrotinae is also a small group, with 20 genera and 47
commented that Marellia probably did not belong to the same group valid species, mainly distributed from Costa Rica to northern Brazil,
as Paulinia and Carbonell (2000) conducted a detailed investigation with the highest diversity in Colombia (Descamps and Amédégnato
of the internal and external morphology of both groups to suggest 1972). Except for a few genera, rhytidochrotines live in montane for-
that Pauliniidae is an artificial group at best. He further commented est (Rowell 2013). Most rhytidochrotines are completely apterous,
that the external similarities between Paulinia and Marellia could often without tympana, and have a short pronotum with exposed
be due to parallel adaptations to the aquatic habitat and not their metathoracic tergites (Descamps and Amédégnato 1972). Many
shared ancestry. Eventually, Eades (2000) erected a new subfam- species are also brilliantly colored. Unlike most other grasshop-
ily, Marelliinae, to accommodate Marellia, but its affinity to other per groups, the male genitalia of rhytidochrotines are known to be
homogeneous across species and genera with a reduced aedeagus grassland-adapted ecomorphs (such as Leptacris Walker, 1870) and
(Amedegnato 1977, Rowell 2013). The lack of tympana and the some have compressed body forms with forward-facing mandibles
lack of species-specific genitalia collectively suggest that these insects characteristic of arboreal ecomorphs (such as Pristocorypha Karsch,
probably rely on non-acoustic and non-genital courtships. Judging 1896), while others are flightless and small (such as Dirshacris
from their protuberant eyes, bright body coloration, and varied pat- Brown, 1959). As such, it is difficult to characterize what a typical
terning, it is likely that visual courtship might be the main mode of hemiacridine is.
species recognition in this group. Rhytidochrotines are also known Most species currently classified as Tropidopolinae prefer long
to feed on ferns (Rowell et al. 1983, Rowell 2013), which is quite grass savanna in Africa and have elongated body forms mimicking
unusual among grasshoppers. Another acridid subfamily that mainly grasses (Rowell and Hemp 2017). In our phylogeny, the single rep-
feeds on aquatic ferns is Pauliniinae (Carbonell 2000) while other resentative of tropidopoline Petamella Giglio-Tos, 1907 grouped

non-acridid fern-feeders belong to Eumastacoidea (Rowell 2013), an with the hemiacridine Leptacris, which suggests that there is a need
ancient lineage that originated in the Jurassic (Song et al. 2015). The to re-classify these two subfamilies. Near the base of clade B, we
association between eumastacoids and ferns makes sense due to their recovered Coptacrinae (20 genera, 116 species) as monophyletic,
antiquity, but the association of rhytidochrotines (and pauliniines) which is characterized by the presence of furculae, an elongated
with ferns must have evolved more recently because modern grass- and tapered supra-anal plate, and subgenital plate with a trans-
hoppers essentially diversified in the Cenozoic. Rowell et al. (1983) verse fold (Rowell and Hemp 2017). The members of this subfam-
tested the feeding preference of a rhytidochrotine, Hylopedetes ily prefer open savanna, savanna woodlands, and forest edges, and
nigrithorax Descamps & Rowell, 1978, from Costa Rica, and found are known to feed on herbaceous plants, with some species spe-
that it specializes on several species of ferns regardless of the second- cializing on Asteraceae (Johnsen 1982, Rowell and Hemp 2017).
ary chemicals produced by the ferns. So, this is an interesting case of Not much is known about the biology of this group but many
a young insect lineage associating with an old plant lineage. Whether species are brachypterous and quite colorful, reminiscent of the
these species can metabolize the plant chemicals (phenols and tan- Ommatolampidinae in the New World.
nins) to use for their protection is unknown. Traulia Stål, 1873 is the only member of Catantopinae repre-
Ommatolampidinae is the largest subfamily in clade A with sented in clade B and all other catantopines included in this ana-
114 genera and 292 valid species and it is rendered paraphyletic lysis are clustered in clade D (orange clade in Figs. 3 and 4), which
in our study. It is a heterogeneous Neotropical group distributed makes its position questionable. This genus has been classified as
from Mexico to South America and Hispaniola. This subfam- Catantopinae because of the presence of the prosternal process,
ily includes morphologically and ecologically diverse species, such but previous phylogenetic studies that included Traulia consist-
as the cryptic and geophilous Vilerna Stål, 1873, moss-mimicking ently found that this genus did not cluster with other catantopines.
Nicarchus Stål, 1878, leaf-litter-inhabiting Microtylopteryx Rehn, For example, Liu et al. (2008) found this genus to group with
1905, canopy-dwelling Anablysis Gerstaecker, 1889, as well as Acridinae and Gomphocerinae based on mitochondrial rRNA and
typical-looking Abracris Walker, 1870. Accordingly, there is great Chapco (2013) suggested that the phylogenetic position of Traulia
diversity in feeding habits and mode of oviposition among omma- was unclear based on his analysis using four mitochondrial genes.
tolampidines (Rowell 2013). There are several well-characterized Morphologically, Eades (2000) questioned the placement of Traulia
tribes within this subfamily, but the relationships among them are in Catantopinae because its phallic structures show resemblance
unclear. Our analysis included members of Syntomacrini, Abracrini, to members of Oedipodinae rather than other catantopines. In our
and Ommatolampidini, and recovered monophyly for the first ML tree, Traulia is at the base of the clade consisting of Acridinae,
two tribes. However, these tribes do not form a clade, but, rather, Gomphocerinae, and Oedipodinae. Therefore, all evidence seems to
are intermingled with Leptysminae and Rhytidochrotinae. In fact, suggest that this genus needs to be reclassified and a more in-depth
Amédégnato and Poulain (1998) speculated that Leptysminae study is necessary to resolve the relationship between Traulia and
and Rhytidochrotinae could have diverged from one stem of the these three subfamilies, which do not possess the prosternal process.
Ommatolampidinae, which seems to fit the pattern we have recov- The clade consisting of Acridinae, Gomphocerinae, and
ered. Thus, it may be possible in the future to erect more groupings Oedipodinae collectively represents the largest radiation within
that are based on our phylogeny, or synonymize Leptysminae and Acrididae, including more than 2,500 valid species (over 37% of
Rhytidochrotinae with Ommatolampidinae. total acridid diversity) (Cigliano et al. 2018). The members of this
clade can produce sound either by stridulation (produced by rubbing
Clade B their hind legs against the forewings) or crepitation (produced by
Clade B (red in Figs. 3 and 4) consists of members of the Old snapping wings when they fold and unfold) (Otte 1981). Their high
World subfamilies: Catantopinae, Coptacrinae, Hemiacridinae, numbers of species, combined with worldwide distribution and com-
Tropidopolinae, and a clade consisting of three cosmopolitan sub- mon association with grasslands, is why they are the most familiar
families without the prosternal process: Acridinae, Gomphocerinae, members of Acrididae to the general public. Simultaneously, though,
and Oedipodinae. Out of the four major clades recovered in our they are also the most controversial group taxonomically as numer-
study, this clade seems to be the most unstable taxonomically since ous authors have struggled to define what constitutes each subfamily
paraphyly is quite rampant. Because our taxon sampling for the Old (Rehn and Grant 1960, Jago 1971). During the early half of the
World subfamilies in this clade was limited, it is difficult to make 20th century, the only distinguishing feature between Acridinae and
too much inference about them at this point, other than their place- Oedipodinae (the concept Gomphocerinae was formalized much
ment in this clade. Both Hemiacridinae (38 genera, 121 species) and later) was the degree of facial angle, which is at an oblique angle in
Tropidopolinae (11 genera, 34 species) are taxonomically ill-defined. acridines and a vertical angle in oedipodines (Uvarov 1941).
Hemiacridinae, in particular, currently includes morphologically However, Uvarov (1941) expressed an opinion that the degree
diverse genera that have been placed in this subfamily without a of facial angle is highly variable and is not a suitable trait to define
clear justification (Rowell and Hemp 2017). For example, some a subfamily, instead suggesting that the morphological adapta-
hemiacridine genera have elongated body forms characteristic of tions that allow sound production should be the main characters
to distinguish these groups. Uvarov (1941) observed that Acridinae needed, especially because this clade contains dozens of agricultur-
could be characterized by a series of pegs on a special ridge of the ally important pest species and is also biologically fascinating.
hind femur that work against the raised second radial vein, while As mentioned above, Acridinae (141 genera, 484 species) is a het-
Oedipodinae lacks this trait. Following this observation, Dirsh erogeneous group, which is currently defined by negative characters,
(1951[1950]) proposed several tribes based on this stridulatory such as the lack of the stridulatory file. In our phylogeny, Acrida
mechanism, such that Truxalini was defined by the presence of the Linnaeus, 1758 (type genus of Acridinae) and Truxalis Fabricius, 1775
stridulatory pegs along the inside of the hind femur coupled with (type genus of Truxalinae) were recovered as sisters. The close rela-
the raised medial and radial vein, and Acridini was defined by the tionship between these two genera was also recovered by Chapco and
absence of these pegs and raised veins. Although Dirsh (1951[1950]) Contreras (2011) as well. These findings also support Jago’s (1996)
observed that the species classified as Oedipodinae could be char- synonymy of Truxalinae under Acridinae. In fact, both genera have a

acterized by the presence of stridulatory intercalary veins, he never- highly slanted head, an elongated body, and strongly ensiform anten-
theless did not recognize Oedipodinae as a separate subfamily and nae, making them well-adapted for inhabiting grasslands. It appears
treated it under Acridinae. that the lack of the stridulatory file in Acrida is a loss of character. Otte
Rehn and Grant (1960) criticized the overemphasis on the strid- (1981) considered there to be only one tribe of Acridinae in the New
ulatory structures as a main taxonomic character and documented World, Hyalopterygini. In our phylogeny, Hyalopteryx Charpentier,
numerous exceptions where the strict adherence to this character 1845, the type genus for the tribe, forms a clade with Dichromorpha
would cause conflicts in taxonomy, which led to their conclusion in Morse, 1896 and Syrbula Stål, 1873, which are currently classified
recognizing only the single subfamily of Acridinae. However, Dirsh as Gomphocerinae. In Chapco and Contreras (2011), several species
(1965) ignored this criticism and placed all species with a stridulatory of Hyalopterygini formed a clade with Dichromorpha, Orphulella
file consisting of a row of pegs along the inside of the hind femora in Giglio-Tos, 1894, and Orphulina Giglio-Tos, 1894, all of which are
either Eremogryllinae (a small subfamily in North Africa, consisting of currently considered gomphocerines. These findings also collectively
two genera and five species that we did not include) or Truxalinae. All suggest that the stridulatory file has been lost and regained many times
other species were placed in Egnatiinae (another small subfamily in the throughout the diversification of Acridinae and Gomphocerinae, and
Middle East, consisting of nine genera and 36 species that we did not the current definition of each subfamily is not adequate.
include) or Acridinae (which included Oedipodinae). Uvarov (1966) Gomphocerinae (192 genera, 1,273 species) is the largest sub-
and Jago (1971) adopted a different view and recognized Truxalinae family within Acrididae and we found it to be a highly paraphyletic
sensu Dirsh that have the stridulatory file consisting of a series of peg- group intermingled with Acridinae and Oedipodinae. We have shown
like hairs as a separate subfamily, Gomphocerinae. Consequently, the that the original definition of Gomphocerinae based on the presence
definition of Truxalinae was restricted to only those species with the of stridulatory file is no longer valid. Nevertheless, the species of
stridulatory file consisting of unmodified hairs lying between peglike typical Gomphocerinae are among the best-studied grasshoppers
cuticular expansions. Uvarov (1966) reintroduced the definition of in terms of mating behavior (Faber 1929, Jacobs 1953, Otte 1970,
Oedipodinae as those without the stridulatory files on hind femora, Eisner 1974). Many species show elaborate pre-copulatory court-
but with a stridulatory file on a raised intercalary vein on the teg- ship behaviors using a combination of acoustic, vibrational, and
mina and that have a rounded-head profile. Otte (1981, 1984) took even visual signals sometimes. Nattier et al. (2011) demonstrated,
a similar approach in distinguishing the three subfamilies in North based on a phylogenetic study of gomphocerine songs, that there are
America, but also noted that the loss of stridulatory pegs appeared clades (such as Chorthippus Fieber, 1852) that include males that
to be quite common, making it difficult to separate Gomphocerinae produce highly complex and unique calling songs, and whose court-
from Acridinae. He classified the Nearctic Acridinae as those with the ship songs are very similar to calling songs. There are other clades in
forewings that are obliquely truncated at apex and male hind wings which males produce relatively simple and non-species-specific call-
with enlarged cells near leading edges. Later, Jago (1996) synonymized ing songs, but highly elaborate and multi-modal courtship songs and
Truxalinae (which has the stridulatory files) under Acridinae based on displays. These patterns show dynamic and rapid evolution of mat-
the morphology of the male epiphallus, which further downplayed the ing signals and behaviors, likely driven by sexual selection.
taxonomic importance of the stridulatory file. Oedipodinae (137 genera, 794 species) is commonly known as
Our phylogeny reflects this taxonomic controversy as none of the band-winged grasshoppers in North America as most species have
three subfamilies in question were recovered as monophyletic. This hind wings that are usually banded or brightly colored with yellow,
lack of monophyly has been suspected for many decades because orange, red, or blue hues, often overlaid with black or smoky bands.
there are many intermediate groups that do not neatly fit into any However, not all species have this characteristic and there are many
of the three subfamilies, such as the tribe Hyalopterygini in the other species outside of Oedipodinae that have convergently evolved
New World (Rehn and Grant 1960). Chapco and Contreras (2011) this trait. Many oedipodine grasshoppers exhibit acoustic commu-
reported the same pattern from a molecular phylogenetic study nication by crepitation, but a more prominent mode of communica-
based on a dense taxon sampling of these three subfamilies. They tion is visual, which involves hind wing color display during flight
suggested that while these subfamilies share a common ancestor, the and various types of hind leg signaling (Otte 1970), although the
current taxonomy does not correspond with the phylogeny, thereby function of hind wing color display might also be related to defense
labeling these subfamilies ‘fuzzy sets’. This pattern also extends to against visual predators. Many oedipodines are cryptically colored
tribal levels. For example, Fries et al. (2007) presented a molecular to mimic substrate coloration and prefer sandy habitats. Nymphs of
phylogeny of Oedipodinae based on mitochondrial genes in which oedipodines are known to express homochromy, the ability to change
they found that many tribes were paraphyletic and suggested that cuticular coloration to match background color during development
the current taxonomic groupings appeared to be based on largely (Rowell 1971, Edelaar et al. 2017, Peralta-Rincon et al. 2017).
convergent characters. Nattier et al. (2011) studied the phylogeny
of Gomphocerinae based on molecular data and also found many Clade C
paraphyletic tribes. The relationships we have recovered in our Clade C (blue in Figs. 3 and 4) includes the Old World subfamilies,
study highlight the taxonomic instability at all levels and a thorough Hemiacridinae and Oxyinae, both of which are recovered as para-
taxonomic and phylogenetic investigation of this clade is urgently phyletic, and Spathosterninae, represented by a single taxon, and the
New World endemic subfamilies Copiocerinae and Proctolabinae, as of phylogenetics, and all previous studies have consistently recov-
well as the large subfamily Melanoplinae, which is found through- ered it as a monophyletic group (Chapco et al. 2001, Amédégnato
out the New World and parts of Eurasia. Many species in this clade et al. 2003, Chintauan-Marquier et al. 2011, Chintauan-Marquier
are associated with herbaceous plants and some groups, such as et al. 2014, Woller et al. 2014). Among melanoplines, there is an
Oxyinae, Copiocerinae, and Proctolabinae are adapted to rainfor- enormous amount of interspecific differences in genital morphology
est habitats (Rowell 2013, Rowell and Hemp 2017) while other (Hubbell 1932, Cohn and Cantrall 1974), primarily in males, but
groups within Oxyinae and Melanoplinae appear to be secondarily females in some genera also show species-specific differences in geni-
associated with grasslands. Brachyptery appears to be common in talia (Cigliano and Ronderos 1994). Melanoplines do not exhibit
this clade and many species have independently adapted to alpine any pre-copulatory courtship behavior, such as visual or acoustic.
habitats (Knowles 2001, Cigliano and Amédégnato 2010, Tatarnic Instead, mating behavior appears to be coercive, in which males

et al. 2013, Pocco et al. 2015). As mentioned above, Hemiacridinae stealthily approach and jump onto females to initiate copulation
is an artificial group at best. While it is not a natural group, previ- (Otte 1970). A recent study by Woller and Song (2017) examined
ous taxonomists have suggested that some species classified under the internal morphology of copulation in Melanoplus rotundipennis
Hemiacridinae may be closely related to Oxyinae (37 genera, 307 spe- (Scudder, 1878) using micro-CT technology and clarified the func-
cies) (Rowell and Hemp 2017). The presence of a radial area bearing tion of many genital components in both males and females. Most
a series of transverse stridulatory veinlets in the tegmina of males has species in the subfamily live in grasslands and compete with graz-
been used as a main feature for characterizing Hemiacridinae (Dirsh ing livestock, and some species have considerable economic impor-
1975). Some species in Oxyinae also have this modification in wing tance in North American rangelands and South American grasslands
venation (Rowell and Hemp 2017) and some hemiacridine species (Pfadt 1988, Cigliano et al. 2002). Many species of melanoplines
have the bridge of epiphallus split in half, a condition that is found in are also adapted to alpine habitats in South America in the Andes
all Oxyinae members (Hollis 1975). Spathosterninae (three genera, (Cigliano and Amédégnato 2010, Pocco et al. 2015, Scattolini et al.
12 species), a small subfamily with three known genera, has also 2018) and North America in the Rockies (Knowles 2001).
been attached to Oxyinae or Hemiacridinae because it has similar
stridulatory veinlets on the tegmina (Dirsh 1975). Thus, it appears Clade D
that at least some members of Hemiacridinae, Spathosterninae, and Clade D (orange in Figs. 3 and 4) represents a group of morpho-
Oxyinae might collectively form a natural group. logically well-differentiated subfamilies that have diversified in the
Copiocerinae, Proctolabinae, and Melanoplinae collectively form Old World. Except for the paraphyletic Catantopinae, the four other
a clade, although Copiocerinae was found to be paraphyletic in our subfamilies included in this clade were shown to be monophyletic
study. The close relationship of these three subfamilies was originally with strong nodal support. In our phylogeny, this clade is divided
postulated by Amedegnato (1977) who established these subfamilies into two smaller clades: 1) Eyprepocnemidinae, Calliptaminae, and
based on shared morphological characters, such as a long vermiform Euryphyminae; 2) Cyrtacanthacridinae and Catantopinae.
preapical diverticulum of the spermatheca, laterally compressed Eyprepocnemidinae, Calliptaminae, and Euryphyminae have
anterior sclerites of the endophallus, and a cup-like male subgeni- been consistently shown to have affinities to each other based on
tal plate. Although our taxon sampling was small, especially for morphology (Dirsh 1975, Rowell and Hemp 2017), but our study
Copiocerinae and Proctolabinae, the resulting topology is congru- is the first to clearly propose that they constitute a monophyletic
ent with the hypothesis based on morphology. Amedegnato (1977), lineage. Not much is known about the biology of the species belong-
as well as Rowell and Flook (2004), suggested that Copiocerinae ing to these subfamilies except for agriculturally important species,
is more closely related to Proctolabinae than Melanoplinae, and such as the Italian locust (Calliptamus italicus (Linnaeus, 1758))
our analyses confirm this idea. Copiocerinae (21 genera, 82 species) and several minor pest species in Eyprepocnemidinae (COPR
is a Neotropical subfamily found from Mexico to South America, 1982). Most species appear to be associated with shrublands or
but the subfamily is not well-defined and does not seem to have woodlands, and several species can be characterized as geophil-
a distinguishing characteristic other than a transverse groove that ous, often being associated with bare soil. Although each subfamily
separates the vertex from the fastigium on the head. Rowell (2013) has a distinct set of morphology that defines them, the grasshop-
commented that the boundaries of the subfamily are not clear, hint- pers in this group have somewhat enlarged eyes, hind wings that
ing at the possibility of paraphyly. Ecologically, copiocerines are are often colored, and hind legs that are often brightly colored (at
known to specialize on rainforest palms, which is quite unusual for least on the inner portion). In our phylogeny, Calliptaminae and
grasshoppers (Rowell 2013). Proctolabinae (29 genera, 214 spe- Euryphyminae are shown to be more closely related to each other
cies), on the other hand, is a more distinct subfamily, characterized than to Eyprepocnemidinae. Both calliptamines and euryphymines
by a thickened transverse ridge bounding the tip of the fastigium, are small in size and cryptic in coloration, resembling soil, and often
elongated second tarsal segment on hind legs, and several characters feed on woody plants. In a way, their general coloration is quite
from the male genitalia (Amedegnato 1977), and its monophyly was reminiscent of many oedipodines. Calliptaminae (12 genera, 93 spe-
well-supported by a previous molecular study (Rowell and Flook cies) is easily characterized by the pincer-like male cerci, which are
2004) as well as hypotheses based on morphology (Descamps 1976, elongated and strongly incurved. The function of these exaggerated
Amedegnato 1977). Proctolabines live in wet forest and many are cerci is unknown, but they are possibly used for holding females
arboreal while others, mostly brachypterous species, are found on during copulation. Interestingly, the epiphallus in calliptamines does
woody forbs and shrubs. Many proctolabines are specialist herbi- not possess lophi, which function as grasping organs in other grass-
vores on Solanaceae and Asteraceae in the Neotropics and engage in hopper species (Randell 1963, Dirsh 1973, Woller and Song 2017).
endophytic or epiphyllic oviposition on host plants (Rowell 2013). It is possible that the elaboration of male cerci corresponds with the
Melanoplinae (146 genera, 1,172 species) is the largest subfamily reduction of lophi. The closely related Euryphyminae (23 genera,
in the New World, which is well-characterized by a thick pallium and 87 species) is mostly confined to southern Africa and is character-
species-specific male cerci and phallic complex. Of all grasshopper ized by male cerci with large basal articulation and strongly scler-
subfamilies, Melanoplinae has received the most attention in terms otized supra-anal plate. Unlike calliptamines, euryphymines have
well-developed lophi. Furthermore, the epiphallus is divided in the in this study are all restricted to the Old World and none of the
middle, similar to those observed in Oxyinae (Dirsh 1973, Rowell species belonging to these Old World families shows any morpho-
and Hemp 2017). Eyprepocnemidinae (26 genera, 159 species) is logical affinity to Acrididae. The earlier study by Flook and Rowell
the most diverse group among the three subfamilies, and is char- (1997) that grouped Proctolabinae (New World endemic subfamily
acterized by a flat dorsum of pronotum, downcurved male cerci, of Acrididae) with the Old World family Pamphagidae is most likely
and articulated ancorae of epiphallus. Most eyprepocnemidines are due to the small molecular character sampling (930 bp from mito-
associated with woodlands or forests, but some species are known chondrial rRNAs) and sparse taxon sampling that did not include
to be pests of economic importance (COPR 1982). any of the New World endemic families. Even the authors mentioned
The subfamily Catantopinae (341 genera, 1,077 species) used that this relationship was very unexpected because the relationship
to be a catch-all group to include any grasshopper species with the did not make sense in terms of male genital morphology.

prosternal process, but now its definition has been reduced to any Our biogeographic analysis using BioGeoBEARS (Fig. 5)
Old World and Australian acridid species with the prosternal pro- suggests that the common ancestor of Tristiridae, Romaleidae,
cess that do not fit well with other subfamilies. Many of the catan- Ommexechidae, and Acrididae diverged from its Old World relatives
topine genera are monotypic or include a small number of species. in the late Cretaceous due to vicariance when the South American
Because its subfamily definition is not based on any distinct mor- continent separated from Africa. This common ancestor gave rise
phological feature, Catantopinae was expected to be paraphyletic, to current families within South America, which was essentially
which is what we recovered, although our taxon sampling beyond isolated until the emergence of the Isthmus of Panama, which is
Australian taxa was quite sparse. All catantopines from Australia, now estimated to have taken place about 20 MYA (Montes et al.
except Stenocatantops Dirsh, 1953 and Xenocatantops Dirsh, 1953 2015, Bacon et al. 2016), although this older date is not universally
form a monophyletic group with strong nodal support (Figs. 3 and accepted (O’Dea et al. 2016). We estimate that the Acrididae origi-
4). About 85% of Australian acridid fauna (~300 sp.) belongs to nated in the early Paleogene in South America.
Catantopinae and there is an incredible amount of morphological The earliest diverging lineage within Acrididae includes the
diversity among these Australian catantopines (Key and Colless South American endemic subfamilies Marelliinae, Pauliniinae,
1993, Rentz et al. 2003). The fact that morphologically diverse spe- Ommatolapidinae, Leptysminae, and Rhytidochrotinae. With the
cies confined within Australia form a clade suggests major adaptive exception of Rhytidochrotinae, which is mostly distributed in the
radiation, equivalent to the radiation of marsupials. montane forests of Colombia (Descamps and Amédégnato 1972),
The subfamily Cyrtacanthacridinae (37 genera, 165 species) the remaining subfamilies are widely distributed in the Amazon
includes some of the largest grasshoppers, which also possess some basin and northern South America, with some later expanding
of the strongest flying capabilities, giving them their common name their range up to Central America. This distribution appears to be
of bird-wing grasshoppers. The group is well-defined by rectangu- related to what has been called the ‘pan-Amazonian’ region (Hoorn
lar mesosternal lobes and its monophyly has been supported previ- et al. 2010), a large region that included the present-day Amazon,
ously based on a morphological phylogeny (Song and Wenzel 2008), Orinoco, Magdalena drainage basins, and Paraná river during the
as well as the current study. This subfamily includes some of the Paleogene. This vast area was characterized by the diverse fauna that
most economically important locust species in the world, such as existed there, elements of which are now restricted to Amazonia.
the desert locust (Schistocerca gregaria (Forskål, 1775)), the Central Furthermore, the diversification of these subfamilies could be also
American locust (Schistocerca piceifrons (Walker, 1870)), the South associated with the large wetland of shallow lakes and swamps that
American locust (Schistocerca cancellata (Serville, 1838)), and the developed in western Amazonia, originating in parallel with the
red locust (Nomadacris septemfasciata (Serville, 1838)). intensified uplift of the Andes (late middle Miocene) (Hoorn et al.
2010). These new aquatic environments, the ‘Pebas system’, may
have favored the diversification of those subfamilies associated with
Historical Biogeography of Acrididae marshy/swamp habitats, wet forests, and canopies. It is interesting
The family Acrididae as a whole has a cosmopolitan distribution. that these grasshoppers continue to be associated with the niches
Historically, many orthopterists assumed the origin of Acrididae to that their ancestors may have evolved in, rather than more typical
be Africa because there is a large diversity of other related families terrestrial and grassland habitats that most other acridids favor,
there, such as Pneumoridae, Pamphagidae, Pyrgomorphidae, and which may suggest conservation of the ancestral ecological niche
Lentulidae (Carbonell 1977, Jago 1979, Amedegnato 1993). The within this lineage.
fact that the South American grasshopper fauna was not studied During the initial diversification period within South America,
in-depth until the 1970s and that most European orthopterists ini- there appears to have been a single transatlantic colonization
tially focused on the Old World fauna probably contributed to this to Africa by the common ancestor of clades B, C, and D (Fig. 5),
thinking as well. For example, Amedegnato (1993), who extensively which took place in the early Paleogene (~57 MYA). Although South
studied South American grasshoppers, maintained that Acrididae America and Africa were already separated at that point, these two
originated in the Old World and diverged from Romaleidae due continents were closer compared to today’s configuration and dis-
to the separation of Africa and South America. However, our bio- persal across the narrowest point between the two continents could
geographical analysis, along with divergence time estimates, show have been possible. In fact, there are a number of organisms, such as
a much more dynamic pattern of diversification and radiation, and amphibians and reptiles, that display similar patterns (George and
sheds interesting new light on the evolution of these grasshoppers. Lavocat 1993). At this point in time, northern Africa was covered
Our study suggests the origin of Acrididae to be South America, with tropical rainforests, not too different from the original habi-
which is a novel hypothesis (Fig. 5). We infer this based on the mono- tats that the ancestral grasshoppers experienced in northern South
phyletic group consisting of Tristiridae (endemic to South America), America. Once in Africa, these ancestral acridids could have quickly
Romaleidae (widely distributed in South America, extending to radiated, giving rise to numerous lineages, which eventually dif-
Central and North America), Ommexechidae (endemic to South ferentiated into what we now recognize as different subfamilies.
America), and Acrididae. The other outgroups that we included However, we currently have several more subfamilies in the New
World scattered throughout the phylogeny in addition to the five habitats (Song et al. 2015). Based on pollen fossils and phytoliths,
subfamilies in clade A (green in Fig. 5). This pattern suggests that Strömberg (2011) estimated that grasslands became abundant in
there must have been some recolonization events occurring from western Eurasia, North America, and southern South America during
the Old World back to the New World. Our study hypothesizes that the Eocene. Although the Acridinae-Gomphocerinae-Oedipodinae
there were at least three distinct waves of recolonization throughout clade as a whole is cosmopolitan, more than 70% of its diversity
the diversification of Acrididae. (~1,790 spp.) occurs in the Palearctic (northern Africa, Europe, and
The first wave of recolonization of the New World was likely temperate Asia) and the Ethiopian (sub-Saharan Africa) region, with
to be a westward transatlantic colonization by the common ances- the former region containing more than 48% of the diversity. This
tor of Copiocerinae, Proctolabinae, and Melanoplinae that took pattern of diversity, coupled with our biogeographical analysis and
place in the early Eocene. It is not clear how this common ancestor the diversification of grasslands, strongly suggest that this group

could have recolonized South America from Africa, but the distance originated in the Palearctic region, from which different lineages
between the two continents was still narrow enough for an unusual expanded their ranges, colonizing new regions. Furthermore, sex-
westward dispersal to have taken place. Upon arrival, probably to ual selection on songs produced by stridulation or crepitation could
northern South America, this common ancestor gave rise to what have played another important role in promoting rapid speciation in
would eventually become the three subfamilies. Many proctolabines this clade. Our analysis indicated that there were numerous recolon-
are known to be associated with the plant family Solanaceae (Rowell ization events from the Old World to the New World throughout the
1978, 2013). The origin of Solanaceae has recently been hypoth- diversification of this clade (Fig. 5). The relative paucity of this clade
esized to be in the Eocene (Särkinen et al. 2013) and this family has in the Neotropics (only 6.5% of the diversity) seems to suggest that
great diversity in the Neotropics, which provides some support for the main routes of recolonization were probably from Eurasia to
the diversification of Proctolabinae. Compared to Copiocerinae and North America, either through the Thulean route (or dispersal flights
Proctolabinae, which are relatively small endemic subfamilies con- across Greenland) or through Beringia from eastern Eurasia to
fined to the Neotropics, Melanoplinae is a much more diverse sub- North America. Additionally, there could have been ecological fac-
family that radiated throughout South, Central, and North America, tors, such as the unsuitability of the habitats and tropical climates,
and extends to Eurasia. Many of its species are associated with either which might have prevented the colonization of the Neotropics.
grasslands or alpine habitats. Amédégnato et al. (2003) conducted The third wave of recolonization of the New World occurred
a molecular phylogenetic analysis of Melanoplinae and included in the Old World subfamily Cyrtacanthacridinae. The genus
the tribes Melanoplini (North America), Podismini (Eurasia), Schistocerca Stål, 1873 is the only genus in this subfamily that has
Dichroplini (South America), and Jivarini (South America). They representatives in both the Old and New Worlds, while all other
recovered basal placement of the South American tribes and put genera occur solely in the Old World (Amedegnato 1993, Song
forth a biogeographical hypothesis suggesting that the center of ori- 2004). Furthermore, within Schistocerca, the infamous desert locust
gin for this subfamily was South America, after which it diversified (S. gregaria) is the only species that occurs in Africa while the rest of
through North America and then to Eurasia. Chintauan-Marquier the genus is found throughout North, Central, and South America.
et al. (2011) found a similar biogeographical pattern, but estimated Recent molecular studies have consistently placed the desert locust
the divergence date of the subfamily to be 69 MYA, which predates at the base of the phylogeny of Schistocerca (Lovejoy et al. 2006,
our estimate of the origin of Acrididae. Woller et al. (2014) included Song et al. 2013, Song et al. 2017), which indicates that the genus
several members of Dactylotini (Central America) that were not well- originated in Africa, and its current diversity is a result of a spectacu-
represented in the previous studies and recovered the basal placement lar transatlantic colonization followed by rapid radiation. Song et al.
of Jivarini, followed by Dichroplini. Our study confirms the South (2017) estimated that the genus diverged from its relatives about 6–7
American origin of Melanoplinae and furthers the inference by sug- MYA, when the distance between Africa and South America was
gesting that the ancestral stock that gave rise to Melanoplinae and essentially identical to what it is today. In 1988, there was a large
the two other related subfamilies actually originated from Africa. swarm of desert locusts that successfully crossed the Atlantic Ocean
We estimate that the common ancestor of Melanoplinae diverged from western Africa to the West Indies (Kevan 1989, Rosenberg and
from the other two subfamilies in the early Eocene (~43 MYA), giv- Burt 1999), which suggests that such a long-distance flight could
ing rise to Jivarini and Dichroplini. Then, this ancestor expanded have been possible in the past. Taxonomically, there are two other
northward to give rise to Dactylotini and Melanoplini in North genera in the Cyrtacanthacridinae in the New World: Halmenus
America, and further expanded westward through the Behring land Scudder, 1893 in the Galapagos and Nichelius Bolívar, 1888 in
bridge to give rise to Podismini in East Eurasia. Several members Cuba. The former is a small brachypterous genus with four species
of Podismini have reached Europe and speciated in the mountain (Snodgrass 1902), but recent phylogenetic studies found the genus
ranges (Kenyeres et al. 2009), similar to how Melanoplus speciated to be closely related to two other fully winged Schistocerca spe-
in the Rocky Mountains in North America (Knowles 2001). The ori- cies in the Galapagos (Lovejoy et al. 2006, Song et al. 2013, Song
gin of the Jivarini, which is exclusively distributed in the Central et al. 2017). This suggests that Halmenus is simply a brachypterous
Andes (Cigliano and Amédégnato 2010), coincides with the first Schistocerca, and currently, we are planning a taxonomic revision
uplift of this geological feature, which slowly developed from the to synonymize Halmenus with Schistocerca to reflect this finding.
mid- Eocene and reached a peak in the Late Oligocene and Early Nichelius is only known from the type series of three specimens and
Miocene (~23 MYA) (Gregory-Wodzicki 2000, Garzione et al. 2008, has not been collected during the past 100 yr (Amedegnato 1993).
Hoorn et al. 2010). So, the highlands of the Andes may have served The type specimens look suspiciously similar to Schistocerca, so it is
as a migration route for Melanoplinae toward North America. quite possible that it might be an aberrant member of Schistocerca.
The second wave of recolonization of the New World was Therefore, it is possible to postulate that there was indeed a single
achieved by several lineages within the Acridinae-Gomphocerinae- transatlantic colonization by the ancestral Schistocerca, which gave
Oedipodinae complex. This clade is specifically associated with rise to the current diversity in the New World.
graminivory (Uvarov 1966, Pfadt 1988) and its diversification closely In Australia, we find perhaps the most dramatic adaptive radia-
corresponds to the evolution and expansion of grasslands and open tion among all grasshopper lineages. Our biogeographical analysis
suggests that there was a single colonization event by the common Science Foundation (grant numbers DEB-1064082 and IOS-1253493 to H.S.)
ancestor of a lineage within Catantopinae that entered Australia in and the US Department of Agriculture (Hatch Grant TEX0-1-6584 to H.S).
the mid-to-late Eocene. By the middle Eocene, Australia was already
an isolated island without any major connections to other landmasses. References Cited
When the ancestral catantopine arrived in Australia, it must have
Amedegnato, C. 1974. Les genres d’acridiens neotropicaux, leur classification
found vast areas of complex habitats where no other acridids had par familles, sous-familles et tribus. Acrida. 3: 193–203.
entered before. The Australian catantopines have diversified in deserts, Amedegnato, C. 1976. Structure et évolution des genitalia chez les Acrididae
grasslands, shrublands, tropical rainforests, and alpine habitats. It is et familles apparentées. Acrida. 5: 1–15.
also possible to find numerous species in this lineage that have con- Amedegnato, C. 1977. Etude des Acridoidea centre et sub americains
verged to resemble the members of other worldwide acridid sub- (Catantopinae sensu lato) anatomie des genitalia, classification, reparti-

families (Rentz et al. 2003), strongly mirroring the diversification of tion, phylogenie. PhD, L’Universite Pierre et Marie Curie. Paris, France.
marsupials from placental mammals. Australia was later colonized by Amedegnato, C. 1993. African-American relationships in the Acridians
(Insecta, Orthoptera), pp. 59–75. In W. George and R. Lavocat (eds.), The
Acridinae, Oedipodinae, Cyrtacanthacridinae, and Oxyinae, but these
Africa-South America connection. Clarendon Press, Oxford.
collectively represent only a small percentage of grasshopper diversity
Amédégnato, C., and M. Descamps. 1978. Diagnoses et signalizations
(68 spp.) on the continent compared to Catantopinae (300+ spp.).
d’Acridiens néotropicaux (Orth. Acridoidea). Acrida. 7: 29–53.
Amédégnato, C., and M. Descamps. 1979. History and phylogeny of the neo-
Concluding Remarks tropical acridid fauna. Metaleptea. 2: 1–10.
Despite the familiarity and economic importance of the Acrididae, a Amédégnato, C., and S. Poulain. 1998. New acridoid taxa from northwestern
large-scale phylogeny of this family has never been proposed until now. South America: their significance for the phylogeny and biogeography of
the family Acrididae (Orthoptera). Ann. Entomol. Soc. Am. 91: 532–548.
Our study represents a crucial step towards understanding the evolu-
Amédégnato, C., W. Chapco, and G. Litzenberger. 2003. Out of South
tion and diversification of these insects. We have recovered monophyl-
America? Additional evidence for a southern origin of melanopline grass-
etic Acrididae and proposed that the family originated in South America
hoppers. Mol. Phylogenet. Evol. 29: 115–119.
based on substantial evidence, contrary to a popular belief that its center Bacon, C. D., P. Molnar, A. Antonelli, A. J. Crawford, C. Montes, and M.
of origin is Africa. We have also shown that Acrididae diverged in the C. Vallejo-Pareja. 2016. Quaternary glaciation and the Great American
early Cenozoic and represents one of the most recently diverged lineages Biotic Interchange. Geology. 44: 375–378.
within Orthoptera, which originated in the early Permian (Song et al. Bazelet, C. S., and M. J. Samways. 2014. Habitat quality of grassland frag-
2015). Because of the relatively young age of Acrididae, we hypoth- ments affects dispersal ability of a mobile grasshopper, Ornithacris cyanea
esize that its current cosmopolitan distribution was largely achieved by (Orthoptera: Acrididae). Afr. Entomol. 22: 714–725.
dispersal followed by relatively rapid radiation in many cases. We esti- Behrensmeyer, A. K., and A. Turner. 2013. Taxonomic occurrences of Suidae
recorded in the Paleobiology Database. Fossilworks. http://fossilworks.org
mate that there have been a number of colonization and recolonization
Bei-Bienko, G. Y., and L. L. Mishchenko. 1963. Locusts and Grasshoppers of
events (three major waves) between the New World and the Old World
the U.S.S.R. and Adjacent Countries Part I, vol. 38. Zoological Institute of
throughout the diversification of Acrididae, and, thus, the current diver-
the U.S.S.R. Academy of Science, Moskva, Russia.
sity in any given region is a reflection of this complex history. Although Belovsky, G. E., and J. B. Slade. 1993. The role of vertebrate and invertebrate
we discovered several intriguing patterns, our phylogeny is admittedly predators in a grasshopper community. OIKOS. 68: 193–201.
based on less than 2% of the current diversity of Acrididae. Therefore, Bernt, M., A. Donath, F. Jühling, F. Externbrink, C. Florentz, G. Fritzsch,
there is still a lot more to discover by further resolving the phylogeny of J. Pütz, M. Middendorf, and P. F. Stadler. 2013. MITOS: improved de
Acrididae using more taxon and character sampling in the future. We novo metazoan mitochondrial genome annotation. Mol. Phylogenet. Evol.
hope that our study can be used as a solid foundation to understand the 69: 313–319.
evolution of these fascinating grasshoppers and that it will be the basis Bouckaert, R., J. Heled, D. Kühnert, T. Vaughan, C.-H. Wu, D. Xie, M.
A. Suchard, A. Rambaut, and A. J. Drummond. 2014. BEAST 2: a soft-
for future taxonomic studies.
ware platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 10:
e1003537.
Supplementary Data Bownes, A., A. King, and A. Nongogo. 2011. Published. Pre-release studies and
release of the grasshopper Cornops aquaticum in South Africa – a new bio-
Supplementary data are available at Insect Systematics and Diversity
logical control agent for water hyacinth, Eichhornia crassipes, pp. 3–13. In
online.
XIII International Symposium on Biological Control of Weeds , September
11-16, 2011, Waikoloa, Hawaii.
Braker, H. E. 1989. Evolution and ecology of oviposition on host plants by
Acknowledgments acridid grasshoppers. Biol. J. Linn. Soc. 38: 389–406.
We thank numerous collaborators who provided valuable specimens used in Bugrov, A., O. Novikova, V. Mayorov, L. Adkison, and A. Blinov. 2006.
this study: the late Christiane Amedegnato, Corinna Bazelet, Antoine Foucart, Molecular phylogeny of Palaeartic genera of Gomphocerinae grasshop-
Claudia Hemp, Taewoo Kim, Kate Umbers, and Michael Whiting. We also pers (Orthoptera, Acrididae). Syst. Entomol. 31: 362–368.
thank several colleagues who provided logistic support and expertise during Cameron, S. L. 2014. How to sequence and annotate insect mitochon-
our field expeditions: Corinna Bazelet, Stephen Cameron, Joey Mugleston, drial genomes for systematic and comparative genomics research. Syst.
Michael Samways, and You Ning Su. A large number of students have con- Entomol. 39: 400–411.
tributed to molecular data generation throughout the duration of this pro- Capinera, J. L., R. D. Scott, and T. J. Walker. 2004. Field guide to grasshop-
ject: Gabriella Alava, Grace Avecilla, Beka Buckman, James Leavitt, Matthew pers, katydids, and crickets of the United States. Cornell University Press,
Moulton, Tyler Raszick, and Steve Gotham. We thank Charlie Johnson and Ithaca, NY.
Richard Metz at Texas A&M AgriLife Research Genomics and Bioinformatics Carbonell, C. S. 1957. Observaciones Bio-Ecológicas sobre Marellia remipes
Service for the NGS data generation and data processing. The comments by Uvarov (Orthoptera, Acridoidea) en el Uruguay. Universidad de la
two anonymous reviewers significantly improved the text. Fieldwork to South Republica Facultad de Humanidades y Ciencias, Montevideo, Uruguay.
Africa and Australia was conducted by the senior author under permit num- Carbonell, C. S. 1977. Origin, evolution, and distribution of the neotropical
bers CRO 177/08CR and CRO 178/08CR (Eastern Cape) and a license num- acridomorph fauna (Orthoptera); a preliminary hypothesis. Rev. Soc.
ber SF007010 (Western Australia). This work was supported by the National Entomol. Argent. 36: 153–175.
Carbonell, C. S. 2000. Taxonomy and a study of the phallic complex, including Dirsh, V. M. 1951[1950]. Revision of the group Truxales (Orthoptera:
its muscles, of Paulinia acuminata (Acrididae, Pauliniinae) and Marellia Acrididae). Eos, Revista española de Entomología. Tomo Extra. 1950:
remipes (Acrididae, incertae sedis). J. Orthoptera Res. 9: 161–180. 119–247.
Chapco, W. 2013. A note on the molecular phylogeny of a small sample of Dirsh, V. M. 1956. The phallic complex in Acridoidea (Orthoptera) in relation
Catantopine grasshoppers. J. Orthoptera Res. 22: 15–20. to taxonomy. Trans. R. Entomol. Soc. Lond. 108: 223–356.
Chapco, W., and D. Contreras. 2011. Subfamilies Acridinae, Gomphocerinae Dirsh, V. M. 1961. A preliminary revision of the families and subfamilies of
and Oedipodinae are “fuzzy sets”: a proposal for a common African ori- Acridoidea (Orthoptera, Insecta). Bull. Br. Mus. (Nat. Hist.) Entomol. 10:
gin. J. Orthoptera Res. 20: 173–190. 351–419.
Chapco, W., G. Litzenberger, and W. R. Kuperus. 2001. A molecular biogeo- Dirsh, V. M. 1965. The African genera of Acridoidea. Cambridge University
graphic analysis of the relationship between North American melanop- Press, New York, NY.
loid grasshoppers and their Eurasian and South American relatives. Mol. Dirsh, V. M. 1973. Genital organs in Acridomorphoidea (Insecta) as taxo-

Phylogenet. Evol. 18: 460–466. nomic character. Zeitschrift für die Zoologische Systematik und
Chapman, R. F., and A. Joern (eds.). 1990. Biology of grasshoppers. John Evolutionsforschung. 11: 133–154.
Wiley & Sons, New York, NY. Dirsh, V. M. 1975. Classification of the Acridomorphoid insects. E.W. Classey
Chintauan-Marquier, I. C., S. Jordan, P. Berthier, C. Amédégnato, and Ltd., Faringdon, Oxon, United Kingdom.
F. Pompanon. 2011. Evolutionary history and taxonomy of a short-horned Eades, D. C. 2000. Evolutionary relationships of phallic structures of
grasshopper subfamily: the melanoplinae (Orthoptera: Acrididae). Mol. Acridomorpha (Orthoptera). J. Orthoptera Res. 9: 181–210.
Phylogenet. Evol. 58: 22–32. Edelaar, P., A. Baños-Villalba, G. Escudero, and C. Rodríguez-Bernal. 2017.
Chintauan-Marquier, I. C., C. Amédégnato, R. A. Nichols, F. Pompanon, Background colour matching increases with risk of predation in a colour-
P. Grandcolas, and L. Desutter-Grandcolas. 2014. Inside the Melanoplinae: changing grasshopper. Behav. Ecol. 28: 698–705.
new molecular evidence for the evolutionary history of the Eurasian Edgar, R. C. 2004. MUSCLE: multiple sequence alignment with high accuracy
Podismini (Orthoptera: Acrididae). Mol. Phylogenet. Evol. 71: 224–233. and high throughput. Nucleic Acids Res. 32: 1792–1797.
Cigliano, M. M., and C. Amédégnato. 2010. The high-Andean Jivarus Giglio- Eisner, N. 1974. Neuroethology of sound production in gomphocerine grass-
Tos (Orthoptera, Acridoidea, Melanoplinae): systematics, phylogenetic hoppers (Orthoptera, Acrididae). I. Song pattern and stridulatory move-
and biogeographic considerations. Syst. Entomol. 35: 692–721. ments. J. Comp. Physiol. A 88: 67–102.
Cigliano, M. M., and R. A. Ronderos. 1994. Revision of the South American Faber, A. 1929. Die Lautäuerungen der Orthopteren (Lauterzeugung,
grasshopper genera Leiotettix Bruner and Scotussa Giglio-Tos (Orthoptera, Lautabwandlung und deren biologische Bedeutung sowie Tonapparat der
Acrididae, Melanoplinae). T. Am. Entomol. Soc. 120: 145–180. Gradflügler). Vergleichende Untersuchungen I. Zeitschrift für Morphologie
Cigliano, M. M., M. L. de Wysiecki, and C. E. Lange. 2000. Grasshopper und Ökologie der Tiere A. 13: 745–803.
(Orthoptera: Acridoidea) species diversity in the Pampas, Argentina. Fenn, J. D., H. Song, S. L. Cameron, and M. F. Whiting. 2008. A mitochondrial
Divers. Distrib. 6: 81–91. genome phylogeny of Orthoptera (Insecta) and approaches to maximiz-
Cigliano, M. M., S. Torrusio, and M. L. de Wysiecki. 2002. Grasshopper ing phylogenetic signal found within mitochondrial genome data. Mol.
(Orthoptera: Acrididae) community composition and temporal variation Phylogenet. Evol. 49: 59–68.
in the Pampas, Argentina. J. Orthoptera Res. 11: 215–221. Flook, P. K., and C. H. F. Rowell. 1997. The phylogeny of the Caelifera
Cigliano, M. M., M. E. Pocco, and C. E. Lange. 2011. Grasshoppers of the (Insecta, Orthoptera) as deduced from mtrRNA gene sequences. Mol.
Andes: new Melanoplinae and Gomphocerinae taxa (Insecta, Orthoptera, Phylogenet. Evol. 8: 89–103.
Acrididae) from Huascarán National Park and Callejón de Huaylas, Fries, M., W. Chapco, and D. Contreras. 2007. A molecular phylogenetic
Ancash, Peru. Zoosystema. 33: 523–543. analysis of the Oedipodinae and their intercontinental relationships. J.
Cigliano, M. M., H. Braun, D. C. Eades, and D. Otte. 2018. Orthoptera Orthoptera Res. 16: 115–125.
Species File. Version 5.0/5.0. [1/8/2018]. http://Orthoptera.SpeciesFile.org. Gandar, M. V. 1982. The dynamics and trophic ecology of grasshoppers
Coetzee, J. A., M. P. Hill, M. J. Byrne, and A. Bownes. 2011. A review on the (Acridoidea) in a South African savanna. Oecologia. 54: 370–378.
biological control programmes on Eichhornia crassipes (C.Mart.) Solms Gangwere, S. K., M. C. Muralirangan, and M. Muralirangan (eds.). 1997. The
(Pontederiaceae), Salvinia molesta D.S. Mitch (Salviniaceae), Pistia strati- bionomics of grasshoppers, katydids, and their kin. CAB International,
otes L. (Araceae), Myriophyllum aquaticum (Vell.) Verdc. (Haloragaceae) New York, NY.
and Azolla filiculoides Lam. (Azollaceae) in South Africa. Afr. Entomol. Garzione, C. N., G. D. Hoke, J. C. Libarkin, S. Withers, B. MacFadden,
19: 451–468. J. Eiler, P. Ghosh, and A. Mulch. 2008. Rise of the Andes. Science. 320:
Cohn, T. J., and I. J. Cantrall. 1974. Variation and speciation in the grasshop- 1304–1307.
pers of the Conalcaeini (Orthoptera: Acrididae: Melanoplinae): the low- Gebeyehu, S., and M. J. Samways. 2002. Grasshopper assemblage response to
land forms of Western Mexico, the genus Barytettix. San Diego Society of a restored national park (Mountain Zebra National Park, South Africa).
Natural History, Memoir. 6: 1–131. Biodiversity & Conservation. 11: 283–304.
Contreras, D., and W. Chapco. 2006. Molecular phylogenetic evidence for George, W., and R. Lavocat (eds.). 1993. The Africa-South America connec-
multiple dispersal events in gomphocerine grasshoppers. J. Orthoptera tion. Clarendon Press, Oxford, United Kingdom.
Res. 15: 91–98. Gillon, Y. 1983. The invertebrates of the grass layer, pp. 289–311. In F.
COPR. 1982. The locust and grasshopper agricultural manual. Centre for Bourliere (ed.), Ecosystems of the World 13: tropical savannas. Elsevier,
Overseas Pest Research, London, United Kingdom. Amsterdam, the Netherlands.
Cullen, D. A., A. Cease, A. V. Latchininsky, A. Ayali, K. Berry, J. Buhl, R. De Gregory-Wodzicki, K. M. 2000. Uplift history of the central and northern
Keyser, B. Foquet, J. C. Hadrich, T. Matheson, et al. 2017. From molecules Andes: a review. Geol. Soc. Am. Bull. 112: 1091–1105.
to management: mechanisms and consequences of locust phase polyphen- Grunshaw, J. P. 1996. A taxonomic revision of the genus Leptacris Walker
ism. Adv. Insect Physiol. 53: 167–285. 1870 and allied genera (Orthoptera: Acrididae: Hemiacridinae). J.
Descamps, M. 1976. La faune dendrophile néotropicale I. Revue des Orthoptera Res. 5: 131–157.
Proctolabinae (Orth. Acrididae). Acrida. 5: 63–167. Guo, Z.-W., H.-C. Li, and Y.-L. Gan. 2006. Grasshopper (Orthoptera:
Descamps, M. 1978. Étude des écosystémes Guyanais III - Acridomorpha den- Acrididae) biodiversity and grassland ecosystems. Insect Sci. 13: 221–227.
drophiles [Orthoptera Caelifera]. Annales de la Société Entomologique de Hahn, C., L. Bachmann, and B. Chevreux. 2013. Reconstructing mitochon-
France. 14: 301–349. drial genomes directly from genomic next-generation sequencing reads - a
Descamps, M., and C. Amédégnato. 1972. Contribution a la faune des baiting and iterative mapping approach. Nucleic Acids Res. 41: e129.
Acridoidea de Colombie (missions M. Descamps) IV. Le groupe Ho, S. Y. W., and M. J. Phillips. 2009. Accounting for calibration uncertainty
Rhytidochrotae. Bulletin du Muséum National d’Histoire Naturelle, 3e in phylogenetic estimation of evolutionary divergence times. Syst. Biol. 58:
série. Zoologie. 65: 1057–1096. 367–380.
Hollis, D. 1975. A review of the subfamily Oxyinae (Orthoptera: Acridoidea). Lovejoy, N. R., S. P. Mullen, G. A. Sword, R. F. Chapman, and R. G. Harrison.
Bull. Br. Mus. 31: 191–234. 2006. Ancient trans-Atlantic flight explains locust biogeography: molecu-
Hoorn, C., F. P. Wesselingh, H. ter Steege, M. A. Bermudez, A. Mora, J. Sevink, lar phylogenetics of Schistocerca. Proc. R. Soc. Lond. B. 273: 767–774.
I. Sanmartin, A. Sanchez-Meseguer, C. L. Anderson, J. P. Figueiredo, et al. Matzke, N. J. 2013. Probabilistic historical biogeography: new models for
2010. Amazonia through time: Andean uplift, climate change, landscape founder-event speciation, imperfect detection, and fossils allow improved
evolution, and biodiversity. Science. 330: 927–931. accuracy and model-testing. Front. Biogeogr. 5: 242–248.
Hubbell, T. H. 1932. A revision of the Puer group of the North American Matzke, N. J. 2014. Model selection in historical biogeography reveals that
genus Melanoplus, with remarks on the taxonomic value of the concealed founder event speciation is a crucial process in island clades. Syst. Biol.
male genitalia in the Cyrtacanthacridinae (Orthoptera, Acrididae). Misc. 63: 951–970.
Publ. Mus. Zool. Univ. Mich. 23: 1–64. Miller, M. A., M. T. Holder, R. Vos, P. R. Midford, T. Liebowitz, L. Chan,
Jacobs, W. 1953. Verhaltensbiologische Studien an Feldheuschrecken. Beiheft P. Hoover, and T. Warnow. 2011. The CIPRES Portals. CIPRES. http://

1 Zeitschrift für Tierpsychologie. 1: 1–228. www.phylo.org/sub_sections/portal.
Jago, N. D. 1971. A review of the Gomphocerinae of the world with a key to Mitchell, J. E., and R. E. Pfadt. 1974. The role of grasshoppers in a short-grass
the genera (Orthoptera, Acrididae). Proc. Acad. Nat. Sci. Phil. 123: 205–343. prairie ecosystem. Environ. Entomol. 3: 358–360.
Jago, N. D. 1979. The breakup of Pangaea and prediction of numbers of subfam- Montes, C., A. Cardona, C. Jaramillo, A. Pardo, J. C. Silva, V. Valencia,
ily elements, living and extinct, in Acridoidea, pp. 139–162. In Proceedings C. Ayala, L. C. Pérez-Angel, L. A. Rodriguez-Parra, V. Ramirez, and
of 2nd Triennial Meeting Pan American Acridological Society, 21–25 July H. Niño. 2015. Middle Miocene closure of the Central American Seaway.
1979, Bozeman, MT. Science. 348: 226–229.
Jago, N. D. 1996. Song, sex and synonymy: the Palaearctic genus Acrida Mugleston, J. D., H. Song, and M. F. Whiting. 2013. A century of paraphyly:
Linnaeus (Orthoptera, Acrididae, Acridinae) and synonymy of the sub- a molecular phylogeny of katydids (Orthoptera: Tettigoniidae) supports
family Truxalinae under the subfamily Acridinae. J. Orthoptera Res. 5: multiple origins of leaf-like wings. Mol. Phylogenet. Evol. 69: 1120–1134.
125–129. Nattier, R., T. Robillard, C. Amédégnato, A. Couloux, C. Cruaud, and
Joern, A., B. J. Danner, J. D. Logan, and W. Wolesensky. 2006. Natural history L. Desutter-Grandcolas. 2011. Evolution of acoustic communication
of mass-action in predator-prey models: a case study from wolf spiders in the Gomphocerinae (Orthoptera: Caelifera: Acrididae). Zoological
and grasshoppers. Am. Midl. Nat. 156: 52–62. Scripta. 40: 479–497.
Johnsen, P. 1982. Acridoidea of Zambia 2, vol. 2. Zoological Laboratory, O’Dea, A., H. A. Lessios, A. G. Coates, R. I. Eytan, S. A. Restrepo-Moreno,
Aarhus University, Aarhus, Denmark. A. L. Cione, L. S. Collins, A. de Queiroz, D. W. Farris, R. D. Norris, et al.
Johnson, N. F., and C. A. Triplehorn. 2005. Borror and DeLong’s introduc- 2016. Formation of the Isthmus of Panama. Sci. Adv. 2: e1600883.
tion to the study of insects, 7th ed. Thompson Brooks/Cole. Belmont, CA. Otte, D. 1970. A comparative study of communicative behavior in grasshop-
Kenyeres, Z., I. S. Rácz, and Z. Varga. 2009. Endemism hot spots, core areas pers. Misc. Publ. Mus. Zool. Univ. Mich. 141: 1–168.
and disjunctions in European Orthoptera. Acta Zool. Cracov. 52B: Otte, D. 1981. The North American Grasshoppers Volume I: acididae,
189–211. Gomphocerinae and Acridinae. Harvard University Press, Cambridge,
Kevan, D. K. M. 1989. Transatlantic travelers. Antenna. 13: 12–15. MA.
Key, K. H. L. 1992. A higher classification of the Australian Acridoidea Otte, D. 1984. The North American Grasshoppers Volume II: acididae,
(Orthoptera). I. General introduction and subfamily Oxyinae. Invertebr. Oedipodinae. Harvard University Press, Cambridge, MA.
Taxon. 6: 547–551. Otte, D. 1995a. Orthoptera Species File. 4. Grasshoppers (Acridomorpha)
Key, K. H. L., and D. H. Colless. 1993. A higher classification of the Australian C. Acridoidea (part). The Orthopterists' Society and the Academy of
Acridoidea (Orthoptera). II. Subfamily Catantopinae. Invertebr. Taxon. 7: Natural Sciences of Philadelphia, Philadelphia.
89–111. Otte, D. 1995b. Orthoptera Species File. 5. Grasshoppers (Acridomorpha)
Knowles, L. L. 2001. Genealogical portraits of speciation in montane grass- D. Acridoidea (part). The Orthopterists' Society and the Academy of
hoppers (genus Melanoplus) from the sky islands of the Rocky Mountains. Natural Sciences of Philadelphia, Philadelphia.
Proc. R. Soc. London, Ser. B. 268: 319–324. Pener, M. P. 1983. Endocrine aspects of phase polymorphism in locusts,
Knowles, L. L., and C. L. Richards. 2005. Importance of genetic drift during pp. 379–394. In R. G. H. Downer and H. Laufer (eds.), Invertebrate
Pleistocene divergence as revealed by analyses of genomic variation. Mol. endocrinology, vol. 1, endocrinology of insects. Alan R. Liss Inc., New
Ecol. 14: 4023–4032. York, NY.
Landis, M. J., N. J. Matzke, B. R. Moore, and J. P. Huelsenbeck. 2013. Pener, M. P., and S. J. Simpson. 2009. Locust phase polyphenism: an update.
Bayesian analysis of biogeography when the number of areas is large. Syst. Adv. Insect Physiol. 36: 1–286.
Biol. 62: 789–804. Peralta-Rincon, J. R., G. Escudero, and P. Edelaar. 2017. Phenotypic plasticity
Lanfear, R., B. Calcott, S. Y. W. Ho, and S. Guindon. 2012. PartitionFinder: in color without molt in adult grasshoppers of the genus Sphingonotus
combined selection of partitioning schemes and substitution models for (Acrididae: Oedipodinae). J. Orthoptera Res. 26: 21–27.
phylogenetic analyses. Mol. Biol. Evol. 29: 1695–1701. Pfadt, R. E. 1988. Field guide to the common western grasshoppers. University
Leavitt, J. R., K. D. Hiatt, M. F. Whiting, and H. Song. 2013. Searching for of Wyoming Agricultural Experiment Station Bulletin. 912: 145.
the optimal data partitioning strategy in mitochondrial phylogenomics: a Pocco, M. E., C. Minutolo, P. A. Dinghi, C. E. Lange, V. A. Confalonieri, and
phylogeny of Acridoidea (Insecta: Orthoptera: Caelifera) as a case study. M. M. Cigliano. 2015. Species delimitation in the Andean grasshopper
Mol. Phylogenet. Evol. 67: 494–508. genus Orotettix Ronderos & Carbonell (Orthoptera: Melanoplinae): an
Li, B., Z. Liu, and Z. M. Zheng. 2011. Phylogeny and classification of the integrative approach combining morphological, molecular and biogeo-
Catantopidae at the tribal level (Orthoptera, Acridoidea). Zookeys. 148: graphical data. Zool. J. Linn. Soc. 174: 733–759.
209–255. Rambaut, A. 2006–2009. FigTree: tree Figure Drawing Tool Version 1.3.1
Litzenberger, G., and W. Chapco. 2001. Molecular phylogeny of selected computer program, version by Rambaut, A.
Eurasian Podismine Grasshoppers (Orthoptera: Acrididae). Ann. Entomol. Rambaut, A., and A. J. Drummond. 2002–2013a. LogCombiner v1.8.0 com-
Soc. Am. 94: 505–511. puter program, version by Rambaut, A., and A. J. Drummond.
Litzenberger, G., and W. Chapco. 2003. The North American Melanoplinae Rambaut, A., and A. J. Drummond. 2002–2013b. TreeAnnotator v1.8.0 com-
(Orthoptera: Acrididae): a molecular phylogenetic study of their puter program, version by Rambaut, A., and A. J. Drummond.
origins and taxonomic relationships. Ann. Entomol. Soc. Am. 96: Rambaut, A., and A. J. Drummond. 2003–2009. Tracer: MCMC Trace
491–497. Analysis Tool Version v1.5.0 computer program, version by Rambaut, A.,
Liu, D., Z. Dong, D. Zhang, Y. Gu, P. Guo, R. Han, and G. Jiang. 2008. and A. J. Drummond.
Molecular phylogeny of the higher category of Acrididae (Orthoptera: Randell, R. L. 1963. On the presence of concealed genitalic structures in
Acridoidea). Zool. Res. 6: 585–591. female caelifera (Insecta; Orthoptera). T. Am. Entomol. Soc. 88: 247–260.
Ree, R. H., B. R. Moore, C. O. Webb, and M. J. Donoghue. 2005. A likelihood genus Orotettix (Orthoptera: Acrididae): ecological niches and evolution-
framework for inferring the evolution of geographic range on phylogen- ary history. Biol. J. Linn. Soc. 123: 697–711.
etic trees. Evolution. 59: 2299–2311. Sheffield, N. C., K. D. Hiatt, M. C. Valentine, H. Song, and M. F. Whiting. 2010.
Rehn, J. A. G., and H. J. Grant. 1960. A new concept involving the subfamily Mitochondrial genomics in Orthoptera using MOSAS. Mitochondrial
Acridinae (Orthoptera: Acridoidea). T. Am. Entomol. Soc. 86: 173–185. DNA. 21: 87–104.
Rehn, J. A. G., and H. J. Grant. 1961. A monograph of the Orthoptera of Snodgrass, R. E. 1902. Papers from the Hopkins Stanford Galapagos
North America (North of Mexico) Volume 1. Monograph of the Academy Expedition, 1898–1899. VIII. Entomological results (7). Schistocerca,
of Natural Sciences of Philadelphia. 12: 1–179. Sphingonotus and Halmenus. Proceedings of the Washington Academy of
Rentz, D. C. F. 1996. Grashopper Country: the abundant orthopteroid insects Sciences. 4: 411–454.
of Australia. University of New South Wales Press, Sydney, Australia. Song, H. 2004. On the origin of the desert locust Schistocerca gregaria
Rentz, D. C. F., R. C. Lewis, Y. N. Su, and M. S. Upton. 2003. A guide to (Forskål) (Orthoptera: Acrididae: Cyrtacanthacridinae). Proc. R. Soc.

Australian grasshoppers and locusts. Natural History Publications, Lond. B. 271: 1641–1648.
Borneo. Song, H. 2010. Grasshopper systematics: past, present and future. J.
R Core Team. 2017. R: A language and environment for statistical computing. Orthoptera Res. 19: 57–68.
R Foundation for Statistical Computing, Vienna, Austria. http://www.R- Song, H., and J. W. Wenzel. 2008. Phylogeny of bird-grasshopper subfamily
project.org/ Cyrtacanthacridinae (Orthoptera: Acrididae) and the evolution of locust
Roberts, H. R. 1941. A comparative study of the subfamilies of the Acrididae phase polyphenism. Cladistics. 24: 515–542.
(Orthoptera) primarily on the bases of their phallic structures. Proc. Acad. Song, H., M. J. Moulton, K. D. Hiatt, and M. F. Whiting. 2013. Uncovering
Nat. Sci. Phil. 93: 201–246. historical signature of mitochondrial DNA hidden in the nuclear genome:
Roberts, H. R. 1975. A revision of the genus Cylindrotettix, including new the biogeography of Schistocerca revisited. Cladistics. 29: 643–662.
species (Orthoptera: Acrididae: Leptysminae). Proc. Acad. Nat. Sci. Phil. Song, H., C. Amédégnato, M. M. Cigliano, L. Desutter-Grandcolas, S.
127: 29–43. W. Heads, Y. Huang, D. Otte, and M. F. Whiting. 2015. 300 million years
Roberts, H. R. 1978. A revision of the tribe Leptysmini except the genus of diversification: elucidating the patterns of orthopteran evolution based
Cylindrotettix (Orthoptera: Acrididae: Leptysminae). Proc. Acad. Nat. Sci. on comprehensive taxon and gene sampling. Cladistics. 31: 621–651.
Phil. 129: 33–69. Song, H., B. Foquet, R. Mariño-Pérez, and D. A. Woller. 2017. Phylogeny of
Roberts, H. R., and C. S. Carbonell. 1979. A revision of the genera Stenopola locusts and grasshoppers reveals complex evolution of density-dependent
and Cornops (Orthoptera, Acrididae, Leptysminae). Proc. Acad. Nat. Sci. phenotypic plasticity. Sci. Rep. 7: 6606.
Phil. 131: 104–130. Stamatakis, A., P. Hoover, and J. Rougemont. 2008. A Rapid Bootstrap
Roberts, H. R., and C. S. Carbonell. 1980. Concluding revision of the sub- Algorithm for the RAxML Web-Servers. Syst. Biol. 75: 758–771.
family Leptysminae (Orthoptera, Acrididae). Proc. Acad. Nat. Sci. Phil. Strömberg, C. A. E. 2011. Evolution of grasses and grassland ecosystems.
132: 64–85. Annu. Rev. Earth Planet. Sci. 39: 517–544.
Ronquist, F. 1997. Dispersal-vicariance analysis: a new approach to the quan- Tatarnic, N. J., K. D. L. Umbers, and H. Song. 2013. Molecular phylogeny of
tification of historical biogeography. Syst. Biol. 46: 195–203. the Kosciuscola grasshoppers endemic to the Australian alpine and mon-
Ronquist, F., M. Teslenko, P. van der Mark, D. L. Ayres, A. Darling, S. Hohna, tane regions. Invertebrate Systematics. 27: 307–316.
B. Larget, L. Liu, M. A. Suchard, and J. P. Huelsenbeck. 2012. MrBayes Thompson, D. C., and D. B. Richman. 1993. A grasshopper that only eats snake-
3.2: efficient Bayesian phylogenetic inference and model choice across a weed?, pp. 18–19. In Sterling, T.M. and Thompson, D.C. (ed.) Research
large model space. Syst. Biol. 61: 539–542. Report 674, Agricultural Experiment Station Cooperative Extension Service
Rosenberg, J., and P. J. A. Burt. 1999. Windborne displacements of desert New Mexico State University, Snakeweed research updates and highlights.
locusts from Africa to the Caribbean and South America. Aerobiologia New Mexico Agricultural Experimental Station Research Report.
15: 167–175. Uvarov, B. P. 1941. New and less known southern Palaearctic Orthoptera.
Rowell, C. H. F. 1971. The variable coloration of the acridoid grasshoppers. Transactions of the American Entomological Society 67: 303–361.
Adv. Insect Physiol. 8: 145–198. Uvarov, B. P. 1966. Grasshoppers and Locusts, vol. 1. Cambridge University
Rowell, C. H. F. 1978. Food plant specificity in Neotropical rain-forest acrid- Press, Cambridge, UK.
ids. Entomol. Exp. Appl. 24: 451–462. Uvarov, B. P. 1977. Grasshoppers and Locusts, vol. 2. Centre for Overseas Pest
Rowell, C. H. F. 1987. The biogeography of Costa Rican acridid grasshoppers, Research, London, UK.
in relation to their putative phylogenetic origins and ecology, pp. 470–482. Vaidya, G., D. J. Lohman, and R. Meier. 2011. SequenceMatrix: concatenation
In B. M. Baccetti (ed.), Evolutionary biology of orthopteroid insects. Ellis software for the fast assembly of multi-gene datasets with character set
Horwood Limited, Chichester, United Kingdom. and codon information. Cladistics. 27: 171–180.
Rowell, C. H. F. 2013. The Grasshoppers (Caelifera) of Costa Rica and Vickery, V. R. 1987. The northern Nearctic Orthoptera: their origins and sur-
Panama, The Orthopterists’ Society. vival, pp. 581–591. In B. M. Baccetti (ed.), Evolutionary biology of orth-
Rowell, C. H. F., and P. K. Flook. 2004. A dated molecular phylogeny of the opteroid insects. Ellis Horwood Limited, Chichester, United Kingdom.
Proctolabinae (Orthoptera, Acrididae), especially the Lithoscirtae, and the Vickery, V. R. 1989. The biogeography of Canadian Grylloptera and
evolution of their adaptive traits and present biogeography. J. Orthoptera Orthoptera. Can. Entomol. 121: 389–424.
Res. 13: 35–56. Woller, D. A., and H. Song. 2017. Investigating the functional morphology of
Rowell, C. H. F., and C. Hemp. 2017. Jago’s Grasshoppers of East and North genitalia during copulation in the grasshopper Melanoplus rotundipen-
East Africa, vol. 2. Rowell & Hemp (privately published). nis (Scudder, 1878) via correlative microscopy. J. Morphol. 278: 334–359.
Rowell, C. H. F., M. Rowell-Rahier, H. E. Braker, G. Cooper-Driver, and L. Woller, D. A., P. Fontana, R. Mariño-Pérez, and H. Song. 2014. Studies in
D. Gomez P. 1983. The palatability of ferns and the ecology of two trop- Mexican grasshoppers: Liladownsia fraile, a new genus and species of
ical forest grasshoppers. Biotropica. 15: 207–216. Dactylotini (Acrididae: Melanoplinae) and an updated molecular phyl-
Samways, M. J., and M. G. Sergeev. 1997. Orthoptera and landscape ogeny of Melanoplinae. Zootaxa. 3793: 475–495.
change, pp. 147–162. In S. K. Gangwere, M. C. Muralirangan, and M. Xia, K. L. 1994. Fauna Sinica, Insecta Vol. 4 Orthoptera: acridoidea (Pamphagidae,
Muralirangan (eds.), The bionomics of grasshoppers, katydids and their Chrotogonidae, Pyrgomorphidae). Science Press, Beijing, China.
kin. CAB International, Wallingford, United Kingdom. Yin, X. C., and K. L. Xia. 2003. Fauna Sinica, Insecta Vol. 32, Gomphoceridae
Särkinen, T., L. Bohs, R. G. Olmstead, and S. Knapp. 2013. A phylogenetic and Acridoidea. Science Press, Beijing, China.
framework for evolutionary study of the nightshades (Solanaceae): a dated Zheng, Z. M. 1993. Taxonomy of grasshoppers. Shanxi Normal University
1000-tip tree. BMC Evol. Biol. 13: 214. Press, Xi’an, China.
Scattolini, M. C., V. A. Confalonieri, A. Lira-Noriega, S. Pietrokovsky, and M. Zheng, Z. M., and K. L. Xia. 1998. Fauna Sinica, Insecta Vol. Orthoptera:
M. Cigliano. 2018. Diversification mechanisms in the Andean grasshopper acridoidea (Oedipodidae and Arcypteridae). Science Press, Beijing, China.

Hojun Song 2018

Uploaded by

Copyright:

Available Formats

Hojun Song 2018

Uploaded by

Document Information

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

Hojun Song 2018

Uploaded by

Copyright:

Available Formats

Insect Systematics and Diversity, (2018) 2(4): 3; 1–25

Evolution, Diversification, and Biogeography of

Downloaded from https://academic.oup.com/isd/article/2/4/3/5052737 by Universidad Nacional de Colombia user on 06 August 2021

Subject Editor: Jessica Ware

Received 6 March 2018; Editorial decision 31 May 2018

Key words: Acrididae, grasshopper, phylogeny, biogeography

Downloaded from https://academic.oup.com/isd/article/2/4/3/5052737 by Universidad Nacional de Colombia user on 06 August 2021

Downloaded from https://academic.oup.com/isd/article/2/4/3/5052737 by Universidad Nacional de Colombia user on 06 August 2021

Subfamily Number of genera Number of species Distribution

Acridinae 141 483 Cosmopolitan

Downloaded from https://academic.oup.com/isd/article/2/4/3/5052737 by Universidad Nacional de Colombia user on 06 August 2021

Cedarinia sp OR490 N/A MG888274 MG888322 MG888230 MG888103 MG888170

Downloaded from https://academic.oup.com/isd/article/2/4/3/5052737 by Universidad Nacional de Colombia user on 06 August 2021

Downloaded from https://academic.oup.com/isd/article/2/4/3/5052737 by Universidad Nacional de Colombia user on 06 August 2021

Stenopola sp OR220 N/A MG888256 MG888302 MG888210 MG888081 MG888148

Downloaded from https://academic.oup.com/isd/article/2/4/3/5052737 by Universidad Nacional de Colombia user on 06 August 2021

Downloaded from https://academic.oup.com/isd/article/2/4/3/5052737 by Universidad Nacional de Colombia user on 06 August 2021

Downloaded from https://academic.oup.com/isd/article/2/4/3/5052737 by Universidad Nacional de Colombia user on 06 August 2021

Downloaded from https://academic.oup.com/isd/article/2/4/3/5052737 by Universidad Nacional de Colombia user on 06 August 2021

Downloaded from https://academic.oup.com/isd/article/2/4/3/5052737 by Universidad Nacional de Colombia user on 06 August 2021

Downloaded from https://academic.oup.com/isd/article/2/4/3/5052737 by Universidad Nacional de Colombia user on 06 August 2021

Downloaded from https://academic.oup.com/isd/article/2/4/3/5052737 by Universidad Nacional de Colombia user on 06 August 2021

Downloaded from https://academic.oup.com/isd/article/2/4/3/5052737 by Universidad Nacional de Colombia user on 06 August 2021

Downloaded from https://academic.oup.com/isd/article/2/4/3/5052737 by Universidad Nacional de Colombia user on 06 August 2021

Downloaded from https://academic.oup.com/isd/article/2/4/3/5052737 by Universidad Nacional de Colombia user on 06 August 2021

Downloaded from https://academic.oup.com/isd/article/2/4/3/5052737 by Universidad Nacional de Colombia user on 06 August 2021

Downloaded from https://academic.oup.com/isd/article/2/4/3/5052737 by Universidad Nacional de Colombia user on 06 August 2021

Downloaded from https://academic.oup.com/isd/article/2/4/3/5052737 by Universidad Nacional de Colombia user on 06 August 2021

Downloaded from https://academic.oup.com/isd/article/2/4/3/5052737 by Universidad Nacional de Colombia user on 06 August 2021

Downloaded from https://academic.oup.com/isd/article/2/4/3/5052737 by Universidad Nacional de Colombia user on 06 August 2021

Downloaded from https://academic.oup.com/isd/article/2/4/3/5052737 by Universidad Nacional de Colombia user on 06 August 2021

Downloaded from https://academic.oup.com/isd/article/2/4/3/5052737 by Universidad Nacional de Colombia user on 06 August 2021

Downloaded from https://academic.oup.com/isd/article/2/4/3/5052737 by Universidad Nacional de Colombia user on 06 August 2021

Downloaded from https://academic.oup.com/isd/article/2/4/3/5052737 by Universidad Nacional de Colombia user on 06 August 2021

You might also like