|Fig. 3. Biogeographic reconstruction for Hylarana s.l. Ball-and-stick model exported from Mesquite MLSAR analysis. The black star denotes the ancestral node for the ingroup Hylarana s.l. Biogeographic regions: A – Africa; B – South Asia (India, Nepal, Sri Lanka); C – Southeast Asia (Myanmar, Thailand, Cambodia, Vietnam, Laos, China, Malaysia, Java, Sumatra); D – Sulawesi; E – Philippines; F – Australasia.|
Numbers on nodes correspond to values in Table 4. Unnumbered nodes designate a probability of 1.00 for all three analyses for that biogeographic region. Island groups that are not colored, but fit within the known range, are excluded because of lack of samples from that locality/region. Assigned biogeographic regions are based on range of species and collection locality when range has slight overlap across biogeographic regions. DOI: 10.1016/j.ympev.2015.05.001
• Most inclusive phylogeny of Hylarana across Africa, Southeast Asia, and Australasia.
• 10 genera recognized from molecular clade diagnosis and morphology of vouchers.
• Biogeographic reconstructions indicate Southeast Asian origin ∼27 MYA with multiple Indian colonizations.
• Colonized New Guinea ∼11 MYA corresponding with formation of Vogelkop Peninsula.
• Colonized Africa from SE Asia ∼19 MYA representing overwater dispersal or a relict distribution.
We present an inclusive molecular phylogeny for Hylarana across its global distribution, utilizing two mitochondrial and four nuclear gene regions for 69 of the 97 currently described species. We use phylogenetic methods to test monophyly of Hylarana, determine relationships among ten putative subgenera, identify major clades, reconstruct biogeographic history, and estimate continental dispersal dates. Results support Hylarana as a monophyletic group originating approximately 26.9 MYA and comprising eight clades that partly correspond to currently described subgenera plus two new groups. The African and Australasian species each form clades embedded within a paraphyletic Southeast Asian group. We estimate that Africa and Australasia were colonized by Hylarana s.l. from SE Asia approximately 18.7 and 10.8 MYA, respectively. Biogeographic reconstructions also support three separate colonization events in India from Southeast Asia. Examination of museum specimens identified morphological characters useful for delineating subgenera and species. We herein elevate all supported subgenera to genus rank and formally describe two new genera to produce a revised taxonomy congruent with our new phylogenetic and biogeographic findings.
Keywords: Phylogenetics; Time calibration; Overwater dispersal; Taxonomy; Lydekker’s Line; Wallace’s Line
Frogs currently placed in Hylarana s.l. have been apportioned among a number of subgenera, most of these created recently (Dubois, 1992, Fei et al., 1990 and Fei et al., 2010). Our molecular analysis identifies a number of well-supported clades within Hylarana s.l. that correspond in varying degrees with several of these previously proposed subgenera while rejecting others. Our results now allow us to better sort among available morphological evidence to support formal recognition of several of these taxa. We believe that partition of Hylarana s.l. into multiple genera using these data better reflects the diverse biogeographic history of this large group than does retaining a single large genus spanning three continents. We expect it will also facilitate more-detailed investigations into these smaller clades. In particular, we believe that the two monophyletic invasions and radiations of Hylarana s.l. into Africa and Australasia over difficult-to-cross biogeographic barriers should be recognized taxonomically so as to emphasize the biological importance of those improbable events. Multiple invasions into India from southeastern Asia are also more easily highlighted and discussed with this revised taxonomic framework. Recognizing the African and Papuan clades, as well as the clades we retrieve that are clearly diagnosable morphologically, requires us to also taxonomically recognize a few additional clades that are more morphologically variable but supported by our molecular evidence so as to avoid leaving a paraphyletic Hylarana. Hence, we divide Hylarana s.l. into ten genera based on a combination of our monophyletic groupings, morphological diagnosability, biogeographical importance, and taxonomic precedence (Table 1 and Table 3).
We raise Amnirana, Chalcorana, Humerana, Pulchrana, Papurana, and Sylvirana (Dubois, 1992), and Hydrophylax (Fitzinger, 1843) to generic rank. We retain Hylarana for the clade containing H. erythraea, H. macrodactyla, H. taipehensis, and H. tytleri. We synonymize Boulengerana, Tenuirana, and Tylerana into Sylvirana, Hylarana, and Papurana, respectively. Additionally, we describe two new genera: one genus monotypic for Hylarana luctuosa, viz. Abavorana gen. nov., and the second, Indosylvirana gen. nov., containing H. flavescens plus H. aurantiaca, H. intermedia, H. milleti, H. montana, H. temporalis, and recently described Indian species (Biju et al., 2014). We tentatively assign untested species to clades based on suggestions of close relationships from the literature. However, these hypotheses need to be further tested with additional data for reliably identified voucher specimens. We briefly describe diagnostic morphological characters of each genus based on our voucher specimens (Table 3) and also from descriptions in the literature (Biju et al., 2014, Bortamuli et al., 2010, Boulenger, 1920, Brown and Guttman, 2002, Dubois, 1992 and Kraus and Allison, 2007). The characters described are put forward as a preliminary delineation and require further exploration within each genus.
Family Ranidae Rafinesque 1814
• Genus Abavorana gen. nov.
ETYMOLOGY: The name is derived from the Latin avus, meaning grandfather, the Latin prefix ab- indicating away or from (in the sense of prior to, in this case), and the Latin rana, meaning frog. The name can be interpreted, thus, as ancestral frog and is in recognition of this early phylogenetic separation from other frogs within our study clade.
TYPE SPECIES: Limnodytes luctuosus Peters, 1871 by monotypy.
MATERIAL EXAMINED: Abavorana luctuosa (FMNH 273219).
DIAGNOSIS: Abavorana can be diagnosed from other Hylarana s.l. by having the unique combination of absence of a vocal sac, small pale spots on body and limbs, shagreened dorsum, red coloration on the dorsum, and absence of rictal ridges and dorsolateral folds.
TAXONOMIC NOTES: Additional description of A. luctuosa in Boulenger (1920). This species was earlier assigned to Pulchrana by Dubois (1992), but has been found here and in other studies to represent a separate lineage sister to remaining taxa in Hylarana s.l. ( Pyron and Wiens, 2011 and Wiens et al., 2009).
RANGE: Disjunct distribution in peninsular Thailand, Malaysia, Sumatra, and Borneo (Frost, 2014).
• Genus Amnirana Dubois, 1992 stat. nov.:
TYPE SPECIES: Hylarana amnicola Perret, 1977 by original designation.
DEFINITION: All descendants of the most recent common ancestor of A. nicobariensis and A. amnicola. By implication, the African taxa Hylarana asperimma, H. fonensis, H. lemairei, H. longipes, H. occidentalis, and H. parkeriana are provisionally included in Amnirana.
MATERIAL EXAMINED: Amnirana amnicola (AMNH 117606, 117621, 122818), A. galamensis (AMNH 23543, MVZ 234148, 245225), A. lepus (CAS 249985, 249987, USNM 584220), and A. nicobariensis (MVZ 239177, FMNH 266995).
TAXONOMIC NOTES: We recognize this clade based on its monophyletic status and biogeographic cohesion and isolation. Data available at this time do not allow for a morphological diagnosis due to high variability within the clade. Dubois (1992) placed the African taxa into two different sections of his classification of Hylarana s.l. based on the presence or absence of distinct humeral glands. However, the body glands in this genus are highly variable among species and, hence, cannot serve to define this clade. Another character previously considered informative at higher taxonomic levels is expansion of the tips of the fingers into discs, and character states of this are highly variable in Amnirana, and plesiomorphic in ranids ( Scott, 2005). Furthermore, whether the posterior section of the abdominal skin is smooth or granular alternately occurs in different species of Amnirana (and differs across other clades of Hylarana s.l.) These variable characters partially explain why African Hylarana s.l. was placed into two sections in Dubois’ (1992) classification. Dubois (1992) placed A. galamensis with H. malabarica in Hydrophylax due to similar unexpanded discs. We did not find the Hydrophylax clade to be closely related to Amnirana in our molecular analysis. We included only five of 11 described species of Amnirana, and included Biju et al. (2014)’s Indian H. malabarica sequences from GenBank. Our molecular analysis could not refute the monophyly of African Amnirana, nor the position of A. nicobariensis (previously placed in Sylvirana) as sister to this African clade. We are hesitant to raise A. nicobariensis to separate generic status, given that the non-molecular synapomorphies of Amnirana are not clear and external morphology provides no diagnostic characters at present. We concede that there is a huge biogeographic gap between A. nicobariensis’ distribution and the rest of Amnirana. We defer any decision of excluding A. nicobariensis from Amnirana until further data are available to support a compelling decision. The range of variation in tadpole characters listed in Bortamuli et al. (2010) does not assist in explaining the placement of A. nicobariensis with the African species, but it is consistent with this placement.
RANGE: Western and central sub-Saharan Africa, and southern portions of the Horn of Africa, associated there with Central African Forests (Frost, 2014). Amnirana nicobariensis occurs in the Nicobar Islands, Peninsular Thailand, Sumatra, Java, Borneo, Sulu Archipelago, and Palawan ( Frost, 2014).
• Genus Chalcorana Dubois, 1992 stat. nov.:
TYPE SPECIES: Hyla chalconotus Schlegel, 1837 by original designation.
DEFINITION: All descendants of the most recent common ancestor of C. macrops and C. chalconota. By implication, Hylarana crassiovis, H. kampeni and H. scutigera are also provisionally included in Chalcorana.
MATERIAL EXAMINED: Chalcorana chalconota (AMNH 107901–11) C. eschatia (FMNH 268851, 268859), C. macrops (MVZ 254478), C. megalonesa (FMNH 235641, 268981), C. parvaccola (FMNH 268613), and C. rufipes (FMNH 26857, 268579, 268587).
DIAGNOSIS: Chalcorana can be diagnosed as the only genus of Hylarana s.l. with 1st finger ⩽ 2nd finger, disc size on fingers ⩾ 2x width of the finger, and humeral gland 1/3 to 1/2 length of humerus. Additionally, they have a gracile body shape and many accessory body glands.
RANGE: Southern and Peninsular Thailand, Java, Sumatra, West Malaysia, northern and western Borneo, and Sulawesi (Frost, 2014).
• Genus Humerana Dubois, 1992 stat. nov.:
TYPE SPECIES: Rana humeralis Boulenger, 1887 by original designation.
DEFINITION: All descendants of the most recent common ancestor of H. sp. 1 (USNM 583186) and H. humeralis. By implication, H. miopus and H. oatesii are also provisionally included in Humerana.
MATERIAL EXAMINED: Humerana oatesii (AMNH 45579), H. sp. 1 (USNM 583186), and H. sp. 2 (USNM 583170).
DIAGNOSIS: Humerana can be diagnosed by its unique combination of having a mid-dorsal color line, 1st finger > 2nd finger, and disc expansion roughly equal to that of the width of the fingers.
RANGE: Myanmar, Peninsular Thailand and Malaysia, northeastern India, Nepal, Bangladesh, and Bhutan (Frost, 2014).
• Genus Hydrophylax Fitzinger, 1843, stat. nov.:
TYPE SPECIES: Rana malabarica Tschudi, 1838 by original designation.
DEFINITION: All descendants of the most recent common ancestor of H. leptoglossa and H. malabarica.
MATERIAL EXAMINED: Hydrophylax gracilis (AMNH 76991–93, 77496, 74235–37, 74281–82, 76990, 77497, 83646), H. malabarica (AMNH 84587, 89797, 38080–84, 38086–89, 40055–67, 63507–08), and H. leptoglossa (AMNH 53080, CAS 239886).
DIAGNOSIS: Hydrophylax can be diagnosed by its unique combination of having a postocular mask (not as distinct as in Papurana), robust body, rear of thighs with strong vermiculations, large rictal gland, prominent humeral glad (but not as prominent as in morphologically similar Sylvirana), and circum-marginal grooves sometimes absent on finger 1.
RANGE: Sri Lanka, India, Bangladesh, southern Myanmar, and western Thailand (Frost, 2014).
• Genus Hylarana Tschudi, 1838 stat. nov.:
TYPE SPECIES: Hyla erythraea Schlegel, 1837 by original designation.
DEFINITION: All descendants of the most recent common ancestor of H. taipehensis and H. erythraea.
SYNONYMS: Tenuirana Fei et al., 1990 syn. nov. Type species Rana taipehensis Fei et al., 1990.
MATERIAL EXAMINED: Hylarana erythraea (AMNH 168529, 168530, FMNH 263289), H. macrodactyla (AMNH 26221, 180616–732, FMNH 255186, USNM 583138, 583140), H. taipehensis (AMNH 163972–73, 168753–54), and H. tytleri (CAS 247465, USNM 583188, 583190).
DIAGNOSIS: Hylarana can be diagnosed by its unique combination of lacking a mid-dorsal color line (present in morphologically similar Humerana), 1st finger subequal to second, and disc expansion of 1.2 to 1.7x the width of the finger.
TAXONOMIC NOTES: H. macrodactyla and H. taipehensis (the two species previously placed in Tenuirana) were considered to be part of Hylarana s.s. by Dubois (1992).
RANGE: Bangladesh, India, Nepal, Bhutan, Cambodia, Laos, Peninsular Malaysia, Myanmar, Thailand, Vietnam, Java, Penang Perak, Borneo, Singapore, Taiwan, and southern China (Frost, 2014). Hylarana s.s. (H. erythraea) has also been introduced to the Philippines ( Diesmos et al., 2002).
• Genus Indosylvirana gen. nov.
ETYMOLOGY: The generic name is Latin, in recognition that the geographic range of the clade is largely restricted to India and that all included species were formerly assigned to Sylvirana.
TYPE SPECIES: Rana flavescens Jerdon, 1853.
DEFINITION: All descendants of the most recent common ancestor of I. milleti and I. flavescens.
MATERIAL EXAMINED: Indosylvirana aurantiaca (AMNH 78924–25, 80086–67) and I. temporalis (AMNH 74217–18, 76988–89, 77490–95).
DIAGNOSIS: Indosylvirana can be diagnosed by its unique combination of having a postocular mask (faded and not as distinct as in Papurana), thin and well-defined dorsolateral folds, and prominent humeral gland extending along ¾ length of arm.
TAXONOMIC NOTES: We were unable to examine voucher specimens of I. milleti, and the diagnosis does not include information for this species. All species of Indosylvirana were previously assigned to Sylvirana by Dubois (1992) but are found to be a separate clade in our analysis.
RANGE: All species except I. milleti are restricted to India and Sri Lanka. Indosylvirana milleti is located in southern Vietnam, southern Thailand, and southwestern Cambodia ( Frost, 2014).
• Genus Papurana Dubois, 1992 stat. nov.:
TYPE SPECIES: Rana papua Lesson, 1826 by original designation.
DEFINITION: All descendants of the most recent common ancestor of P. daemeli and P. papua. By implication, New Guinean taxa H. grisea and H. novaeguineae are provisionally included in Papurana as all other New Guinean species of Hylarana s.l. are representatives of Papurana, and these species are morphologically similar to the remaining members of the genus. Dubois (1992) also placed H. elberti, H. florensis, and H. moluccana in Papurana. This hypothesis needs further testing using both molecular and morphological data, but we provisionally include them in Papurana.
SYNONYMS: Tylerana Dubois, 1992 syn. nov. Type species Rana jimiensis Tyler, 1963.
MATERIAL EXAMINED: Papurana arfaki (AMNH 79933–34, 191673), P. daemeli (AMNH 74863–68, 81292–93), P. garritor (AMNH 131003), P. jimiensis (AMNH 84583) P. kreffti (AMNH 35404), P. novaeguineae (AMNH 84566), P. papua (AMNH 98992–93), and P. supragrisea (AMNH 66616).
DIAGNOSIS: Papurana can be diagnosed by the unique combination of having a postocular eye mask, robust body shape, rear of thighs with strong vermiculations, and dorsolateral folds either absent or thin, with asperities.
TAXONOMIC NOTES: Kraus and Allison (2007) recorded various characters to distinguish among species of New Guinean Hylarana. Papurana jimiensis and P. arfaki were originally assigned to Tylerana by Dubois (1992). The greatest morphological variation in this genus exists between (P. arfaki + P. jimiensis) and all other New Guinean species of Papurana.
RANGE: New Guinea; D’Entrecasteaux Islands; Sudest, Louisiade Islands; Aru Islands; New Hanover Island; New Britain; Yapen; Seram; Manus; Waigeo; Solomon Islands; New Ireland; Cape York Peninsula, northeastern Queensland, Australia; and northeastern border of the Gulf of Carpentaria, Northern Territory, Australia (Frost, 2014). The ranges of the provisionally included species (P. elberti, P. florensis, and P. moluccana) include Flores, Sumba, Timor, Wetar, Babar, Tanimbar, Lombok, and Moluccas.
• Genus Pulchrana Dubois, 1992 stat. nov.:
TYPE SPECIES: Polypedates signatus Günther, 1872 by original designation.
DEFINITION:All descendants of the most recent common ancestor of P. baramica and P. signata. By implication, H. centropeninsularis and H. debussyi are also provisionally included in Pulchrana.
MATERIAL EXAMINED: Pulchrana baramica (AMNH 90514–17; FMNH 248217, 266574, 266927), P. glandulosa (AMNH 90542–49), P. picturata (FMNH 245786, 266946), P. signata (AMNH 90592–99, FMNH 273117, 269721), and P. similis (FMNH 266275).
DIAGNOSIS: Pulchrana can be diagnosed by its unique combination of weakly or strongly warty skin; a mottled to spotted dorsum, sometimes with bright coloration; fine or warty dorsolateral folds, also sometimes with bright coloration; and a large outer metatarsal tubercle.
TAXONOMIC NOTES: Brown and Guttman (2002) previously examined the Pulchrana signata complex using morphology and molecules. With the exception of Abavorana luctuosa, our study supports the original delineation of Pulchrana ( Dubois, 1992).
RANGE: Southern Vietnam, Peninsular Thailand, Peninsular Malaysia, Java, Borneo, Siberut Island, Sumatra, Singapore, Bangka Island, Natuna Islands, Sulu Archipelago, and the Philippines (Frost, 2014).
• Genus Sylvirana Dubois, 1992 stat. nov.:
TYPE SPECIES: Lymnodytes nigrovittatus Blyth, 1856 by original designation.
DEFINITION: All descendants of the most recent common ancestor of S. spinulosa and S. nigrovittata. Hylarana hekouensis and H. menglaensis were described as part of the S. nigrovittata group ( Fei et al., 2008) and are also provisionally placed in Sylvirana. We were unable to include in our analyses several other mainland Southeast Asian and Indian species that have also been placed in Sylvirana. For these species, it is necessary to further test their taxonomic placement. It is likely, for instance, than one or more (especially among the Indian species) may be more closely related to Indosylvirana or Hydrophylax. These species are H. attigua, H. celebensis, H. chitwanensis, H. garoensis, H. lateralis, H. latouchii, H. margariana, and H. montivaga. We consider these incertae sedis.
SYNONYMS: Boulengerana Fei et al., 2010 syn. nov. Type species Rana guentheri Boulenger, 1882.
MATERIAL EXAMINED: Sylvirana cubitalis (CAS 210634, FMNH 265818, 270736), S. guentheri (AMNH 16190, 161462–63, 163940–42), S. mortenseni (FMNH 263303), S. nigrovittata (AMNH 161270–75, USNM 583124–25, 583178), and S. spinulosa (MVZ 236683).
DIAGNOSIS: Similar to Indosylvirana, Hydrophylax, and Papurana, Sylvirana can be diagnosed by its unique combination of having a postocular eye mask, robust body shape, rear of thighs with strong vermiculations, thick dorsolateral folds, and a humeral gland that is less prominent than that seen in Indosylvirana, but more prominent than those in Hydrophylax and Papurana. It can be differentiated from Papurana based on thicker and better-developed dorsolateral folds, less developed postocular mask, and more prominent humeral gland; from Hydrophylax by its smaller rictal ridge, generally larger discs on the fingers, and more prominent humeral gland; and from Indosylvirana by its thicker dorsolateral folds and less prominent humeral gland.
TAXONOMIC NOTES: Sylvirana guentheri was the only species assigned to Boulengerana. We synonomize it with Sylvirana because it falls within that clade.
RANGE: Mainland China, Hainan Island, Taiwan, Myanmar, Thailand, Laos, Cambodia, Vietnam, Bhutan, Nepal, Bangladesh, and West Bengal (Frost, 2014).
Lauren A. Oliver, Elizabeth Prendini, Fred Kraus and Christopher J. Raxworthy. 2015. Systematics and Biogeography of the Hylarana Frog (Anura: Ranidae) Radiation Across Tropical Australasia, Southeast Asia, and Africa.
Mol. Phylogenet. Evol. (2015), DOI: 10.1016/j.ympev.2015.05.001
Mol. Phylogenet. Evol. (2015), DOI: 10.1016/j.ympev.2015.05.001