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| Members of the new genus Nanohyla gen. nov. in life (males): N. annectens from Genting Highlands, Pahang, Malaysia, N. annamensis from Bidoup – Nui Ba N.P., Lam Dong, Vietnam, N. arboricola from Chu Yang Sin N.P., Dak Lak, Vietnam, N. hongiaoensis from Bidoup – Nui Ba N.P., Lam Dong, Vietnam, N. marmorata from Kon Chu Rang N.R., Gia Lai, Vietnam, N. nanapollexa from Kon Plong, Kon Tum, Vietnam, N. perparva from Gunung Mulu, Sarawak, Malaysia, N. petrigena from Gunung Mulu, Sarawak, Malaysia and N. pulchella from Bidoup – Nui Ba N.P., Lam Dong, Vietnam. in Gorin, Scherz, Korost & Poyarkov, 2021. DOI: 10.3897/zse.97.57968 Photos by Nikolay A. Poyarkov, Vu Dang Hoang Nguyen and Indraneil Das. |
Abstract
The genus Microhyla Tschudi, 1838 includes 52 species and is one of the most diverse genera of the family Microhylidae, being the most species-rich taxon of the Asian subfamily Microhylinae. The recent, rapid description of numerous new species of Microhyla with complex phylogenetic relationships has made the taxonomy of the group especially challenging. Several recent phylogenetic studies suggested paraphyly of Microhyla with respect to Glyphoglossus Günther, 1869, and revealed three major phylogenetic lineages of mid-Eocene origin within this assemblage. However, comprehensive works assessing morphological variation among and within these lineages are absent. In the present study we investigate the generic taxonomy of Microhyla–Glyphoglossus assemblage based on a new phylogeny including 57 species, comparative morphological analysis of skeletons from cleared-and-stained specimens for 23 species, and detailed descriptions of generalized osteology based on volume-rendered micro-CT scans for five species–altogether representing all major lineages within the group. The results confirm three highly divergent and well-supported clades that correspond with external and osteological morphological characteristics, as well as respective geographic distribution. Accordingly, acknowledging ancient divergence between these lineages and their significant morphological differentiation, we propose to consider these three lineages as distinct genera: Microhyla sensu stricto, Glyphoglossus, and a newly described genus, Nanohyla gen. nov.
Key Words: Amphibians, integrative taxonomy, narrow-mouthed frogs, micro-computed tomography, Nanohyla gen. nov, osteology, sexual dimorphism, taxonomic revision
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| Figure 1. Distribution ranges of the three clades of the Microhyla–Glyphoglossus assemblage. Distribution area of Microhyla I is shown in yellow, of Microhyla II in red, and of Glyphoglossus in blue. Distributional data from Gorin et al. (2020). Question mark denotes the unconfirmed record of “Microhyla annamensis” from Khao Sebab in eastern Thailand by Taylor (1962). |
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| Figure 11. Members of the new genus Nanohyla gen. nov. in life (males): N. annectens from Genting Highlands, Pahang, Malaysia (A), N. annamensis from Bidoup – Nui Ba N.P., Lam Dong, Vietnam (B), N. arboricola from Chu Yang Sin N.P., Dak Lak, Vietnam (C), N. hongiaoensis from Bidoup – Nui Ba N.P., Lam Dong, Vietnam (D), N. marmorata from Kon Chu Rang N.R., Gia Lai, Vietnam (E), N. nanapollexa from Kon Plong, Kon Tum, Vietnam (F), N. perparva from Gunung Mulu, Sarawak, Malaysia (G), N. petrigena from Gunung Mulu, Sarawak, Malaysia (H), and N. pulchella from Bidoup – Nui Ba N.P., Lam Dong, Vietnam (I). Insets show tympanic area of the each species; white arrow points at the tympanic rim of the external tympanum. Photos by Nikolay A. Poyarkov (A–С, D–F, I), Vu Dang Hoang Nguyen (D), and Indraneil Das (G, H). |
Nanohyla Poyarkov, Gorin & Scherz, gen. nov.
Chresonymy: Microhyla (partim)–Boulenger 1900; Smith 1923; Inger and Frogner 1979; Inger 1989; Bain and Nguyen 2004; Poyarkov et al. 2014; Hoang et al. 2020.
Microhyla (Microhyla) (partim)–Dubois 1987 (as a part of the subgenus Microhyla).
Type species: Microhyla annectens Boulenger, 1900.
Etymology: The genus name is derived from the Greek νᾶνος (nanos), meaning “dwarf”, “pygmy”, and the mythological figure, Hylas (Ancient Greek: Ὕλας), which is probably derived from the Ancient Greek verb “ὕλαω” meaning “to bark” (Bourret 1942). In classical mythology, Hylas, son of King Theiodamas, was a youth who served as Heracles’ companion, lover, and servant. Heracles took Hylas with him on the Argonauts’ expedition, during which Hylas was kidnapped by nymphs of the spring in Pegae, Mysia, and turned into an echo. Heracles left the ship and was searching for Hylas for a great length of time, calling his name: “His adjunxit Hylan nautae quo fonte relictum / Clamassent ut littus Hyla! Hyla! omne sonaret” (“The mariners cried on Hylas till the shore / Then Re-echoed Hylas! Hylas! soothed...”; Virgil 1916, Ecl. 6, 43). The genus name refers to the small body size (< 25 mm) of all known Nanohyla species, while maintaining resemblance to its sister genus Microhyla, from which it is separated herein. The new genus name is feminine in gender.
Suggested common name: Pygmy Narrow-mouthed Frogs.
Taxonomic content:
Nine species, including: Nanohyla annamensis comb. nov. (Smith, 1923); Nanohyla annectens comb. nov. (Boulenger, 1900); Nanohyla arboricola comb. nov. (Poyarkov, Vassilieva, Orlov, Galoyan, Tran, Le, Kretova & Geissler, 2014); Nanohyla hongiaoensis comb. nov. (Hoang, Nguyen, Luong, Nguyen, Orlov, Chen, Wang & Jiang, 2020); Nanohyla marmorata comb. nov. (Bain & Nguyen, 2004); Nanohyla nanapollexa comb. nov. (Bain & Nguyen, 2004); Nanohyla petrigena comb. nov. (Inger & Frogner, 1979); Nanohyla perparva comb. nov. (Inger & Frogner, 1979); and Nanohyla pulchella comb. nov. (Poyarkov, Vassilieva, Orlov, Galoyan, Tran, Le, Kretova & Geissler, 2014).
Nanohyla annamensis (Smith, 1923);
Nanohyla annectens (Boulenger, 1900);
Nanohyla arboricola (Poyarkov, Vassilieva, Orlov, Galoyan, Tran, Le, Kretova & Geissler, 2014);
Nanohyla hongiaoensis (Hoang, Nguyen, Luong, Nguyen, Orlov, Chen, Wang & Jiang, 2020);
Nanohyla marmorata (Bain & Nguyen, 2004);
Nanohyla nanapollexa (Bain & Nguyen, 2004);
Nanohyla petrigena (Inger & Frogner, 1979);
Nanohyla perparva (Inger & Frogner, 1979);
Nanohyla pulchella (Poyarkov, Vassilieva, Orlov, Galoyan, Tran, Le, Kretova & Geissler, 2014).
Diagnosis: The new genus is assigned to the subfamily Microhylinae on the basis of phylogenetic affinities and the following combination of morphological character states: vomers small, confined to the anterior and medial margins of choanae; clavicles and, in most cases, procoracoids absent, maxillary arcade edentate (Parker 1934). Nanohyla gen. nov. differs from other Microhylinae genera by the following combination of osteological character states: (1) frontoparietals fused with exoccipitals; (2) exoccipitals fused with each other (incomplete fusion in N. pulchella); (3) neopalatines present; (4) sphenethmoids completely fused with parasphenoid (incomplete fusion in N. pulchella); (5) crista parotica entirely cartilaginous; (6) otic ramus of squamosal well-developed; (7) tympanic annulus well-developed; (8) transverse processes of presacral vertebrae with the following orientation: IV and V posterolaterally, II, VII and VIII anterolaterally, III and VI at right angle to body axis; (9) clavicles absent; (10) omosternum present, cartilaginous; (11) prehallux cartilaginous; (12) terminal phalanges of longest fingers and toes T-shaped. The combination of diagnostic external morphological characters includes: (13) small to extremely small frogs (adult SVL 11.8–25.8 mm); (14) snout rounded or pointed in profile; (15) supratympanic fold present; (16) ridge on posterior sides of choanae absent; (17) first finger (FI) length less than ½ FII or reduced to a nub; (18) finger discs present, at least on FII–FIV; (19) dorsal median longitudinal grooves on finger discs generally present (with the exception of N. perparva); (20) toes dorsolaterally flattened, prominent discs present; (21) dorsal median longitudinal grooves on toe discs present; (22) metatarsal tubercle single (inner metatarsal tubercle present, outer absent); (23) dorsomedial line absent; (24) superciliary tubercles absent; (25) tibiotarsal articulation of adpressed hindlimb reaching well beyond snout; (26) toe webbing well-developed (at least one-half webbed); (27) skin on dorsum feebly granular to tubercular; (28) tympanum externally distinct at least in males (N. annamensis, N. annectens, N. arboricola, N. marmorata, N. nanapollexa, N. pulchella) or barely distinct (N. hongiaoensis, N. perparva, N. petrigena); (29) terrestrial or scansorial semi-arboreal microhabitat preference.
Phylogenetic definition: The genus Nanohyla gen. nov. includes all species sharing a more recent common ancestor with Nanohyla annectens than with Microhyla achatina and Glyphoglossus molossus.
Distribution: The distribution area of Nanohyla gen. nov. covers montane forests of the Annamite (Truong Son) Mountains in Vietnam, eastern Laos, and north-eastern Cambodia, the Titiwangsa Mountain Range in the southernmost Thailand and peninsular Malaysia, mountains of Borneo (including Sabah and Sarawak of Malaysia, Brunei, and Kalimantan of Indonesia) and the Sulu Archipelago of the Philippines (see Fig. 1). The occurrence of Nanohyla gen. nov. in Cardamom Mountains in eastern Thailand (the record of “M. annamensis” from Khao Sebab by Taylor [1962], see Fig. 1) is questionable (see Poyarkov et al. 2014, 2020a).
Conclusions:
Miniaturized amphibians are characterized by a high proportion of cryptic species, along with numerous anatomical homoplasies, muddying our estimates of their evolutionary relationships and diversity (e.g., Hanken and Wake 1993; Rovito et al. 2013; Parra-Olea et al. 2016; Rakotoarison et al. 2017; Scherz et al. 2019; Gorin et al. 2020). Integrative taxonomic approaches, optimally combining the results of molecular phylogenetic analyses with morphological, acoustic and behavioral data, represent the most promising approach for better understanding of species boundaries, diversity and evolutionary relationships in microhylid frogs, including the genus Microhyla (Hasan et al. 2014; Garg et al. 2019; Poyarkov et al. 2018a, 2019; Gorin et al. 2020). Many recent phylogenetic studies of miniaturized frogs demonstrate that the diversity of these groups is unexpectedly high, at both the species and supraspecific levels, due to a combination of overlooked diversity (cryptic species) and microendemism (Oliver et al. 2017; Rakotoarison et al. 2017; Clemente-Carvalho et al. 2011; Poyarkov et al. 2018a; Zimkus et al. 2012; Blackburn et al. 2008; Lourenço-de-Moraes et al. 2018; Rodriguez et al. 2013; Köhler et al. 2008; Scherz et al. 2019). The present analysis of the Microhyla–Glyphoglossus assemblage diversity represents a case in point: miniaturized taxa, that were previously assigned ad hoc to Microhyla s. lat., were demonstrated to belong to two deeply divergent clades, together closely related to the genus Glyphoglossus, which consists of species of a much larger body size and very different ecology. Upon closer examination of their phylogenetic relationships from molecular data, as well as morphology, ecology, and biogeography, we found that these deep clades were older than most other Microhylinae genera, and sufficiently different to justify recognition as distinct genera. This yielded the new genus Nanohyla gen. nov. described herein. This result further underlines the importance of genetic data, useful for independently elucidating diversity and evolutionary relationships within groups with extensive homoplasies (Mott and Vieites 2009; Heideman et al. 2011; Scherz et al. 2019).
The Microhyla–Glyphoglossus assemblage (perhaps better now called the Microhyla–Nanohyla–Glyphoglossus assemblage) shows highly dynamic body size evolution, and a propensity to miniaturize, with at least nine separate miniaturization events inferred across Microhyla and the new genus Nanohyla. Convergence in body size in these two genera has generated some homoplasies, but both have unique, apomorphic features. It is clear, however, that, in order to gain a comprehensive understanding of the evolution of miniaturization in these frogs, much more extensive sampling of outgroups is needed. The Microhylidae, however, form an ideal group in which to study the evolution of miniaturization, which is one of several phylogenetically recurring frog ecomorphs (Moen et al. 2015).
Vladislav A. Gorin, Mark D. Scherz, Dmitriy V. Korost and Nikolay A. Poyarkov. 2021. Consequences of Parallel Miniaturisation in Microhylinae (Anura, Microhylidae), with the Description of A New Genus of Diminutive South East Asian Frogs. Zoosystematics and Evolution. 97(1): 21-54. DOI: 10.3897/zse.97.57968
