Feener - 1997 - AnnuRevEntomol - Diptera Parasitoids

October 29, 1996 9:8 Annual Reviews FEENTEXT.
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Annu. Rev. Entomol. 1997. 42:73–97

Copyright c 1997 by Annual Reviews Inc. All rights reserved
DIPTERA AS PARASITOIDS
Donald H. Feener Jr.
Department of Biology, University of Utah, Salt Lake City, Utah 84112
Brian V. Brown
Entomology Section, Natural History Museum of Los Angeles County, 900 Exposition
Boulevard, Los Angeles, California 90007
KEY WORDS: parasitoid, host relationships, parasitic Diptera, bionomics
ABSTRACT
Parasitoids in the insect order Diptera include an estimated 16,000 species, or
approximately 20% of the total number of species with this life-style. Parasitoids
in this order are exceedingly diverse in both their habits and evolutionary origins,
which makes them an underutilized but highly suitable group for quantitative
studies of character convergence and adaptive radiation. This review focuses on
several aspects of the bionomics of dipteran parasitoids that have received little
comprehensive treatment, including processes associated with host location and
attack, patterns of host use, and the evolutionary and ecological consequences
of host-parasitoid interactions. Throughout the review we contrast the patterns
found within the parasitic Diptera against those found in the better studied parasitic
Hymenoptera. We conclude that more intensive study of dipteran parasitoids is re-
quired before we can understand the general conditions that favor the evolution of
insect parasitoids and the truly magnifying themes of their behavior and ecology.
INTRODUCTION
Research on insect parasitoids has increased explosively in the last 15 years
(45, 46, 65, 68, 75, 77, 121, 167). This increase has come with the growing
recognition that host-parasitoid systems offer unparalleled opportunities to ex-
amine fundamental questions in behavioral and evolutionary ecology. In recent
years, insect parasitoids have served as model systems in studies of information
processing (152, 158), optimal foraging and clutch size (33, 67, 69, 73, 143),
sex allocation strategies (31, 68), and mechanisms of interspecific interactions
(9, 77, 148). These studies have revealed new levels of sophistication and
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74 FEENER & BROWN
subtlety in insect behavior and provide some of the strongest evidence for the
fundamental and enduring role of natural selection in molding this behavior.
Renewed interest in parasitoids as biological control agents has coincided with
the adoption of parasitoids as model theoretical and experimental systems (38,
76, 78, 80, 81, 88). That interest has been prompted in part by the deeper under-
standing of parasitoid behavior and ecology these new approaches bring, and
in part by an increasing disenchantment with chemical means of pest control
(38).
Parasitoids occur in five orders of holometabolous insects: Hymenoptera,
Diptera, Coleoptera, Lepidoptera, and Neuroptera (45). Hymenopteran para-
sitoids account for nearly 78% of the estimated number of species and conse-
quently have served as models of choice for nearly all recent research on insect
parasitoids (68, 77, 167). However, several unique features make this group
of questionable value in understanding the evolution and general significance
of the parasitoid life-style. First, parasitoids in the Hymenoptera represent a
single evolutionary lineage in contrast to the dozens, perhaps hundreds, of par-
asitoid lineages in the Diptera, Coleoptera, and some other orders (45). Thus,
by itself, the parasitic Hymenoptera can shed very little light on the general
conditions that favor the origin of insect parasitoids. Second, the Hymenoptera
are alone among the Holometabola in retention of the primitive lepsimatid form
of ovipositor and associated accessory glands (65). Possession of this oviposi-
tor gives female hymenopteran parasitoids direct access to concealed hosts and
small hosts such as eggs or early stage larvae that are not directly accessible
to parasitoids in other groups. Moreover, venom produced in the modified ac-
cessory glands allows hymenopteran parasitoids to subdue large active hosts
and manipulate the behavior and physiology of hosts in favor of their progeny.
Again, such opportunities are not as obviously available to other parasitoids.
Finally, only hymenopteran parasitoids are haplodiploid. Such a sex-deter-
mining system gives females control over the sex ratio of their progeny, per-
mitting them both to match the sex of their progeny to the size of the host and
to reduce the intensity of local mate competition in mixed-sex clutches (31,
68). While all of these features clearly have contributed to the remarkable eco-
logical and evolutionary success of the parasitic Hymenoptera, they are just as
clearly not essential to the ecological and evolutionary success of parasitoids
in general. A broader understanding of the parasitoid life-style requires that
we examine other groups of insect parasitoids in the same detail that we have
examined hymenopteran parasitoids.
Parasitoids in the order Diptera are the subject of this review. This order
includes an estimated 16,000 described species of parasitoids, or about 20% of
the known species with this life-style (45). We do not attempt a comprehensive
DIPTERA AS PARASITOIDS 75
review of the natural history of these parasitoids but instead focus on selected
topics of general interest, specifically evolutionary origins and biogeography,
host location and reproductive behavior of adults, larva-host interactions, evo-
lution of host specificity, and the impact of these parasitoids on the evolution
and ecology of their hosts. General accounts of the natural history of dipteran
parasitoids can be found in the books by Askew (6), Clausen (34), Ferrar (58),
and Oldroyd (108) and in the Manual of Nearctic Diptera (95–97). Families re-
ceiving recent specialized reviews include the Bombyliidae (173), Calliphoridae
(125), Phoridae (42), Sarcophagidae (113), Sciomyzidae (12), Rhinophoridae
(112), and Tachinidae (10, 79, 99, 114).
Throughout this review we use the better studied parasitic Hymenoptera
as a standard against which we compare the natural history of the parasitic
Diptera (65, 68). Our goal is to identify the major commonalities and differ-
ences between these two groups of parasitoids, which should serve as points of
departure for future studies (46). Several themes emerge in the course of this re-
view. First, generalizations about the parasitoid life-style derived from studies
of the parasitic Hymenoptera often do not hold for the parasitic Diptera or hold
only in a highly modified form. Second, repeated independent evolution within
the Diptera of structures (e.g. piercing ovipositors, respiratory funnels) and
behaviors (e.g. planidiform first instar larvae, phonotaxic host location) asso-
ciated with the parasitoid life-style make this group an underutilized but highly
suitable group for quantitative studies of character convergence and adaptive
radiation. And finally, as a consequence of the diverse evolutionary origins of
the parasitic Diptera, host-parasitoid interactions involving this group are them-
selves diverse and multifaceted. The distinctive signatures of these interactions
can be found in the physiology, behavior, and ecology of hosts and perhaps in
the structure of entire ecological communities.
TAXONOMY, BIOGEOGRAPHY, AND EVOLUTIONARY

ORIGINS
The taxonomic distribution and evolutionary origins of the parasitoid life-style
have been discussed authoritatively by Eggleton & Belshaw (45), who recog-
nized parasitoids in 21 families of Diptera. They hypothesized that this life-style
has evolved over 100 times in the Diptera. Most dipteran parasitoids arose from
saprophagous ancestors and have ancestors and hosts that live in or near the
soil surface (46).
The Phoridae, our group of interest, provide an instructive example of these
generalizations. Although known largely as saprophages, many phorids are
parasitoids, predators, and even herbivores. Parasitoids are found in three of
76 FEENER & BROWN
the five major subfamilies of phorids recognized by Brown (18): Hypoceri-

nae, Aenigmatiinae, and Metopininae. Species of the other two subfamilies,
Phorinae and Conicerinae, are mostly saprophages. Within the Hypocerinae,
parasitoids are known with certainty for only one genus, Peromitra, two species
of which attack bibionid fly larvae. Unfortunately, the life history of few other
species of hypocerines are known, although species of Stichillus and Trineuro-
cephalus, the closest relatives of Peromitra, are suspected to be parasitoids of
bees. The more primitive genus Hypocera has one species that apparently is
a saprophage (M Buck, personal communication). Within the Aenigmatiinae
(including “Thaumatoxeninae”) species of many genera are associated with
burrowing social insects, and some are known to be parasitoids; others are
mostly saprophagous.
Within the largest subfamily, Metopininae, the bulk of the genera are orga-
nized into two groups: the Metopina group and the Megaselia group. Some
parasitoids are known in the Metopina group, but many have unknown life
histories, living within nests of burrowing social insects (ants and termites).
Many other species are saprophages. In the Megaselia group, there are many
saprophages and some specialized predators, in addition to the parasitoids. The
large Apocephalus subgroup of genera are all parasitoids, mostly of ants (18).
In this subgroup, there is no indication of a saprophagous ancestor previously
associated with social insects. Thus, general trends found in the Phoridae are
the apparent acquisition of parasitoid behavior from a scavenger host associa-
tion (possibly in the Hypocerinae and Megaselia group) and the predisposition
of taxa associated with burrowing social insects to become parasitoids of those
insects (the Metopina group).
A questionable generalization about parasitic Hymenoptera that is obviously
not applicable to Diptera is a paucity of tropical species (66). Contrary to
expectations, a number of authors have found that the number of species of
parasitic Hymenoptera does not always decrease with decreasing latitude (66,
75). In Diptera, this is certainly not the case for Phoridae and at least some
Tachinidae (107). Comparison on a region-to-region basis or a site-to-site basis
shows that the Neotropical fauna is much larger than that in the Nearctic Region.
For instance, the Apocephalus fauna of one tropical site, La Selva Biological
Station in Costa Rica, is at least three times larger than that of the entire Nearctic
Region (24). Other genera have not been studied as intensively, but in southern
Brazil, the portion of the Pseudacteon fauna that parasitizes fire ants alone
is about 18 species (14, 171) and species that parasitize other types of ants
doubtlessly are also present. That greatly exceeds of the Nearctic Pseudacteon
fauna of only seven species. In general, the described Neotropical fauna is
about three to four times larger than the described Nearctic fauna.
INTERACTIONS BETWEEN ADULT PARASITOIDS

AND HOSTS
Host Location
Host location behavior of insect parasitoids has been studied extensively and
reviewed repeatedly (68, 87, 154, 162–164). Both hymenopteran and dipteran
parasitoids use an astonishing assortment of environmental cues to locate hosts.
The nature of these cues is often subtle and complex, reflecting the intense se-
lection pressure faced by parasitoids searching for hosts. In summarizing this
vast literature, Godfray (68) recognized three broad, partially overlapping cate-
gories of information available for use in host location: signals originating from
the microhabitat or food plants of potential hosts, signals indirectly associated
with the activity of hosts in the microhabitat, and signals arising directly from
the hosts themselves. The information in these categories varies consistently in
both its reliability and detectability (158, 161). Signals derived directly from
hosts are the most reliable indicators of their location and identity. However,
because hosts are under constant selection pressure to minimize their conspic-
uousness to natural enemies, these signals are often too weak for detection over
long distances. Cues emanating from microhabitat or food plant of potential
hosts, in contrast, are frequently easier to detect at a distance, but provide little
reliable information concerning the specific location and identity of hosts. Thus,
signal reliability is often inversely related to signal detectability, a condition
Vet & Dicke refer to as the “reliability-detectability problem” (158, 161).
Parasitoids have evolved several general strategies of host location in the face
of this reliability-detectability trade-off in information content. Host-seeking
females that are directly attracted to their hosts typically use signals associated
with sexual communication systems of their hosts (164). Unlike most host-
derived cues, these signals have evolved to advertise the presence and identity
of the sender and are therefore both easy to detect at long distances and serve
as very reliable indicators of host location and identity. Moreover, because
of reliability and evolutionary stability of this kind of cue, the response of
parasitoids to them is more likely to be congenitally fixed than responses to cues
indirectly linked to the presence of hosts (160). Apparently, few hymenopteran
parasitoids have evolved the means to exploit the communication systems of
their hosts (164). However, as the following examples illustrate, a wide range
of dipteran parasitoids use this strategy of host location.
Females of the tachinid Ormia (=Euphasiopteryx) ochracea are attracted by
the mating songs of male crickets (Gryllidae) and ovolarviposit on or near these
males (1, 27, 168, 169). Females of O. ochracea detect the song of their host via
a specialized tympanal hearing organ located on the front panel of the prothorax
78 FEENER & BROWN
(123, 124). Males also possess a tympanal hearing organ, but are never attracted
to cricket calling songs. The ears of males and females are sexually dimorphic
in both structure and function, and their differences presumably account for
differences in attraction to hosts. The ear of the female has a larger tympanal
membrane, and its frequency tuning curve is 40–50 dB more sensitive than the
male’s to the carrier frequency of cricket song (4–6 kHz) (123, 124). Male and
female ears are equally sensitive at higher frequencies and are probably used
in predator detection (123).
Other species of ormiine tachinids orient phonotaxically to their hosts and
presumably share the novel structural features found in O. ochracea (25, 60, 61,
85, 168). Host location by phonotaxis has evolved independently in at least one
species of sarcophagid in the tribe Emblemasomatini (Colcondamyia auditrix)
(145). Females, but not males, of this species orient to the calling song of the
cicada Okanagana rimosa. The acoustical organ has not yet been located in
species of Colcondamyia, but given the behavior of the flies, it is likely to be
convergent in structure and function to the tympanal hearing organ of Ormia
species. Because the components of acoustical signals are easy to manipulate
experimentally, these systems offer excellent opportunities for exploring the
specificity of sensory systems used in host location (168). It would be especially
interesting to know whether the behavioral responses of hosts and parasitoids
to various song components parallel the structure-function convergence of their
ears.
While phonotaxis is a particularly spectacular example of exploitation of
host communication systems, detection of chemical cues is probably a more
common method. The tachinid parasitoid Trichopoda pennipes, for example, is
attracted to the aggregation pheromone of its pentatomid host Nezara viridula
(74, 100). Only males produce and release this pheromone, and, like calling
male crickets, they are more likely to be parasitized than females (100). The
pheromone is actually a blend of several sesquiterpene-dominated compounds
that vary in proportion across the geographic range of N. viridula (4). T. pen-
nipes is differentially responsive to these pheromone strains, leading Aldrich
et al (3) to conclude that some of the geographic variation in pheromone blends
is the result of parasitoid-induced selection pressure. Several other species of
tachinid parasitoids of pentatomids show similar proficiency at discriminating
between the natural pheromone of their hosts and synthetic pheromones of
slightly different structure (2).
Other forms of intraspecific communication are sometimes used by dipteran
parasitoids during host location. The elaborate systems of intraspecific commu-
nication in ants offer abundant opportunities for exploitation by the parasitoids
that utilize them as hosts (82). Phorid parasitoids of ants are often attracted to
nest sites or the recruitment trails of hosts and appear to use olfactory signals
as orientation cues (21, 44). For example, males and females of Apocephalus
paraponerae are attracted to injured or freshly killed workers of the giant trop-
ical ant Paraponera clavata (21). In addition to oviposition, flies may feed and
mate while on that host. Recently, Feener et al (56) showed the host-location
cues used by these parasitoids are two chemicals produced in the mandibular
glands of workers. These compounds, 4-methyl-3-heptanone and 4-methyl-3-
heptanol, are released by disturbed, fighting, injured, or freshly killed workers
and may serve to warn other workers of imminent danger. They have been iden-
tified as alarm pheromones in several other species of ants related to P. clavata
and may act to determine the realized host range of the parasitoid (56). Unlike
many species that exploit the communication systems of their hosts (see above),
males of phorid parasitoids of ants are often more responsive to host-location
cues than females. Presumably, males in these systems are using hosts as pre-
ferred mating sites, which may also influence host range and the opportunity for
sympatric speciation. We return to this topic in the section on host specificity.
A second general strategy of host location partitions the task into two separate
phases involving different life-history stages. In the first phase, adult females
locate the microhabitat of potential hosts. Once in the general vicinity of a
host, females scatter eggs or larvae on the surface of the substrate and then
leave the area. Actual contact with hosts occurs in the second phase and is left
to the immature stages. There are three basic mechanisms by which immatures
may contact hosts: Hosts may ingest the parasitoid egg during feeding, the
parasitoid larva may in wait in ambush for a passing host, or the parasitoid
larva may actively search for suitable hosts (72).
This general two-phase strategy is the most common method of host location
in the parasitic Diptera. All three mechanisms of host contact are found within
this group. In the tachinid tribe Goniini, contact with the host occurs passively
in the egg stage. Microtype eggs deposited by females remain dormant in the
environment until accidentally ingested by a feeding host. Eggs are then stimu-
lated to hatch by a combination of salivary juice, mechanical rupture, and high
pH in the host’s gut (72). Many members of the tachinid subfamily Tachininae
practice the ambush mechanism of host contact, with newly hatched larvae us-
ing the chorion of the egg as a cup in which to stand. From its vertical position
the larva rotates in response to moving objects and attaches to a suitable host
as it passes (72). Most dipteran parasitoids that rely on immatures for host
contact produce actively searching larvae. Such actively searching planidiform
larvae have evolved independently in numerous dipteran families, including
the Acroceridae, Nemestrinidae, Bombyliidae, Calliphoridae, Rhinophoridae,
and many Tachinidae (especially in the large tribe Dexiini). Actively searching
80 FEENER & BROWN
larvae allow many of these species to utilize hosts that live in places inaccessible
to adult flies (e.g. soil, rotten wood, healthy wood).
Comparative studies of the adaptations associated with these three mech-
anisms of host contact provide compelling evidence of repeated instances of
convergent evolution in the structure and function of eggs and larvae (72). We
know considerably less about the ecology and behavior of these host-seeking
life stages. In contrast to our knowledge about habitat location in adults (94,
105, 127, 128, 130), we know virtually nothing about specific cues used by
host-seeking larvae to detect the presence of a suitable host, nor do we know
anything about the how long eggs and larvae remain viable in the environment
while awaiting host contact (36). Presumably, life expectancy of these stages
has evolved to match the average time course to host contact, which may differ
among the three contact mechanisms (32). Variation in life expectancy of these
stages may also reflect trade-offs between endurance while waiting for a host
and readiness for growth once the host is found (32). Investigation of these
and other life-history characteristics of eggs and larvae should enhance our
understanding of the various strategies of host location in the parasitic Diptera.
A third general strategy of host location links unreliable but easy-to-detect
stimuli to reliable but hard-to-detect stimuli through associative learning (68,
152, 159). In this form of learning, responses to stimuli are newly acquired
or enhanced by linkage to a reinforcing stimulus. For example, females of the
specialized braconid Microplitis croceipes are innately attracted to a nonvolatile
chemical in the frass of its hosts, larvae of Heliothis and Helicoverpa species
(98). If females discover host frass in association with a more volatile chem-
ical (e.g. volatiles from the food plant of the host or experimentally provided
vanilla), they subsequently orient toward the new stimulus in the absence of the
original stimulus (48, 90, 98). This form of linkage between a nonvolatile host-
recognition cue and a more volatile, easily detected secondary cue increases
searching efficiency (89, 111). Other studies indicate that these parasitoids can
also learn to associate visual and olfactory cues in a similar manner and may be
able to link other sensory modalities as well (152). So far, associative learning
has been found in more than 20 species of hymenopteran parasitoids, includ-
ing braconids, eucoilids, aphidiids, ichneumonids, and trichogrammatids and
is probably the most common method of host location in this group (152, 159).
Associative learning is also likely to be common in dipteran parasitoids, but so
far it has been reported in only one species, the tachinid Drino bohemica (101).
In the laboratory, females of this species learned to associate the movement of
a tray in the bottom of the cage with the presentation of hosts (late-instar larvae
of tenthredinoid sawflies). Visual detection of the host’s presence apparently
served as the reinforcing stimulus. How D. bohemica takes advantage of such
visually mediated learning under more natural circumstances remains to be

studied. Presumably, a learned response to a mechanosensory stimulus allows
the parasitoid to detect the presence of hosts in the absence of visual cues. This
may happen if hosts are hidden in vegetation. Using the paradigm developed
above, we would expect to find learning in other dipteran parasitoids that have
the opportunity to make links between inconspicuous hosts and readily available
microhabitat components. Those species that utilize herbivorous hosts provide
the best opportunity to study the links between their host-location behavior and
associative learning.
Superparasitism and Host Discrimination
Superparasitism is defined as the deposition of a clutch of eggs in a host already
parasitized by a member of the same species (68, 156). Because the progeny
of a superparasitizing female are normally at a competitive disadvantage rel-
ative to the progeny of the previous parasitoid, natural selection should favor
females with the ability to discriminate parasitized from unparasitized hosts.
Quantitative observational studies in the field and experimental studies in the
laboratory, reaching back nearly 100 years, have documented such host discrim-
ination in a total of 150–200 species of parasitic Hymenoptera, representing
nearly all families that oviposit directly on hosts (59, 68, 131, 157). These
parasitoids use a variety of cues to distinguish between parasitized and unpar-
asitized hosts, including externally and internally applied chemical markers,
visual or tactile detection of eggs or larvae on the cuticle of the host, presence
of necrotic host tissue, or absence of movement by the host (68). Having estab-
lished the widespread recognition of previously parasitized hosts by parasitic
Hymenoptera, researchers have recently focused on the conditions under which
superparasitism, or the apparent absence of such recognition, is adaptive (68,
146, 155).
In contrast to parasitic Hymenoptera, superparasitism in the parasitic Diptera
appears to be both widely distributed across species and common within pop-
ulations. Superparasitism has been reported in conopids (137), phorids (55),
and numerous tachinid species (70, 92, 93, 99, 142, 150, 153, 170). Super-
parasitism may occur in other groups as well (6, 34), but reliable data are
lacking. Within populations, superparasitism may occur regularly and some-
times reach high levels. Maier (92) reported superparasitism by the solitary
tachinid Parasetigena silvestris to be as high as 83% in one population of the
lepidopteran host Lymantria dispar. At one nest of the leaf-cutting ant Atta
cephalotes, the solitary phorid Neodohrniphora curvinervis superparasitized
19% of suitable workers (55). Sometimes superparasitism of individual hosts
can reach spectacular levels (13, 151). Bobadilla (13), for example, counted
148 macrotype eggs of the solitary tachinid Euphorocera peruviana attached
82 FEENER & BROWN
to the cuticle of a caterpillar in the noctuid genus Melipotis. None of the larvae
that hatched from these eggs successfully completed development.
The widespread occurrence of superparasitism in the parasitic Diptera sup-
ports the impression that the ability to discriminate between parasitized and
unparasitized hosts is entirely lacking or severely limited in this group (6, 155).
For several reasons, however, we suspect that future, more quantitative studies
of oviposition behavior will uncover numerous instances of host discrimination
in the parasitic Diptera. First, female dipteran parasitoids that oviposit directly
on their hosts should face the same disadvantages from superparasitism as
hymenopteran parasitoids and therefore should experience the same selection
pressures for the ability to recognize parasitized hosts. As is often true in hy-
menopteran parasitoids, superparasitism in dipteran parasitoids frequently low-
ers the probability of successful emergence of adults or reduces size, longevity,
or fecundity of those that do emerge (70, 93, 142). Second, superparasitism of-
ten occurs in species that are capable of recognizing prior parasitization (157);
therefore evidence of superparasitism is not evidence for the lack of such recog-
nition. And third, recognition has evolved in other dipteran groups under similar
selection pressure (e.g. fruit-infesting tephritid flies) (126), demonstrating that
phylogenetic or physiological constraints need not limit the evolution of such
behavior.
Several recent studies help illuminate the conditions under which recogni-
tion of parasitized hosts, or the lack thereof, should be observed in the parasitic
Diptera. Females that make direct contact with hosts during offspring deposi-
tion often have the best opportunity to assess host quality, especially if hosts are
relatively abundant, sluggish, and passively defended (e.g. lepidopteran and
coleopteran larvae). In the first study to provide definitive experimental evi-
dence for host discrimination in dipteran parasitoids, Lopez et al (91) showed
that females of two solitary tachinid parasitoids, Myiopharus doryphorae and
Myiopharus aberrans, actively avoid ovolarvipositing in previously parasitized
larvae of their host, the Colorado potato beetle (Leptinotarsa decemlineata).
Recognition of host parasitization in both species occurs only after contact
with the integument of a host and presumably involves chemoreceptors and/or
mechanoreceptors located on the tarsi (91). Superparasitism in both field and
laboratory was exceedingly rare in these species unless availability of unpara-
sitized hosts was low. Under these circumstances, female parasitoids otherwise
capable of recognizing parasitized hosts can often gain fitness by accepting pre-
viously parasitized hosts (33, 143, 166). Alternatively, superparasitism in these
instances may represent a nonadaptive breakdown in the tendency to refrain
from offspring deposition. Which of these hypotheses is true for Myiopharus
species has not yet been determined.
Evolution of the ability to discriminate between parasitized and unparasitized

hosts may be less advantageous in species that attack agile, actively defended
hosts, such as ant workers or other adult insects, because added time required
for such discrimination may subject ovipositing females to increased risk of
injury or death. Many ant species have unique defense postures or movements
that make oviposition by phorid parasitoids difficult and dangerous (51–54).
We have repeatedly seen ovipositing females of Apocephalus attophilus, a par-
asitoid of leaf-cutting ants, captured and killed by minim workers that hitchhike
on the leaf fragments carried by their larger more attack-susceptible sisters (57).
In Neodohrniphora curvinervis, another parasitoid of leaf-cutting ants, success-
ful oviposition requires females to insert an egg through the foramen magnum
of a host that is either running rapidly ahead of the fly or standing its ground
and flailing its fore- and midlegs about its head and thorax (55). Defending
ants may damage ovipositing females with blows to the body from their flailing
legs or by pinching the fly between their head and thorax during oviposition.
To avoid damage, oviposition must be quick and precise, which may not leave
time to assess host condition, resulting in a high level of superparasitism (55).
Phorids that parasitize mortally injured or freshly killed ants (e.g. species in
the genus Rhyncophoromyia and the Apocephalus miricauda group) may have
more opportunity to recognize the condition (21–23, 56), but such behavior
remains to be investigated.
In the majority of dipteran parasitoids, ovipositing females never make con-
tact with prospective hosts, and therefore there is little opportunity to recognize
prior parasitization by adult females. While it is possible that host-seeking lar-
vae have evolved that ability, we suspect it is rarely advantageous because host
encounter rates of such larvae are probably much lower than those of more mo-
bile adults. Given the low probability of encountering another more suitable
host, host-seeking larvae should be more willing to accept previously para-
sitized hosts than host-seeking adult females. Species that practice a mixed
reproductive strategy in which either larvae or adults contact hosts may also
lack the ability to recognize parasitized hosts. Adamo et al (1) found no evi-
dence that females of the tachinid O. ochracea discriminate between parasitized
and unparasitized hosts. Partial reliance on host-seeking larvae may reduce se-
lection for the evolution of such discrimination in adults because it increases
the uncertainty associated with a particular clutch size.
Behaviors other than recognition of prior host parasitization might reduce
superparasitism in parasitic Diptera. Coupland & Baker (37) argued that the rea-
son females of the solitary snail parasitoid, Sarcophaga penicillata, remain on
the host for 5–65 min after larviposition is to protect against subsequent super-
parasitism. Rather than directly protecting against superparasitism, however,
84 FEENER & BROWN
we suspect that this “post-ovipositional host-guarding” behavior allows the

larva to gain enough of a growth advantage in the host to prevent development
of subsequent larvae.
INTERACTIONS BETWEEN LARVAL PARASITOIDS

AND HOST
Researchers have recognized four general developmental strategies in the in-
sect parasitoids (8, 65, 68). The larvae of ectoparasitoids develop externally,
usually with their mouthparts buried in the body of their host. The larvae of
endoparasitoids develop within the body of their host and feed on the host from
the inside. These terms clearly apply to dipteran parasitoids as well as hy-
menopteran parasitoids. Most dipteran parasitoids are endoparasitoids, except
for bombyliids, which develop externally to their hosts. Askew & Shaw (8)
expressed dissatisfaction with this classification for hymenopteran parasitoids
and suggested an alternative classification based on whether a parasitoid per-
mits the host to grow or metamorphose beyond the stage attacked. Koinobionts
in this classification are parasitoids that allow their hosts to continue to de-
velop after oviposition, whereas idiobionts are parasitoids that paralyze or kill
their hosts before oviposition. Because no dipteran parasitoids paralyze their
host or arrest its development with venom, all would have to be classified as
koinobionts. However, as noted by Belshaw (11), much variation occurs in the
amount of host development after oviposition of dipteran parasitoids.
In the Hymenoptera, interactions between parasitoid larvae and their hosts are
largely governed by physiological, immunological, and biochemical processes
(65, 68, 132, 134, 148, 149, 165). Early larval instars of most hymenoptera
parasitoids occur in the hemocoel and are therefore subjected to the host en-
capsulation response. Encapsulation is typically prevented by the venom and
associated constituents (e.g. polydnaviruses, etc) injected during oviposition.
Dipteran parasitoids do not inject venom into host during oviposition, and
thus developing larvae must have other ways of countering the host’s immune
response. Two general strategies of physical avoidance of the host’s imm-
une system have apparently evolved repeatedly in the parasitic Diptera. Larvae
of many dipteran parasitoids (e.g. species in the Nemestrinidae, Acrocideae,
Bombyliidae, Cryptochetidae, some Calliphoridae, and most Tachinidae) main-
tain contact with outside air by attaching their posterior spiracles to the host’s
tracheal system or a hole in the integument (6, 34, 46). In many instances, the
larvae of these parasitoids turn the immune response of their host to their own
advantage by building a respiratory funnel from products of the host’s immune
response (133). The presence of such a respiratory funnel allows the developing
parasitoid continuous access to fresh air through the host’s tracheal system or
a hole in the host’s integument. In other species (e.g. some Tachinidae), larvae
move into a specific tissue (nerve ganglia, muscles, glands) and do not elicit
an immune response from the host. Larvae remain in these protected locations
until they are ready to consume the host. It is not yet known how the larvae
of the Phoridae, Pipunculidae, and Rhinophoridae avoid the immune system of
their hosts.
Larval development times vary widely both within and among families of
dipteran parasitoids. Some species delay their development and only kill the
host at or close to pupation. Others develop rapidly after oviposition, and still
others enter a true diapause and develop only after a change of seasons.
We have recently identified two different development strategies in the ant-
decapitating genus Apocephalus (Phoridae) (21, 22, 51–57, 118). Species spe-
cialized to grow on healthy hosts have a relatively slow rate of larval develop-
ment, taking two weeks or longer to complete larval development in the host’s
head capsule. During most of this period the host remains healthy and actively
engaged in its colony-related tasks. At the end of this period, the host is decap-
itated and pupation takes place in the now detached head capsule (116, 118).
Pupae appear to have specialized morphological features that allow them to
remain protected and undetected in the head capsule (118). In contrast, species
that specialize on injured, dead, or dying hosts have very rapid development,
with larvae leaving hosts within 4–5 days, crawling away from the host and
pupating in the soil (22). These developmental strategies are correlated with
several features involved in host location and clutch size, which suggests the
exploitation of two different adaptive syndromes, one associated with healthy
hosts and one associated with injured or dying hosts.
Another unique developmental feature found in dipteran parasitoids is the
emergence of some tachinids from living hosts (40, 49, 50). English Loeb et al
(50) reported that caterpillars of the arctiid moth Platyprepia virginalis not only
sometimes survived the emergence of the tachinid Thelairia bryanti, but were
also capable of eclosure as adults able to produce viable offspring. Although
probably rare, these instances of nonlethal parasitization may nonetheless have
important evolutionary consequences for hosts, a subject we address below.
PATTERNS OF HOST USE AND EVOLUTION OF HOST

SPECIFICITY
Dipteran parasitoids use a wider array of hosts than any other group of par-
asitoids, encompassing 22 orders distributed across 5 phyla (45, 46, 58). In
contrast, hosts of the more diverse parasitic Hymenoptera are restricted to 19
86 FEENER & BROWN
orders, all within the single phylum Arthropoda. Host associations unique to the
parasitic Diptera include terrestrial flatworms (order Tricladida), earthworms
(order Haplotaxida), freshwater and terrestrial pulmonate snails (orders Ba-
sommatophora and Stylommatophora), woodlice (order Isopoda), scorpions,
termites, and anurans. In some instances exploitation of these unusual hosts
evolved more than once. Terrestrial snails, for example, serve as hosts for species
in the Phoridae, Sciomyzidae, Calliphoridae, and Sarcophagidae. Use of mil-
lipedes as hosts has evolved at least four times within the Diptera (Phoridae,
Phaeomyiidae, Muscidae, and Sarcophagidae), only once in the Coleoptera and
never in the Hymenoptera. All of these unusual noninsect hosts are associated
with substrate-zone habitats (e.g. soil, leaf litter, or other organic matter on
the ground) and reflect the important role these habitats play in the evolution
of the parasitoid life-style within the Diptera (45). In contrast, evolution of
the parasitoid life-style in the Hymenoptera is closely tied to vegetation-zone
habitats (45, 64, 65), which offer little opportunity for the exploitation of such
soil-dwelling hosts (45).
Patterns of host use vary widely among the 21 dipteran families containing
parasitoids (45). Host use is broadest in those families with many evolutionary
origins of the parasitoid life-style. As a group, parasitoids in the Phoridae utilize
a greater taxonomic range of hosts than those in any other family (18, 42). A
majority of species attack adult ants or other aculeate Hymenoptera, but other
hosts include adult lampyrid beetles (19, 20); scales; termite soldiers, workers,
and young nymphs (41, 43); pupae of coccinellid beetles; the larvae of several
disparate dipteran families; millipedes; earthworms; and snails. Disney (42)
provides a comprehensive review of host relationships in the Phoridae. Host use
in the Sarcophagidae is nearly as broad as that found in the Phoridae (45, 58).
Hosts include a variety of insect families, as well as millipedes, earthworms,
and snails. At least one species appears to be an endoparasite of anurans (39).
While it is clear that the parasitoid life-style evolved many times within each
of these families, precise estimates of the numbers of times are impossible due
to the lack of detailed family-level phylogenies. Future systematic studies of
the multiple lineages of parasitoids within these families should help identify
any common initial conditions necessary for the evolution of the parasitoid
habit and the role of host constraints in governing the potential for subsequent
adaptive radiation.
Broad patterns of host use also occur in the Tachinidae. Unlike the Phoridae
and Sarcophagidae, however, this family is entirely parasitic, so diversification
of host use must have followed the acquisition of the parasitoid life-style. The
broad host range in tachinids is clearly related to the diversification of repro-
ductive strategies and host-location mechanisms found within the family (10,
11, 99, 106, 172). Tachinids also exploit insect herbivores to a far greater
extent than any other group of dipteran parasitoids (5, 45, 58, 79), and this
expansion into vegetative zone habitats must have led to an explosive increase
in the opportunities for host utilization. However, as with the Phoridae and
the Sarcophagidae, most noninsect hosts remain associated with the substrate
zone (45).
Most other families of dipteran parasitoids exploit a taxonomically restrictive
range of hosts (45). Families with the most limited range of hosts include the
Pipunculidae and Pyrgotidae (6, 34, 45). Members of these families possess
independently evolved piercing ovipositors, which they use to insert eggs into
the body of their hosts, often while in flight (6, 34, 45). Such specialized
structures and behavior suggest that the oviposition process may often limit
opportunities for host range expansion.
Evolution of resource (i.e. host) specificity has been reviewed recently in a
general ecological context by Futuyma & Morano (63) and in insect herbivores
by Jaenike (83). Evolution of host specificity in insect parasitoids is a complex
multifaceted problem, involving processes associated with both host-seeking
adults and developing larvae. Most research on evolution of host specificity in
the parasitic Hymenoptera has emphasized physiological and immunological
interactions between developing parasitoid larvae and their hosts as the ultimate
factor limiting host use (7, 8, 65, 68, 140). However, host use is equally
governed by the behavior of host-seeking adults (141). The host range of a
parasitoid can be influenced by the nature of the cues used by females in host
location (122, 141), or by the ability of females to overcome host defenses or
other barriers to host access during the process of oviposition (71). Host range
may be further modified by the mating system of the parasitoid. If males use
hosts as a means of finding receptive females, then the specificity of cues used
in host location by each sex may be reinforced by the other sex (115), leading
to increased host specificity and the potential for sympatric speciation (26, 35,
63).
Processes governing host specificity in dipteran parasitoids have received
only limited quantitative attention to date. Belshaw (11) examined the effects of
several life history characteristics on the level of polyphagy in the Tachinidae.
A high level of polyphagy in this family is significantly correlated with the
ability of larvae to physically avoid the host encapsulation response by building
a respiratory funnel or by moving to tissues incapable of an encapsulation
response (e.g. nerve ganglia, muscles, or glands). Many tachinid species
may therefore not depend strongly on biochemical adaptation to each host
species, allowing a high level of polyphagy. Members of many other families of
dipteran parasitoids also counter the encapsulation responses of hosts through
88 FEENER & BROWN
physical means (6, 34, 45, 46), which suggests that host ranges in dipteran
parasitoids are less constrained by larva-host interactions than those in the
parasitic Hymenoptera.
Several lines of evidence suggest that host specificity in dipteran parasitoids
is more often determined by the events leading up to oviposition, rather than by
the events occurring after oviposition. Several groups of dipteran parasitoids
attack adult insects that are highly mobile, agile, and often heavily armored
(e.g. Phoridae, Pipunculidae, Pyrgotidae, some Tachinidae). Utilization of
these hosts requires specifically modified ovipositors and specialized approach
behavior. Ovipositors of closely related phorid parasitoids, for example, are
often markedly different in structure and appear to correlate with structural
features of host ants. Moreover, to gain access to hosts, females of these para-
sitoids must evade both individual-level and colony-level defensive behaviors
that often vary among closely related species (52, 54, 55, 57). Host specificity
in this group is further reinforced through the use of species-specific commu-
nication signals of hosts by females seeking hosts and males seeking mates
(56). In many respects this host-parasitoid system is ideally suited for future
comparative and experimental studies of host specificity.
BEHAVIORAL INTERACTIONS IN AN ECOLOGICAL

AND EVOLUTIONARY CONTEXT
Interactions between host and parasitoid are often governed by specialized be-
havior associated with oviposition attack and parasitoid development. Studies
to date have focused on classifying and enumerating these behavioral mech-
anisms rather than considering their evolutionary and ecological implications
(68, 71). Behavioral interactions between host and parasitoid can have effects
at several levels of ecological organization with consequences that are both
wide-ranging and profound. In this section we illustrate some of the effects
dipteran parasitoids may have on the ecology and evolution of their hosts by
examples in three families: Conopidae, Tachinidae, and Phoridae.
A host newly infested with a parasitoid enters into a life and death struggle
over the control of its body. The nature of this struggle and its impending
outcome is often reflected in behavioral changes not seen in uninfested hosts.
A developing parasitoid may modify host behavior for its own advantage by
making the host move to a concealed location where it is protected against
predation and inclement weather (15–17, 62, 139, 147) or to a site that facilitates
parasitoid dispersal after emergence. Alternatively, changes in host behavior
may represent a defense reaction of the host that reduces the impact of parasitism
on itself or its kin (139, 144). Conspicuous behavioral changes that benefit the
host are more likely to occur in hosts that live in closely knit kin groups such
as the colonies of social insects (144) or in hosts with a chance to survive and
reproduce after the emergence of the parasitoid (49, 50).
Bumblebees parasitized by conopid flies undergo several behavioral changes,
some of which appear to benefit the host and others that benefit the parasitoid
(102–104, 120, 135, 136, 138). Parasitized foragers are less likely to return to
the nest at night than unparasitized ones. By remaining outside at night hosts
slow the rate of development of their parasitoid and thereby extend their lifetime
and the length of time they can forage usefully for the colony. This behavior
appears to be under the control of the host and benefits the well-being of the
colony at the expense of the parasitoid. When bees are near death, parasitized
individuals bury themselves in soil more often than unparasitized ones, which
reduces the likelihood that their bodies will be discovered by predators. This
behavior benefits the parasitoid but has no fitness consequences for the host. The
time course of these behavioral changes may vary with changes in the relative
fitness consequences to host and parasitoid. Behavioral changes occurring
shortly after parasitization usually favor the host, while those occurring later
tend to favor the parasitoid. Similar complex changes in host behavior may be
expected in other host-parasitoid systems involving social insects (e.g. phorid
parasitoids and host ants).
Behavioral changes in parasitized hosts may also benefit solitary hosts if
they are likely to survive parasitization and reproduce. English Loeb and his
colleagues (49, 50, 84) found that woolly bear caterpillars (P. virginalis) par-
asitized by the tachinid T. bryanti alter their host plant preference from bush
lupine (Lupinus arboreus) to poison hemlock (Conium maculatum). This host-
plant switch increases the probability that parasitized caterpillars will survive
to adulthood and produce viable offspring, and it may represent a form of
self-medication. This behavioral change thus appears to benefit the host (84).
Parasitoids not only alter the behavior of individual hosts but can also modify
behavioral interactions among individuals within populations. This is perhaps
best seen when parasitoids exploit sexual communication signals of hosts (3,
27–29, 74, 100, 169, 174). In these systems, only signal senders (usually males)
attract parasitoids and, as a result, often suffer much higher levels of parasitism
than signal receivers (usually females). High levels of mortality associated with
parasitism may select for reduced or modified signal output, but this selection
may be countered by a reduction in the ability to attract mates. The evolution
of alternative mating strategies is a likely outcome of such conflicting sele-
ction pressures. Male field crickets (Gryllus integer), for example, vary ge-
netically in the amount of time they devote to calling each night (29). Some
males call regularly and are very successful at attracting females and mating
90 FEENER & BROWN
with them. Other males (satellites) call infrequently, or not at all, and intercept
females attracted by the calling of neighboring males. These satellites have
lower reproductive success than calling males because they are less likely to
encounter receptive females (28). Calling males, however, are far more likely
to attract the acoustically orienting parasitoid O. ochracea and thus suffer much
higher levels of parasitism than satellites (28). Cade (29, 30) argued that yearly
variation in the frequency of parasitism by O. ochracea is a major force in
maintaining the underlying genetic variation in reproductive strategies of G.
integer.
Selection pressure from parasitoids may also alter the nature of the signal
itself. Zuk and her colleagues (129, 174, 175) compared the calling character-
istics of the cricket Teleogryllus oceanicus in native populations in the South
Pacific, where it is apparently unparasitized, against populations on Hawaii,
where it has been introduced along with the parasitoid O. ochracea. Relative
to native populations, Hawaiian populations of T. oceanicus show more trun-
cated calling periods and reduced song characteristics (e.g. pulse duration,
trill duration, inter-chirp interval, and inter-song interval), consistent with se-
lective pressure to reduce risky calling. Exactly how these changes affect the
attraction of phonotactic flies and sexually receptive females has yet to be deter-
mined. Similar selection pressures may operate in host species with chemically
based communication signals (3), but these systems have not been examined in
detail.
Behavioral interactions between hosts and parasitoids may also affect the or-
ganization of ecological communities (86). Several recent studies suggest that
specialized phorid parasitoids may frequently mediate the outcome of com-
petitive interactions among ant species (51, 54, 110, 119). Females of these
parasitoids are attracted to recruitment trails of host ant species and lay their
eggs in foraging workers. Larval development occurs in the head capsule of
hosts and eventually results in their decapitation, as detailed above (116, 118).
Ant species most likely to serve as hosts for phorid parasitoids are typically
dominant competitors that use nestmate recruitment to defend or usurp food
sources from other ant species (e.g. ants in the genera Camponotus, Pheidole,
Solenopsis, among others). Host ant species have evolved a variety of spe-
cialized behaviors to defend workers against ovipositing parasitoids (52, 53,
55, 109, 119), hitchhikers in leaf-cutting ants being a particularly spectacular
example (47, 57). Activation of these defense behaviors often interferes with
the ability of workers to harvest food sources or guard them against competing
species (51, 53–55, 57, 109, 110, 119). Thus, the mere presence of parasitoids
may be enough to alter the balance between competing ant species or the abil-
ity of a particular species to dominate local ecological interactions (51). These
systems are especially remarkable because the community-level consequences

of the parasitoids arise indirectly from the threat of parasitism rather than from
its actual frequency. This allows the influence of the parasitoids to be magnified
far beyond their abundance, and thus they serve as “keystone” species in ant
communities. Circumstantial evidence suggests that such processes may be
essential in understanding the invasion success of pest ant species such as the
red imported fire ant (51, 54, 110, 119).
ACKNOWLEDGMENTS
We thank DH Janzen, R Karban, JE O’Hara, D Robert, TJ Walker, DM Wood,
NE Woodley, and DK Yeates for reprints, unpublished manuscripts, and infor-
mation. We thank DD Judd for first suggesting that we undertake this review
and her continued enthusiasm for the project. We are also grateful to the Na-
tional Science Foundation for support during the preparation of this manuscript
(grant DEB-9528005 to DH Feener and grant DEB-9407190 to BV Brown).
SD Torti made many helpful comments on the manuscript.
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October 29, 1996 9:8 Annual Reviews FEENTEXT.

Annu. Rev. Entomol. 1997. 42:73–97

KEY WORDS: parasitoid, host relationships, parasitic Diptera, bionomics

74 FEENER & BROWN

TAXONOMY, BIOGEOGRAPHY, AND EVOLUTIONARY

76 FEENER & BROWN

the five major subfamilies of phorids recognized by Brown (18): Hypoceri-

INTERACTIONS BETWEEN ADULT PARASITOIDS

78 FEENER & BROWN

80 FEENER & BROWN

visually mediated learning under more natural circumstances remains to be

82 FEENER & BROWN

Evolution of the ability to discriminate between parasitized and unparasitized

84 FEENER & BROWN

we suspect that this “post-ovipositional host-guarding” behavior allows the

INTERACTIONS BETWEEN LARVAL PARASITOIDS

PATTERNS OF HOST USE AND EVOLUTION OF HOST

86 FEENER & BROWN

88 FEENER & BROWN

BEHAVIORAL INTERACTIONS IN AN ECOLOGICAL

90 FEENER & BROWN

systems are especially remarkable because the community-level consequences

92 FEENER & BROWN

94 FEENER & BROWN

69. Godfray HJC, Partridge L, Harvey PH. survival. Ecology. In press

96 FEENER & BROWN

7:794–98 1991. Parasitoid diets: Does superpara-

Semiochemicals and learning in para- parasitoid of field crickets. J. Insect Be-

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