Saxifragales

History

Saxifragales was first described in 1820 by Berchtold and Presl in 1820 as a group of plants, Saxifrageae, with five genera, including Saxifraga, lending their names as the botanical authority (Bercht. & J.Presl).^[8] At times, that authority has also been given to Dumortier, due to a later publication (1829). Dumortier first used the word Saxifragaceae.^[9] By the time of John Lindley's The Vegetable Kingdom (1853), the term Saxifragales was in use, which Lindley called an Alliance, containing five families.^[10] Later, the Saxifragales were placed in the angiosperm class Dicotyledons, also called Magnoliopsida.^[11]

Phylogeny

The order Saxifragales has undergone considerable revision in both placement and composition, since the use of molecular phylogenetics, and the use of the modern Angiosperm Phylogeny Group (APG) classification.^[1][12] They are identified as a strongly monophyletic group.^[13]

In the initial APG publication (1998), the Saxifragales were identified within the core eudicots clade but its relationship to other clades was uncertain. The core eudicots consist of the order Gunnerales and a large clade of Pentapetalae (so named for having a synapomorphy of pentamerous (5 part) perianths), the latter representing about 70% of all angiosperms, with eight major lineages.^[14][15] Later (2003), the order was described as "one of the major surprises of molecular phylogenetic analyses of the angiosperms", having elements previously placed in three or four separate subclasses based on morphology.^[16][3] This was eventually resolved in the third APG system (2009) placing Saxifragales as a sister group to the rosids (Rosidae), within the Pentapetalae clade.^[17][18][19] This large combination has subsequently been given the name superrosids (Superrosidae), representing part of an early diversification of the angiosperms.^[3][1][20] Among the rosids, they share a number of similarities with the Rosales, particularly Rosaceae, including a hypanthium, five part flowers and free floral parts.^[21] As circumscribed, Saxifragales account for 1.3% of eudicot diversity.^[22]

Biogeography and evolution

Diversification among Saxifragales was rapid, with the extensive fossil record^{[24][25][26][27][28][29]} indicating that the order was more diverse and more widespread than an examination of the extant members suggests, with considerable phenotypic diversity occurring early.^[2] The earliest fossil evidence is found in the Turonian-Campanian (late Cretaceous), suggesting a minimum age of 89.5 Myr. However, molecular divergence time estimation suggest an earlier time of 102–108 Myr, into the early Cretaceous, for the crown and stem groups respectively. Within the order Saxifragales, the molecular data imply a very rapid initial diversification time of about 6–8 Myr, between 112 and 120 Myr, with major lineages appearing within 3–6 Myr.^[30][3][31]

The ancestral state appears to be woody, as in Peridiscaceae and the woody clade, but is also ancestral to Grossulariaceae. A number of independent transitions to a herbaceous habit occurred in the ancestors of Crassulaceae, Saxifragaceae and the base of the Haloragaceae-Penthoraceae clade (the other two families in Haloragaceae s.l. remaining woody), while other taxa reverted to a woody habit, especially Crassulaceae. Most of Saxifragales have a superior ovary, but some families show frequent transition with inferior or subinferior position, particularly Saxifragaceae and to a lesser extent Hamamelidaceae. Almost all Grossulariaceae have an inferior ovary. The ancestral carpel number is two, with transition to higher numbers, such as four in Haloragaceae s.l. and Peridiscaceae with five in Penthoraceae. The ancestral carpel number for Crassulaceae is five, decreasing to four in Kalanchoe, where it is synapomorphic for the genus, though the most frequent transition in this family is 6–10, but only where stamen number is increased above five. Some Macaronesian taxa (Aeonieae) have 8–12, with up to 32 carpels for Aeonium.^[3]

The ancestral petal number is five, with three major transitions; 5 to 0, 5 to 4, 5 to 6–10. Increased petal number is seen in Paeoniaceae and Crassulaceae, particularly where stamen number is also increased. Cercidiphyllum + Daphniphyllum, Chrysosplenium and Altingia are examples of the complete loss of petals. The ancestral stamen:petal ratio is 1, with transitions characterising several clades, e.g. Paeonicaceae+woody clade >2, Crassulaceae 2 (but Crassula 1). Overall there has been a decrease over evolution, but independent of a decrease in petal number, so that it is the stamen number that has decreased.^[3] The ancestral habitat appears to be forests, followed by early diversification into desert and aquatic habitats, with shrubland the most recent colonization.^[2]

Species diversification was rapid following a transition from a warmer, wetter Earth in the Eocene (56–40 Myr) to early Miocene (23–16 Myr), to the cooler drier conditions of the mid-Miocene (16–12 Myr). However, this appears to not have coincided with ecological and phenotypic evolution, which are themselves correlated. There is a clear lag, whereby increase in species diversification was followed later by increases in niche and phenotypic lability.^[32]

Subdivision

The first APG classification (1998) placed 13 families within the order Saxifragales:^[33]

This was subsequently revised to 15, in the fourth version (2016).^[1] The Saxifragales families have been grouped into a number of informally named suprafamilial subclades, with the exception of the basal split of Peridiscaceae, which thus forms a sister group with the rest of Saxifragales. The two major ones are (Paeoniaceae + the woody clade of primarily woody families) and the "core" Saxifragales (i.e. the primarily herbaceous families), with the latter subdivided into two further subclades, (Haloragaceae sensu lato + Crassulaceae) and the Saxifragaceae alliance.^[3]

In the clade Haloragaceae sensu lato (s.l.) + Crassulaceae the genera constituting Haloragaceae s.l. are all small, and APG II (2003) proposed merging them into a single larger Haloragaceae s.l., but transferred Aphanopetalum from Cunoniaceae to this group.^[16] The Saxifragaceae alliance represents Saxifragaceae together with a number of woody members of the traditional Saxifragaceae sensu Engler (1930).^[34] Within this, APG II (2003) proposed placing the two species of Pterostemon that constitute Pterostemonaceae within Iteaceae, and all subsequent versions have maintained this practice.^[16] Thus Saxifragales sensu APG II consisted of only 10 families. The third version (2009) added Peridiscaceae (from Malpighiales), as sister to all other families, but re-expanded Haloragaceae to provide for a narrower circumscription, Haloragaceae sensu stricto (s.s.), to give a total of 14 families. APG IV (2016) added the parasitic family Cynomoriaceae to provide a total of 15 families, although its placement within the order remained unclear.^[35][1]

Of the 15 families included in APG IV, the basal divergence Peridiscaceae underwent radical shifting and recircumscription from 2003 to 2009. Originally, it consisted of two closely related genera, Peridiscus and Whittonia. The APG II system placed the family in Malpighiales, based on a DNA sequence for the rbcL gene from Whittonia. This sequence turned out to be not from Whittonia, but from other plants whose DNA had contaminated the sample.^[36] After placement in Saxifragales, it was expanded to include Soyauxia in 2007,^[37] and Medusandra in 2009.^[38]

In the first of the subclades of the remaining Saxifragales, Paeoniaceae possesses many unique features and its taxonomic position was controversial for a long time,^[39] and Paeonia was placed in Ranunculales, close to Glaucidium,^[40][41] prior to transfer to Saxifragales as sister to the woody clade.^[30][42]

In the woody clade, the genus Liquidambar was included in Hamamelidaceae until molecular phylogenetic studies showed that its inclusion might make Hamamelidaceae paraphyletic, and was segregated as a separate monotypic family, Altingiaceae in 2008.^[30] Cercidiphyllaceae was for a long time associated with Hamamelidaceae and Trochodendraceae and was often thought to be closer to the latter,^[43] which is now in the basal eudicot order Trochodendrales.^[44] Daphniphyllum was always thought to have an anomalous combination of characters^[45][45] and was placed in several different orders before molecular phylogenetic analysis showed it to belong to Saxifragales.^[46]

In the core Saxifragales, Crassulaceae^[47] and Tetracarpaeaceae^[48] have been associated with Saxifragaceae, while Penthorum has been associated both with Crassulaceae and Saxifragaceae,^[49] before being placed here. Aphanopetalum was often placed in Cunoniaceae, a family in Oxalidales, even though there were good reasons to put it in Saxifragales,^[50] and it was subsequently transferred.^[51] Haloragaceae was included in Myrtales,^[52] before being placed in Saxifragales.^[53]

The other "core" group, the Saxifragaceae alliance comprises four families: Pterostemonaceae, Iteaceae, Grossulariaceae, and Saxifragaceae,^[30] which have long been known to be related to each other, but the circumscription of Saxifragaceae has been much reduced and Pterostemonaceae submerged as Pterostemon in Iteaceae.^[54]

Most of the families are monogeneric. Choristylis is now considered a synonym of Itea, but the addition of Pterostemon, gives Iteaceae two genera.^[55] Liquidambar and Semiliquidambar are also submerged into Altingia, making Altingiaceae monogeneric.^[56][57] About 95% of the species are in five families: Crassulaceae (1400), Saxifragaceae (500), Grossulariaceae (150–200), Haloragaceae (150), and Hamamelidaceae (100).^[22][30][58]

The relationships of the Saxifragales families to each other is shown in the following cladogram. The phylogeny in this cladogram still has some uncertainty as to the exact relationships, and the phylogenetic tree is subject to further revision.^[59][60] Cynomoriaceae, previously placed in Santales or Rosales is included in Saxifragales, but unplaced within it. Li et al. (2019) have slightly different relationships, and also place Cynomoriaceae as the first branch in the Crassulaceae+Haloragaceae s.l. tree, i.e. as sister to those two families.^[31] The number of genera in each family is shown in parentheses:

Families

Peridiscaceae Main article: Peridiscaceae The Peridiscaceae (Ringflower family) are a small tropical family of 4 genera and 11–12 species of small trees and shrubs found in the Guiana Shield of S America (2 genera, one of which, Whittonia, is thought to be extinct) and West and Central Africa (2 genera). The majority of species occur in the African genus Soyauxia. The name comes from the Greek, peri (around) discos (ring).[6][61][21]

Paeoniaceae Main article: Paeoniaceae The Paeoniaceae (Peony family) consist of a single genus (Paeonia) with about 33 species of perennial herbs and small shrubs with showy flowers, found from the Mediterranean to Japan, but two species occur in western N America. They are commercially important as popular garden ornamentals, cultivated since antiquity, and have been used medicinally. The herbaceous varieties are derived from P. lactiflora, while the shrubs are derived from P. suffruticosa (tree peony), both Asian species. The botanical name comes from its Greek name, paionia, named in turn for the God Pan.[6][61][21]

Altingiaceae Main article: Altingiaceae The Altingiaceae (Sweetgum family) consist of a single genus (Liquidambar) with 15 species of trees with unisexual flowers found in Eurasia, but with one species in North and Central America, Liquidambar styraciflua (American sweetgum). Liquidambar is used for its resin and timber, as well being ornamental trees. The nominative genus and family are named after Willem Alting, and Liquidambar for liquid ambar, Arabic for the resin.[6][61][21]

Hamamelidaceae Main article: Hamamelidaceae The Hamamelidaceae (Witch-hazel family) consists of trees and shrubs with a widespread distribution, but main centres in East Asia and Malaysia. They are found in wet woodlands and forested slopes. The family has 26 genera and about 80–100 species, in five subfamilies, of which the nominative, Hamamelidoideae, contains over 75% of the genera. The species have uses as medicaments, timber and ornamental plants for their flowers, such as Hamamelis (witch hazel) or leaves, such as Parrotia persica (Persian ironwood). The family and nominative genus is named for the Greek hamamelis, the wych elm.[61][21][6]

Cercidiphyllaceae Main article: Cercidiphyllaceae The Cercidiphyllaceae (Caramel-tree family) are a small family of deciduous trees found in China and Japan, with a single genus, Cercidiphyllum and two species, C. japonicum and C. magnificum. The trees are valued for their wood (katsura) and as ornamentals. C. japonicum is the largest deciduous tree in Japan. The name is derived from the Greek words kerkis (poplar) and fyllon (leaf), from a supposed similarity in leaves.[61][21]

Daphniphyllaceae Main article: Daphniphyllaceae The Daphniphyllaceae (Laurel-leaf family) consist of a single genus, Daphniphyllum, with about 30 species. They are evergreen unisexual trees and shrubs distributed in SE Asia and the Solomon Islands. The dried leaves of Daphniphyllum macropodum[a] have been used for smoking in Japan and Siberia. The name is derived from the Greek words dafne (laurel) and fyllon (leaf), from a supposed resemblance to the leaves of the former (Laurus nobilis).[61][21]

Crassulaceae Main article: Crassulaceae The Crassulaceae (Orpine and Stonecrop family) are a medium size diverse and cosmopolitan family, that form the largest family within Saxifragales. They are mainly succulent, rarely aquatic, with a specialised form of photosynthesis (Crassulacean Acid Metabolism). Genera vary from 7 to 35, depending on the circumscription of the large genus Sedum, and there are about 1,400 species. Uses are diverse, including spices, medicaments and roof coverings as well as ornamental rock garden and household plants such as the S African Crassula ovata, the jade or money plant. The name is derived from the Latin, crassus (thick), referring to the fleshy leaves.[61][21][6]

Aphanopetalaceae Main article: Aphanopetalaceae The Aphanopetalaceae (Gum-vine family) consists of a single genus of Australian climbing shrubs, Aphanopetalum, which has two species, A. clematidium (SW Australia) and A. resinosum (Queensland, NSW). The name is derived from the Greek words afanos (inconspicuous) and petalon (petal).[61][21]

Tetracarpaeaceae Main article: Tetracarpaeaceae The Tetracarpaeaceae (Delicate-laurel family) is a very small evergreen Australian shrub family with a single genus, Tetracarpaea and a single species, T. tasmannica, confined to subalpine Tasmania. The name is derived from the Greek words tetra (four) and carpos (fruit), referring to the ovaries which have four carpels.[61][21][6]

Penthoraceae Main article: Penthoraceae The Penthoraceae (Ditch-stonecrop family) is a very small family of rhizomatous perennial herbs found in eastern N America and E Asia, in mainly wet environments. It consists of a single genus, Penthorum with two species, P. sedoides in N America and P. chinense from Siberia to Thailand. P. sedoides is used in aquaria and water gardens.[62] The name is derived from the Greek word pente (five) referring to the five-part fruit.[61][21][6]

Haloragaceae Main article: Haloragaceae The Haloragaceae (Water-milfoil family) is a small family of trees, shrubs, perennial, annual terrestrial, marsh and aquatic herbs with global distribution, but especially Australia. It consists of 9–11 genera and about 145 species. The largest genus is Gonocarpus with about 40 species. The major horticultural genus is Myriophyllum (watermilfoil) whose species are valued as aquaria and pond plants but may escape and naturalise, becoming invasive. Some cultivars of Haloragis are valued as ornamentals.[62] Only one genus, Haloragodendron, is a shrub and is confined to S Australia. The family and nominative genus, Haloragis are named from the Greek words halas (salt) and rhoges (berries).[61][21][6]

Iteaceae Main article: Iteaceae The Iteaceae (Sweetspire family) is a widespread small family of trees and shrubs, with 2 genera, and 18–21 species, found in tropical to northern temperate regions. The larger genus, Itea (c. 16 spp.) is more widespread, from the Himalayas to Japan and western Malesia and one species in eastern N America (I. virginica) whereas Pterostemon (c. 2 spp) is confined to Oaxaca, Mexico. I. virginica and I. ilicifolia, from China, are valued as ornamental shrubs. The name is derived from the Greek word itea (willow) for its rapid growth and similar leaf form.[61][21][6]

Grossulariaceae Main article: Grossulariaceae The Grossulariaceae (Gooseberry family) are shrubs that are usually deciduous. The single genus, Ribes, has about 150 species that are commercially important and widely cultivated for their fruit and also grown as ornamentals, such as R. uva-crispa (gooseberry) and R. nigrum (blackcurrant). They are found in temperate northern hemisphere regions but extending through the Andes into S America. The family name is derived from the Latin word grossulus (an unripe fig), and Ribes is Latinised from the semitic word ribas (acid taste).[61][21][6]

Saxifragaceae Main article: Saxifragaceae The Saxifragaceae (Saxifrage family) are mainly perennial herbs distributed throughout the Northern Hemisphere and Andes, and New Guinea, in damp woodlands and cooler northern regions, rarely aquatic, but are adapted to a wide range of moisture conditions. The family, greatly reduced, includes 35 genera and about 640 species, in two lineages, saxifragoids (e.g. Saxifraga, rockfoil) and heucheroids (e.g. Heuchera, coral bells). The largest genus is Saxifraga, the type genus (370 species), though several genera are monotypic. Saxifragaceae are the most horticulturally important of the herbaceous Saxifragales. They provide foodstuffs and medicaments and include many ornamentals, particularly of border, rock and woodland gardens, such as Astilbe, though the largest number of cultivated species belong to Saxifraga. The family and type genus name are derived from the two Latin words saxum (rock), and frango (to break), but the exact origin is unknown, although surmised to be either because of the ability of Saxifraga to grow in crevices in rocks or medicinal use for kidney stones.[61][21][6]

Cynomoriaceae Main article: Cynomoriaceae The Cynomoriaceae (Tarthuth or Maltese Mushroom family) consists of a single genus, Cynomorium with one or two species, C. coccineum (Mediterranean basin) and C. songaricum (central Asia and China; sometimes treated as a variety of C. coccineum). They are perennial bisexual herbaceous parasitic plants lacking chlorophyll, from deserts and arid regions. They have been harvested for food, as a dye and in traditional medicine. The name is derived from two Greek words kynos (dog), and morion (penis), for its shape.[61][21]