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. 2021 Jul 18;42(4):389–400. doi: 10.24272/j.issn.2095-8137.2021.039

Phylogenetic and morphological significance of an overlooked flying squirrel (Pteromyini, Rodentia) from the eastern Himalayas with the description of a new genus

Quan Li 1,13,#, Feng Cheng 1,12,#, Stephen M Jackson 2,3,4,5,#, Kristofer M Helgen 3,5, Wen-Yu Song 6,1, Shao-Ying Liu 7, Daosavanh Sanamxay 8, Song Li 1,9, Fei Li 10, Yun Xiong 11, Jun Sun 11, Hong-Jiao Wang 1, Xue-Long Jiang 1,*
PMCID: PMC8317177  PMID: 34047079

Abstract

The flying squirrels (Pteromyini, Rodentia) are the most diverse and widely distributed group of gliding mammals. Taxonomic boundaries and relationships within flying squirrels remain an area of active research in mammalogy. The discovery of new specimens of Pteromys (Hylopetes) leonardi Thomas, 1921, previously considered a synonym of Hylopetes alboniger, in Yunnan Province, China allowed a morphological and genetic reassessment of the status of this taxon. Phylogenetic reconstruction was implemented using sequences of two mitochondrial (12S ribosomal RNA and 16S ribosomal RNA) and one nuclear (interphotoreceptor retinoid-binding protein) gene fragments. Morphological assessments involved examinations of features preserved on skins, skulls, and penises of museum specimens, supplemented with principal component analysis of craniometric data. Together these assessments revealed that this taxon should be recognized not only as a distinct species, but should also be placed within a new genus, described here as Priapomysgen. nov.

Keywords: Eastern Himalayas, Flying squirrel, Penis, Priapomys, Pteromyini, New genus, Systematics, Taxonomy

INTRODUCTION

Flying squirrels (Pteromyini, Rodentia) are the most diverse lineage of gliding mammals. Extant species range in size from pygmy flying squirrels (Petaurillus, 13.5 g) to giant flying squirrels (Petaurista, 2 710 g) (Thorington et al., 2012) and occur in forests in Europe, Asia, and North America. Their distribution ranges from tropical lowlands to taiga, even to above the tree-line within the Himalayas (Jackson & Schouten, 2012).

The taxonomic history of flying squirrels is convoluted and unstable, with major taxonomic changes being reviewed by Thorington et al. (2002) and Jackson & Thorington (2012). Current taxonomy tentatively recognizes 56 living species in 15 genera (Arbogast et al., 2017; Jackson & Schouten, 2012; Jackson & Thorington, 2012; Jackson et al., 2021; Koprowski et al., 2016; Li et al., 2019; Thorington et al., 2012) as well as 70 fossil species placed both in extant genera and 19 extinct genera (Jackson & Thorington, 2012; Lu et al., 2013; Qiu, 2019; Tiunov & Gimranov, 2019). Until recently most taxonomic revisions were mainly based on morphological comparisons rather than the phylogenetic analysis of genetic data.

In this paper we review the taxonomic status of a largely overlooked flying squirrel taxon, Pteromys (Hylopetes) leonardi, which was described by Thomas (1921) based on a single specimen collected from Kachin State in northern Myanmar. Subsequently, Pocock (1923) recognized Hylopetes as a genus distinct from Pteromys, and leonardi was recognized as a valid species within Hylopetes by Ellerman (1940). This taxon was treated as a subspecies of H. alboniger (without critical review or analysis) by Ellerman & Morrison-Scott (1951), Ellerman (1961), Yin (1967), Wang (2003), Smith & Xie (2008) and Thorington et al. (2012), and synonymized entirely with H. alboniger by Corbet & Hill (1992), Thorington & Hoffmann (2005), and Jackson & Thorington (2012). The taxon leonardi was previously known only by the holotype (lodged at the Natural History Museum, London, catalogue number 20.8.8.2), which does superficially resemble specimens of Hylopetes alboniger, and no morphological and genetic assessments involving the holotype of leonardi have since been published.

During field studies conducted between 2014 and 2016 on Mount Gaoligong, in the western part of Yunnan Province, China, five specimens of a flying squirrel morphologically very similar to “P. (H.) leonardi” were collected. Subsequently, we also identified another eight specimens similar to “P. (H.) leonardi” from northwest Yunnan Province within the collections of the Kunming Institute of Zoology (Chinese Academy of Sciences) and Dali University. Our initial genetic analysis revealed that these “P. (H.) leonardi” specimens (Yunnan population, hereafter) were most closely related, albeit with a deep genetic divergence, to species within the Sundaland endemic genus Iomys, rather than to species of Hylopetes. Therefore, the aims of this study were to: (1) determine whether these Yunnan specimens belong to the same species as the holotype of leonardi, (2) undertake a comprehensive morphological and genetic study to clarify the taxonomic status of leonardi, and (3) recommend changes to its taxonomic status if appropriate.

MATERIALS AND METHODS

Ethics statement

Methods for all animal research undertaken for this study were approved by the Animal Ethics Committee of the Kunming Institute of Zoology, Chinese Academy of Sciences (approval ID: SMKX2018021).

Morphological techniques

We examined 469 specimens of flying squirrels that included all living species except Hylopetes winstoni and Petaurillus emiliae (Supplementary Text). Museum collections that were accessed to examine these specimens included the American Museum of Natural History, New York, United States (AMNH); Natural History Museum, London, United Kingdom (BMNH); Dali University, Dali, Yunnan Province, China (DU); Field Museum, Chicago, United States (FMNH); Kunming Natural History Museum of Zoology, Kunming Institute of Zoology (KIZ), Chinese Academy of Sciences (CAS), Kunming, Yunnan Province, China; Muséum National d’Histoire Naturelle, Paris, France (MNHN); National Museum of Natural History, Smithsonian Institution, Washington DC, United States (USNM); Naturalis Museum, Leiden, Netherlands (NML); Zoological Collection of the Faculty of Environmental Sciences, National University of Laos, Vientiane, Lao PDR (NUoL); and Zoological Collection of the Zoological Survey of India, Kolkata (Calcutta), India (ZSI).

Terminology of cheekteeth

Dental abbreviations in the text are: P for premolars, M for molars, superscript (Px, Mx) for upper premolars and upper molars, subscript (Px, Mx) for lower premolars and lower molars. Dental observations were made under a light microscope (Keyence digital microscope system VHX-2000C with 50X Kenyence VH-Z00R lens, Japan). Terminology for cheekteeth occlusal morphologies is modified from Zhou et al. (1975), Kawamura (1988), Tong (2007), Li et al. (2019), Qiu (2019), and Jackson et al. (2021) (Figure 1); equivalents of terms used by other authors are given in Supplementary Table S1.

Figure 1.

Figure 1

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Terminology of four typical kinds of upper cheekteeth (above) and lower cheekteeth (bottom) of living flying squirrels

“Eupetaurus form” (Eupetaurus only), “Petaurista form” (Petaurista and Aeretes), “Trogopterus form” (Trogopterus, Belomys, and Pteromyscus), and “Hylopetes form” (Eoglaucomys, Glaucomys, Hylopetes, Petaurillus, Petinomys, and Pteromys (Hylopetes) leonardi (=Priapomys gen. nov.)); the cheekteeth of Pteromys are closest to the Petaurista form but simplified; the cheekteeth of Biswamoyopterus, Aeromys, and Iomys are closest to the Hylopetes form but with some modification. Abbreviations for upper molars: Paracone (pa), metacone (me), protocone (pr), hypocone (hy), parastyle (past), mesostyle (msst), paraconule (pacu), metaconule (mecu), anteroloph (anl), paraloph (pal), metaloph (mel), posteroloph (pol), endoloph (enl), mesolophule (mslu), anterolophule (anlu), preparaconule crista (prepalc), postmetaconule crista (pomelc), anterior valley (av), central valley (cv), posterior valley (pv), anterior flexus (af), central flexus (cf), posterior flexus (pf). Abbreviations for lower molars: protoconid (prd), hypoconid (hyd), metaconid (med), entoconid (end), mesoconid (msd), paraconid (pad), ectostylid (ecstd), metastylid (mestd), hypoconulid (hycud), anterolophid (anld), protolophid (prld), entolophid (enld), posterolophid (pold), ectolophid (ecld), anterobuccal sinusid (asd), hypoflexid (hyfd), anterior fossettid (afd), central flexid (cfd), posterior fossettid (pfd).

Craniodental measurements

Craniodental variables were measured with handheld Vernier Calipers (Mitutoyo 500-197, 200 mm, Japan) to the nearest 0.01 mm following a modified version of the measurements recorded by Helgen et al. (2009) and Li et al. (2012) (24 variables, Figure 2).

Figure 2.

Figure 2

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Craniodental measurements taken for this study

Greatest length of skull (GLS), length of nasals (LN), zygomatic breadth (ZB), anterior breadth of nasals (ABN), posterior breadth of nasals (PBN), interorbital breadth (IOB), condylobasal length (CBL), palate length (PL), post palatal length (PPL), length of incisive foramina (LIF), length of auditory bulla (LAB), length from P3 to M3 (LP3 M3), length from P4 to M3 (LP4 M3), breadth of P4 (BP4), breadth of M1 (BM1), breadth of M3 (BM3), inside breadth of bony palate at P4 (IBPP4), inside breadth of bony palate at M3 (IBPM3), breadth across infraorbital foramina (BIF), breadth of occipital condyle (BOC), mastoid breadth (MB), breadth across paroccipital process (BPP), length from P4 to M3 (LP4M3), and height of mandible (HM).

A Principal Component Analysis (PCA) based on the covariance matrix was used to evaluate variation in 20 of 24 craniodental variables (LP3 M3 was excluded because Iomys spp. have no P3; BP4, BM1, BM3 were also excluded because only specimens lodged at KIZ measured these variables) taken from P. (H.) leonardi (holotype+4 specimens of the Yunnan population), from similar sized flying squirrels which occur sympatrically or parapatrically with P. (H.) leonardi (i.e., Hylopetes alboniger, n=10; H. phayrei, n=10; Belomys pearsonii, n=2), and from flying squirrels most closely related genetically to P. (H.) leonardi (Iomys horsfieldii, n=7; I. sipora, n=2). Missing data was filled with the average of the species. Raw measurements were log-transformed to standardize variances and improve normality. All analyses were performed using PAST v.4.02 (Hammer et al., 2001).

Morphological comparison

Qualitative comparisons of craniodental morphological features were made for all available skulls in Supplementary Text, and included: (1) the pattern of internal septae of the auditory bulla (Supplementary Figure S1); (2) the development of the coronoid process; (3) presence or absence of P3; (4) the development of the mesostyle, mesolophule, anterolophule, paraconule, metaconule, metaloph, lingual flexus, hypoconulid, protolophid, and entolophid on the cheekteeth.

Non-cranial morphology that was assessed included checking for the presence of ear tufts (Supplementary Figure S2) and the shape and size of the glans penis. Detailed pelage comparisons were also made between the Yunnan specimens and the holotype of P. (H.) leonardi.

Molecular techniques

Most of the sequences used in this study were downloaded from GenBank, especially from the studies of Mercer & Roth (2003) and Li et al. (2020) (Supplementary Table S2). In addition, four new samples (two P. (H.) leonardi of the Yunnan population, KIZ034951, KIZ034952; one Hylopetes alboniger, KIZ034942; and one Petaurista elegans, KIZ034939) were sequenced. We did not include previously widely used “Aeretes” sequences (GenBank accession Nos.: AY227593, AY227535, AY227481) in our analyses, because these come from a misidentified specimen (Roth & Mercer, 2015: 223, Quan Li, personal observation).

DNA extraction and PCR

Total genomic DNA was extracted from muscle tissue of four specimens collected from Mount Gaoligong using the DNeasy Tissue kit (Qiagen, Germany). Two mitochondrial (12S ribosomal RNA (12S), and 16S ribosomal RNA (16S)) and one nuclear (interphotoreceptor retinoid-binding protein (IRBP)) gene fragments were amplified with rtaq DNA Polymerase (Takara, Japan) with the primers presented in Supplementary Table S3. PCR products were purified with the QIAquick PCR Purification kit (Qiagen, Germany) and sequenced with the BigDye Terminator Cycle kit v3.1 (USA) using an Applied Biosystems automated sequencer (ABI 3730xl, USA). Sequencing reads were assembled and edited using the DNASTAR Lasergene v7.1 (Burland, 2000).

Phylogenetic analyses, divergence time estimation, and intergeneric genetic differences calculation

All sequences were assembled by Seqman (Burland, 2000) and aligned in MEGA 7.0 (Kumar et al., 2016). MEGA 7.0 was also used to calculate K2P distance between taxa based on the 12S and 16S loci. Sequences of the aplodontiid Aplodontia rufa, and the sciurids Ratufa bicolor, Sciurus vulgaris, and Tamiasciurus hudsonicus were employed as outgroups. Three datasets were applied in the phylogenetic analyses: (1) the mtDNA dataset based on 12S and 16S, (2) the IRBP dataset, and (3) the mtDNA+nuDNA concatenated dataset. This study used RAxML (Edler et al., 2021) and Beast 1.8.2 (Drummond et al., 2012) to construct the Maximum Likelihood (ML) and Bayesian (BI) trees respectively. The best evolutionary model for each gene fragment was estimated using the Bayesian Information Criterion (BIC) in PartitionFinder (Lanfear et al., 2012). In ML analyses, this study used GTR+G for each partition and 1 000 replicates for the rapid bootstrapping algorithm, while in BI analyses, 12 models (GTR, GTR+G, HKY, HKY+G, TrN, TrN+G, TrNef, TrNef+G, K80, K80+G, SYM, SYM+G) were provided for substitution model selection of each partition. Each BI analysis was composed of a random starting tree, an uncorrelated lognormal relaxed molecular clock model, and a birth-death tree prior. Two fossil occurrences were applied as calibration points when constructing the BI trees: the oldest fossil squirrel (Douglassciurus jeffersoni) which dates to the late Eocene (ca. 36 million years ago (Ma)) (Emry & Thorington, 1984; Goodwin, 2008), and the fossil flying squirrel Miopetaurista neogrivensis, dated to ca. 11.6 Ma (Casanovas-Vilar et al., 2018). Each analysis consisted of 3×107 generations sampled every 1 000 generations. Convergence was assessed using Tracer v1.7.1 (Rambaut et al., 2018) and the 1st 15% of the generations were discarded as burn-in. Maximum-likelihood bootstrap proportions (BP)≥70 and Bayesian posterior probability (PP)≥0.95 were considered as strong supports.

RESULTS

PCA

A PCA evaluated morphological variation in 20 craniodental variables among P. (H.) leonardi and related species (“similar sized+sympatric/parapatric” or “genetic similarity”, see Methods section). The 1st component (65.5% of variation) separated samples mainly on the basis of HM, LN, ZB, and PL, the 2nd component (13.25% of variation) on the basis of LIF, LAB, and IBPP4, and the 3rd (6.31% of variation) on the basis of PBN, LIF, IBPP4, BIF, and LAB (Supplementary Table S4). The bivariate scatter plot of specimen-scores on component 1 clearly distinguished Hylopetes alboniger and H. phayrei from P. (H.) leonardi, Iomys horsfieldii, I. sipora, and Belomys pearsonii. Additionally, component 2 further distinguished Iomys horsfieldii, I. sipora, and Belomys pearsonii from P. (H.) leonardi (Figure 3). The holotype of P. (H.) leonardi clusters with samples of the Yunnan population (Figure 3). Raw craniodental measurements were given in Supplementary Table S5.

Figure 3.

Figure 3

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Principal component analysis scatter-plot of the skulls of Pteromys (Hylopetes) leonardi (=Priapomys leonardi) and related species (“similar sized+sympatric/parapatric” or “genetic similarity”)

Red dots: Yunnan population of Pteromys (Hylopetes) leonardi; Red star: Holotype of Pteromys (Hylopetes) leonardi; Blue filled squares: Iomys horsfieldii; Blue open squares: Iomys sipora; Green open triangle: Hylopetes phayrei; Green filled triangle: Hylopetes alboniger; and Purple X: Belomys pearsonii.

Morphological comparisons

Skins: The specimens of the Yunnan population (mass 150–204 g, head body length 195–210 mm, tail length 194–213 mm, ear length 33–37 mm, hindfoot length 40–45 mm) are slightly larger than the holotype of P. (H.) leonardi (Thomas (1921) measured on the skin: head body length 180 mm, tail length 125 mm, hindfoot length 39 mm). The tail of the holotype appears to be notably shorter (Tail length/Head and body length=69% in the holotype, 88%–106% in the Yunnan population) and broader than in the Yunnan population (Figure 4). Except for these aspects, their skins are very similar, especially in overall pelage color, and in having white throat patch and facial patterns (Figure 4). The fur is long and fine, with the general color above being blackish buffy, the hairs having long blackish slaty bases and buffy tips. The venter is overall pinkish buffy, with the chest and axillary regions pure white. The face and the streaks running along the sides of the neck are buff. The ears are naked, prominently black, and larger than most other small-sized flying squirrels (e.g.: body size: Hylopetes alboniger>P. (H.) leonardi>Belomys pearsonii, ear length: P. (H.) leonardi=33–37 mm, Hylopetes alboniger=24–35 mm, Belomys pearsonii=22–24 mm). Ear tufts are absent. The dorsal surfaces of the hands and feet are blackish, lighter along their inner edges terminally. The tail is flat, very thick and bushy; its wool-hair buffy, its long hairs glossy blackish (Thomas, 1921). The uropatagium (tail membrane or interfemoral membrane) is less developed than in the larger flying squirrels.

Figure 4.

Figure 4

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Skin comparison of Pteromys (Hylopetes) leonardi (=Priapomys leonardi) and related species (“similar sized+sympatric” or “genetic similarity”)

From top to bottom: Pteromys (Hylopetes) leonardi (holotype, BMNH20.8.8.2), Pteromys (Hylopetes) leonardi (Yunnan population, KIZ034951), Iomys horsfieldii (USNM153684), Hylopetes alboniger (KIZ034942), and Belomys pearsonii (KIZ034940).

Skulls: The skulls of the Yunnan population and the holotype of P. (H.) leonardi are similar (Figure 5) and resemble other small sized flying squirrels in overall shape (Supplementary Figure S3A, B, C). However, the auditory bullae are relatively much smaller (Supplementary Figure S3B, C) (length of auditory bulla: P. (H.) leonardi=7.46–7.91 mm, Hylopetes alboniger=8.65–9.35 mm, Belomys pearsonii=9.24–9.45 mm) and the palate is unusually arched between the molars to form a strongly developed posterior palatal spur (Supplementary Figure S3B).

Figure 5.

Figure 5

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Skull and dentition comparison of Pteromys (Hylopetes) leonardi (=Priapomys leonardi) and related species (“similar sized+sympatric” or “genetic similarity”)

From left to right: Pteromys (Hylopetes) leonardi (holotype, BMNH20.8.8.2), Pteromys (Hylopetes) leonardi (Yunnan population, KIZ034951), Iomys horsfieldii (AMNH185169), and Hylopetes alboniger (KIZ034942).

Cheekteeth: The cheekteeth of the Yunnan population and the holotype of P. (H.) leonardi are very similar (Figure 5) and generally resemble other small sized flying squirrels, especially Glaucomys and Eoglaucomys (Supplementary Figure S3D, see Diagnosis). The cheekteeth are relatively small. The enamel is slightly sculpted between and on the sides of the ridges. All major ridges of the upper cheekteeth (anteroloph, paraloph, metaloph, posteroloph, endoloph) are developed normally, except the metaloph is absent on M3. The buccal side of the endoloph usually possesses traces of the anterolophule and mesolophule. Most specimens do not possess a mesostyle, and their mesolophules do not develop into mesolophs extending to the outer exit of the central valley (the single exception is KIZ034952, which possesses a very faint mesoloph and a very small mesostyle). As a result, from the buccal side of the upper cheekteeth, only three cusps can be seen in P. (H.) leonardi, rather than four cusps in most species of Hylopetes and Petinomys (Supplementary Figure S4). The endoloph does not develop a distinct hypocone and there is not any distinct lingual fold. The paraconule is absent and the metaconule is small but recognizable on P4, M1, and M2. The lower cheekteeth also resemble those of other small sized flying squirrels, with the protolophid and entolophid less developed, the paraconid does not merge with the protoconid, and the anterobuccal sinusid present.

Glans penis: The glans penis of the holotype of P. (H.) leonardi, although male, is missing. The male Yunnan specimens possess a bony, slim, ultralong (17% of head and body length), and “S” shaped glans with two faint smooth crests on the right side (Supplementary Figure S5). Due to the rarity of well-preserved penile specimens, we only examined the glans of species of 11 living genera, of which the glans of Iomys was damaged (tip missing, only the base was left); the glans of Aeretes, Aeromys, Petaurillus, Petinomys are still unreported. The glans of most flying squirrels we examined were usually stouter, shorter (2%–7% of head and body length), and with more developed crest(s) than the Yunnan specimens (Supplementary Figure S5 and Table S6), whereas Glaucomys volans and Iomys horsfieldii possess a slightly similar glans. The glans of Glaucomys volans is ultralong (16% of head and body length), straight, and the baculum was half the length of the glans. In contrast, the glans of the Yunnan population was “S” shaped, and the baculum was as long as the glans. The only available glans sample of Iomys is a broken glans base (AMNH185169), which was as slim as the glans of the Yunnan population. However, because the tip is missing, we cannot tell if Iomys shares a similarly elongated glans with the Yunnan population (Supplementary Figure S5). More details of the morphological comparisons are shown in Supplementary Table S6.

Phylogeny

The phylogenetic reconstructions used three different datasets and showed similar topologies with both BI and ML approaches (Figure 6; Supplementary Figure S6). In all trees, the samples of the Yunnan population clustered in a monophyletic clade and showed a sister relationship with Iomys, with strong support (PP=1, BP=83–99).

Figure 6.

Figure 6

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Flying squirrel phylogeny (includes all genera except Aeretes) and node dating estimates based on Bayesian and Maximum likelihood approaches utilizing the mtDNA+nuDNA concatenated dataset

Numbers of the branches are Bayesian posterior probabities (top left), likelihood bootstrap values (top right), and node dating estimate values (bottom). Dot is the fossil occurrence of Douglassciurus jeffersoni and star is the fossil occurrence of Miopetaurista neogrivensis.

Divergence time

Estimated flying squirrel intergeneric (14 genera excluding the genus Aeretes and the Yunnan population) divergence times from the mtDNA+nuDNA concatenated dataset range from 4.56 to 23.9 Ma. The Yunnan population splitting with its sister lineage, the genus Iomys, is estimated to have occurred in the late Miocene (11.27 Ma, 95% CI=6.19–12.07) (much younger than the divergence time between the Yunnan population and Hylopetes: 16.61 Ma, 95% CI=9.94–15.99). This is older than the divergence time for many accepted sister genus pairs, 6.64 Ma (95% CI=4.44–9.05) for Aeromys vs. Biswamoyopterus and 4.56 Ma (95% CI=3.32–6.8) for Trogopterus vs. Belomys) (Figure 6).

Intergeneric genetic differences

For mitochondrial 12S ribosomal RNA sequences, the range of intergeneric (14 genera excluding the genus Aeretes and the Yunnan population) divergences were 5.4%–15.2% (Supplementary Table S7A). The genetic distances between the Yunnan population and other genera ranged from 6.9 to 14.2%, which is greater than 5.4% for Trogopterus and Belomys.

For mitochondrial 16S ribosomal RNA sequences, the range of intergeneric (14 genera excluding the genus Aeretes and the Yunnan population) divergences were 5.2%–14.7% (Supplementary Table S7B). The genetic distances between the Yunnan population and other genera ranged from 5.6 to 13.3%, which is greater than some intergeneric variations, such as 5.2% for Aeromys and Biswamoyopterus, and 5.5% for Trogopterus and Belomys.

DISCUSSION

The Yunnan population and the holotype of P. (H.) leonardi are slightly different in body size and tail length and shape (see Results). However, as there was only one specimen available (holotype) from the type locality (northern Myanmar), we do not know if these differences are consistent or statistically significant. There is a distance of only ca. 100 km between the type locality (N28°5′, E97°25′; Thomas, 1921) and the nearest sampling point of the Yunnan population. However, the Irrawaddy River runs between them (Figure 7), which may contribute to geographical variation between these populations. Based on the PCA (Figure 3) and the qualitative morphological comparisons (see Results), we found that the Yunnan population is very similar to the holotype in most respects. We consider that the Yunnan population and the holotype are the same species and thus that our morphological and genetic analysis using the samples of the Yunnan population represent the taxon leonardi.

Figure 7.

Figure 7

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Currently hypothesized distribution of Pteromys (Hylopetes) leonardi (=Priapomys leonardi) and two other flying squirrel genera

“Iomys spp.” include all species of Iomys, which is the sister lineage of Pteromys (Hylopetes) leonardi; and “Hylopetes spp.” include all species of Hyloptes, with which Pteromys (Hylopetes) leonardi has previously been confused taxonomically. Data from IUCN.

Based on the PCA (Figure 3), skins (Figure 4), skulls/teeth (Figure 5), glans (Supplementary Figure S5), and genetic analyses (Figure 6), it is clear that leonardi is a distinct species from H. alboniger, with which it has previously been confused or allied (see Introduction). These analyses also indicate that leonardi has a sister relationship with Iomys, albeit with a deep, intergeneric-level divergence. In considering whether leonardi should be allocated to the genus Iomys, or described as the type species of new genus sister to Iomys, we considered three criteria for defining a new genus (Dong et al., 2010; Liu et al., 2012): (1) generic monophyly; (2) reasonable compactness as defined by consistent levels of intergeneric divergence across flying squirrel systematics; and (3) ecological, morphological, or biogeographical distinctness.

Morphological differences evident between leonardi and Iomys included: (1) P3 absent in Iomys vs. present in leonardi; (2) hypocone present in Iomys vs. absent in leonardi; (3) paraloph, metaloph, protolophid, entolophid much more developed in Iomys than in leonardi; and (4) quadricuspidate molars in Iomys vs. non-quadricuspidate molars in leonardi. Hunter & Jernvall (1995) proposed that the hypocone is a key innovation that has allowed invasion of, and diversification within, herbivorous adaptive zones. We speculate that possession of a hypocone byIomys suggests a more herbivorous diet, while lack of a hypocone inleonardi suggests an overall more omnivorous diet.

The species of Iomys inhabit a variety of tropical forests in Sundaland (Jackson & Schouten, 2012). Conversely, leonardi lives in subtropical evergreen broad-leaved forest and temperate mixed coniferous and broad-leaved forest of the eastern Himalayas (Quan Li, personal observation). There is a large gap between the distributions of leonardi and Iomys (Figure 7). Various other sister genus/species pairs show a similar disjunct East Himalaya/Annamite and Sundaic distribution, such as the crested arguses Rheinardia, colugos Galeopterus, banded civets Hemigalus and Chrotogale, and striped rabbits Nesolagus. This general biogeographic pattern may result from several large-scale marine transgressions (Woodruff, 2003) and the gradual aridification and seasonality of the Indochina Peninsula during the Late Cenozoic (Morley, 2018). Given major morphological differences between leonardi and Iomys, their different biogeographic occurrences, respective monophyly of the genus Iomys and the taxon leonardi, and comparative intergeneric level genetic difference between leonardi and Iomys, here we describe a new genus for the taxon leonardi, which represents an overlooked major phylogenetic lineage within the Pteromyini.

Taxonomy

Class Mammalia Linnaeus, 1758

Order Rodentia Bowdich, 1821

Family Sciuridae Fischer de Waldheim, 1817

Subfamily Sciurinae Fischer, 1817

Tribe Pteromyini Brandt, 1855

Subtribe Glaucomyina Thorington and Hoffmann, 2005

Priapomys gen. nov.

Type species: Pteromys (Hylopetes) leonardi Thomas, 1921.

Included species: Priapomys leonardi (Thomas, 1921) (李氏小飞鼠).

Referred specimens: BMNH20.8.8.2 (holotype), adult male, skin, skull, collected from Kachin State (N28.083°, E97.417°, 2 438 m a.s.l.), northern Myanmar. Collected 11 January 1917, by P. M. Leonard.

　KIZ034951 (adult female, Genbank accession Nos. MW929354, MW929358, MW929361), KIZ034954 (adult female), skin, skull, collected from Qiqi (其期, N27.715°, E98.571°, 2 171 m a.s.l.), Mt. Gaoligong, Gongshan, Yunnan Province, China. Collected 15–16 December 2014, by Q. Li.

KIZ034952 (adult male, Genbank accession Nos.: MW929355, MW929359, MW929362), KIZ034953 (juvenile female), skin, skull, collected from Jidu (基独, N27.715°, E98.516°, 2 601 m a.s.l.), Mt. Gaoligong, Gongshan, Yunnan Province, China. Collected 17 October 2016, by Q. Li.

KIZ035090 (adult male), whole body preserved in ethanol, collection information as for KIZ034952 and KIZ034953.

KIZ034971 (juvenile female), skull, collected from Zhiziluo (知子罗, N26.544°, E98.973°, 2 649 m a.s.l.), Mt. Biluo, Fugong, Yunnan Province, China. Collected 2 November 2011, by C.Z. Pu.

KIZ0410099 (adult female), skin, skull, collected from Maku (马库, N27.694°, E98.291°, 1 416 m a.s.l.), Mt. Gaoligong, Dulongjiang, Yunnan Province, China. Collected 5 November 2004, by X.L. Jiang.

DUE110001, DUE110002, DUE110003, DUE110005, DUE110006, DUE110007, skins; from the upper Mekong river valley (unknown whether these were collected from the east or the west bank), Weixi, Yunnan Province, China, by staff of Dali University; sex, maturity, and dates of collection not recorded.

Etymology: The specific name is derived from Priapus (the Greek god of fertility), and mys, Greek for mouse (and mouse-like animals). Priapomys is masculine. The ultralong glans of penis of the type species inspired the name.

Suggested English name: Himalayan Large-eared Flying Squirrel (喜山大耳飞鼠属).

Diagnosis: External morphology (less developed uropatagium, flat tail) and overall shape of skull generally resemble other small-sized flying squirrel genera (Figure 4; Supplementary Figure S3A, B, C). The external ear is larger than most other small-sized flying squirrels, while the auditory bulla is very small; there are no ear tufts.

Cheekteeth are generally similar to other genera of Glaucomyina, but the combination of characteristics can distinguish Priapomys from other extant flying squirrel genera (Figure 5; Supplementary Figure S3D). The endoloph does not develop a distinct hypocone, no central notch/flexus (endoloph develops a distinct hypocone to form a central notch/flexus in Aeromys, Belomys, Biswamoyopterus, Eupetaurus, Iomys, Pteromyscus, and Trogopterus). Posterior flexus absent (present in Aeretes and Petaurista). Mesolophule usually obsolete, not extending to the outer exit of the central valley, and mesostyle absent (mesolophule connect to the well-developed mesostyle to form a distinct “mesoloph” in most species of Petinomys and Hylopetes). Metaloph complete and metaconule less developed (metaloph deeply notched to cut off a separate metaconule in Pteromys). Anteroloph, posteroloph, and paraconid distinct (much reduced in Petaurillus). Thus, Priapomys can be easily distinguished from most living flying squirrel genera by dentition, except Eoglaucomys and Glaucomys.

The cheekteeth of Priapomys have more pitted enamel than Eoglaucomys and Glaucomys, and a more well-developed paraconid (Supplementary Figure S3D). Moreover, the auditory bulla of Priapomys is much smaller than Eoglaucomys and Glaucomys, and the postorbital processes are more developed than in Glaucomys (Supplementary Figure S3A, B, C). The glans penis of Priapomys also differs from Eoglaucomys and Glaucomys (Supplementary Figure S5 and Table S6).

Distribution: Priapomys leonardi is known to occur in northern Myanmar (Kachin State), at Mount Gaoligong (the watershed of the Ayeyarwady (=Irrawaddy) River and the Nu (=Salween) River), and in the upper Mekong River Valley (Weixi, Yunnan Province, China). Therefore, we suspect that Priapomys leonardi may occur more broadly in suitable habitat of eastern Himalayas, especially north of the known localities. No specimens have been collected south of Baoshan, China (N25°; Figure 7).

Natural history: Very little is yet known about the natural history of Priapomys leonardi. The Yunnan population inhabits evergreen broad leave forests and coniferous broad leave mixed forests at an elevation of 1400–2700 m a.s.l., and populations in Myanmar presumably inhabit similar environments (holotype collected from 8000 feet (=2438 m a.s.l.), Thomas (1921)). Hylopetes alboniger, Belomys pearsonii, Petaurista yunanensis, Petaurista elegans, and Biswamoyopterus gaoligongensis occur sympatrically with Priapomys leonardi at Mount Gaoligong.

Conservation: Little is currently known about the conservation status of Priapomys leonardi. Due to its small body size, it is not a major target for hunting and poaching, but it is captured by indiscriminate traps set for hunting meat by herb collectors who visit its range. During 2014 to 2016, Q. Li observed this species being sold at game markets on northern Mount Gaoligong where it is abundant. While the known extent of occurrence is relatively small, ca. 25 000 km2 based on the known localities (Figure 7), it does not qualify for the IUCN ranking of Vulnerable (extent of occurrence<20 000 km2). Therefore, we recommend an IUCN Red List classification of Near Threatened (NT) for this species, based on our current understanding of threats to the species, and its distribution.

Key to the genera of living flying squirrels:

1) (a) endoloph does not develop a distinct hypocone, central notch/flexus indistinct. 2

(b) endoloph develops a distinct hypocone, central notch/flexus distinct. 3

2) (a) coronoid process much reduce; metaloph deeply notched to cut off a separate metaconule. Pteromys

(b) coronoid process normal, higher than condylar process; metaloph does not deeply notch to cut off a separate metaconule. 4

3) (a) P3 always absent, chewing surface of molars is quadricuspidate. Iomys

(b) P3 usually present, chewing surface of molars is not quadricuspidate. 5

4) (a) posterior flexus distinct. 6

(b) posterior flexus indistinct. 7

5) (a) metacone and metaloph completely absent on M3. 8

(b) metacone and metaloph present or at least recognizable on M3. 9

6) (a) incisor grooved. Aeretes

(b) incisor ungrooved. Petaurista

7) (a) auditory bulla septae complex, arachnoid (cobweb-like) . Petinomys#

(b) auditory bulla septae<4.10

8) (a) ear tufts present, auditory bulla septae complex, honeycomb. Biswamoyopterus

(b) ear tufts absent, auditory bulla septae<4.Aeromys

9) (a) mesostyle absent, paraconule, metaconule indistinct.... Eupetaurus

(b) mesostyle present, paraconule, metaconule distinct. 11

10) (a) mesolophule connects to the well-developed mesostyle to form a distinct “mesoloph”, four cusps can be seen from the buccal side of the upper cheekteeth. Hylopetes*

(b) mesostyle and mesolophule absent or obsolete, three cusps can be seen from the buccal side of the upper cheekteeth. 12

11) (a) ear tufts absent, auditory bulla septae ca. 5............. Pteromyscus

(b) ear tufts present, auditory bulla septae complex, honeycomb. 13

12) (a) body size very small (<50 g), cheekteeth simplified, anteroloph, posteroloph and small cusps reduced.Petaurillus

(b) body size not very small (>50 g), cheekteeth normal, anteroloph, posteroloph and small cusps distinct.14

13) (a) P4>>M1. Trogopterus

(b) P4≥M1. Belomys

14) (a) auditory bulla large, postorbital process reduced........ Glaucomys

(b) auditory bulla normal or very small, postorbital process normal. 15

15) (a) auditory bulla normal, enamel smooth, paraconid of P4 reduced, glans short, stout, and glove-like. Eoglaucomys

(b) auditory bulla very small, enamel slightly pitted, paraconid of P4 normal, glans slim and ultralong......................... Priapomys gen. nov.

*: Hylopetes nigripes (endemic to Palawan) and Hylopetes bartelsi (endemic to Java) lack the distinct mesoloph and mesostyle which most species of Hylopetes possess; #: The internal septae of the auditory bulla of Petinomys setosus is honeycomb.

NOMENCLATURAL ACTS REGISTRATION

The electronic version of this article in portable document format will represent a published work according to the International Commission on Zoological Nomenclature (ICZN), and hence the new names contained in the electronic version are effectively published under that Code from the electronic edition alone (see Articles 8.5–8.6 of the Code). This published work and the nomenclatural acts it contains have been registered in ZooBank, the online registration system for the ICZN. The ZooBank LSIDs (Life Science Identifiers) can be resolved and the associated information can be viewed through any standard web browser by appending the LSID to the prefix http://zoobank.org/.

PublicationLSID:

urn:lsid: zoobank.org: pub: AAEF4232-D698-4763-9140-738B847F95D7.

Priapomys gen. nov. LSID:

urn: lsid: zoobank. org: act: DF0C8CAA-1CD4-4DE7-9484-E77027EB2977.

SCIENTIFIC FIELD SURVEY PERMISSION INFORMATION

Permission for field surveys in Gongshan County was granted by the Gongshan Management Bureau of Gaoligongshan National Nature Reserve.

SUPPLEMENTARY DATA

Supplementary data to this article can be found online.

Click here for additional data file. (2.5MB, pdf)

COMPETING INTERESTS

The authors declare that they have no competing interests.

AUTHORS’ CONTRIBUTIONS

Q.L. designed the study, contributed to the collection and identification of the specimens, interpreted the data, and drafted the manuscript. F.C. performed the genetic analyses. S.M.J. revised the manuscript and provided the specimen photos from European museums. K.M.H. reviewed the taxonomic and morphological data and analysis and revised the manuscript. S.Y.L. supervised the study of penis morphology. F.L. provided extensive field observations and photographs. D.S. and S.L. provided important samples. W.Y.S. and H.J.W. input data and performed partial molecular experiments. Y.X. and J.S. organized the whole field expedition. X.L.J. supervised the whole process of the study. All authors read and approved the final version of the manuscript.

ACKNOWLEDGEMENTS

We are especially grateful to Guo-Qiang Wang for providing the first Yunnan Priapomys leonardi specimen that initiated this study. We thank Da-Zhou Peng, Xue-Ken Wang, Zhi-Jun Long, Jin-Lin Qian, and Chun-Liao Qian for their assistance in the field. We are grateful to Qi-Gao Jiang-Zuo and Qiang Li for discussions on dentition. We thank Roberto Portela Miguez and Louise Tomsett, from the Natural History Museum, London; Dr Krishnamoorthy Venkataraman, of the Zoological Survey of India; Hein Van Grouw of the Leiden Museum; Darrin Lunde and Melissa T.R. Hawkins from the National Museum of Natural History (Smithsonian Institution); Marisa Surovy, Eleanor Hoeger, and Sara Ketelsen from the American Museum of Natural History; Julian Kerbis Peterhans, Lawrence Heaney, and Adam Ferguson, from the Field Museum of Natural History; and staff at Dali University for access to specimens. We thank Ji-Shen Wang and Will Duckworth for their suggestions on Latin names of the new genus and zoogeography. We are very grateful to contributors to the Biodiversity Heritage Library for making historical literature so easily accessible. We also thank IUCN for providing easy downloadable summaries of species distribution information. Bernie Dominiak and Sebastian Comte reviewed a final draft of the manuscript prior to submission for publication.

Funding Statement

This study was supported by the Second Tibetan Plateau Scientific Expedition and Research Program (STEP, 2019QZKK0501), National Natural Science Foundation of China (32000304), Yunnan Fundamental Research Projects (202101AT070294), National Key Research and Development Program of China (2017YFC0505200), Strategic Priority Research Program of Chinese Academy of Sciences (XDA20050202), Biodiversity Survey, Monitoring and Assessment (2019HB2096001006), and Kadoorie Farm & Botanic Garden

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Supplementary Materials

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Click here for additional data file. (2.5MB, pdf)

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