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Molecular and Morphological Evidence for a New Species of the Genus Typhlomys (Rodentia: Platacanthomyidae)

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Molecular and Morphological Evidence for a New Species of the Genus Typhlomys (Rodentia: Platacanthomyidae) ZOOLOGICAL RESEARCH Molecular and morphological evidence for a new species of the genus Typhlomys (Rodentia: Platacanthomyidae) DEAR EDITOR, visual assistance (Panyutina et al., 2017). Although eye In this study, we reassessed the taxonomic position of degradation (Cheng et al., 2017) is a feature present in other Typhlomys (Rodentia: Platacanthomyidae) from Huangshan, mammals, such as moles (Carmona et al., 2008), it is usually Anhui, China, based on morphological and molecular associated with fossoriality and is uncommon among evidence. Results suggested that Typhlomys is comprised of scansorial/arboreal species; Typhlomys is the only currently up to six species, including four currently recognized species known taxon. (Typhlomys cinereus, T. chapensis, T. daloushanensis, and T. Despite the unique morphology and life history of this nanus), one unconfirmed candidate species, and one new genus, the exact species composition of Typhlomys is still species (Typhlomys huangshanensis sp. nov.). Morphological unclear (Jansa et al., 2009). In the original taxonomic analyses further supported the designation of the Huangshan description based on pelage, external measurements, and specimens found at mid-elevations in the southern Huangshan skull morphometrics, Typhlomys contained five subspecies, Mountains (600 m to 1 200 m a.s.l.) as a new species. including Typhlomys cinereus cinereus, T. c. chapensis, T. c. The family Platacanthomyidae is comprised of two extant daloushanensis, T. c. guangxiensis, and T. c. jingdongensis genera, Platacanthomys and Typhlomys (Musser & Carleton, (Wang et al., 1996). Subsequently, Abramov et al. (2014) 2005). Molecular phylogenetic findings support Platacan- supported the specific status of T. c. chapensis given the thomyidae as a unique lineage and sister to all other Muroidea significant molecular and skull morphology differences families, although their external morphology is similar to between this subspecies and nominal T. c. cinereus. Recent dormice of the family Gliridae and their molar structure is molecular phylogenetic studies confirmed the monophyly of similar to Gymnuromys from Madagascar (Abramov et al., Typhlomys and suggested that it is composed of at least five 2014; Jansa et al., 2009; Musser and Carleton, 2005). species based on genetic evidence of multiple loci and skull The genus Typhlomys (Milne-Edwards, 1877), which means morphology and morphometrics (Cheng et al., 2017). The “blind mouse” (Jansa et al., 2009), possesses small shrew-like research of Cheng et al. (2017) determined the species level eyes and is the lesser-known member of Platacanthomyidae. recognition of T. cinereus, T. daloushanensis, and T. These animals have a long hairy tail, long vibrissae, and chapensis, described a new species (T. nanus), and identified prominent ears, with the tip of their tails covered in a tuft of a putative new species. long white hair (Hong, 1982). Their long vibrissae are a tactile Typhlomys is mainly distributed in montane regions of aid in the capture of prey (Anjum et al., 2006), and their short southern China and northwestern Vietnam (Abramov et al., limbs exhibit scansorial and fossorial advantage in terms of 2014; Cong et al., 2013). As a mid-high elevation inhabitant leverage (Rubin & Lanyon, 1984). Such morphological (340–2 300 m a.s.l.), the distribution of Typhlomys is strongly adaptations suggest an arboreal and burrowing lifestyle (Cui related to complex geographical regions (Abramov et al., et al., 2020; Smith, 2008). As an arboreal animal with vestigial 2012). For example, in southwest China, the extremely eyes, these rodents have developed a form of echolocation for complex topography and well-developed river systems in the orientation and navigation in complex environments without Received: 31 May 2020; Accepted: 20 November 2020; Online: 24 Open Access November 2020 This is an open-access article distributed under the terms of the Foundation items: This project was supported by the Global Creative Commons Attribution Non-Commercial License (http:// Environment Facility Project "Securing Biodiversity Conservation and creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted Sustainable Use in Huangshan Municipality", Biodiversity Survey, non-commercial use, distribution, and reproduction in any medium, Monitoring and Assessment Project of Ministry of Ecology and provided the original work is properly cited. Environment, China (2019HB2096001006) and Natural Science Copyright ©2021 Editorial Office of Zoological Research, Kunming Foundation of Universities of Anhui Province (KJ2019A0486) Institute of Zoology, Chinese Academy of Sciences DOI: 10.24272/j.issn.2095-8137.2020.132 100 Science Press Zoological Research 42(1): 100−107, 2021 Hengduan Mountain region have led to the allopatric (clade F) was strongly supported as sister species (PP≥0.99). divergence of species within the genus Typhlomys (Chen et In the mitochondrial cyt b gene tree (Figure 1A-a), the al., 2017; Fjeldså et al., 2012; Liu et al., 2012) and may have phylogenetic tree still showed the same topological structure led to the differentiation of two different genetic populations (T. with an additional T. cinereus from Guangdong (Lv et al., nanus and T. chapensis, Cheng et al., 2017). In southeast 2016). China, there are similar river valley systems (Song et al., The cyt b uncorrected genetic distances among different 2017), but only one species (T. cinereus) has been discovered species ranged from 11.3% to 19.2% (Supplementary Table to date (Cong et al., 2013; Wang, 1990; Wang et al., 1996). S4). Considering that species-level divergence in different Thus, to some extent, the species diversity of Typhlomys may mammal groups ranges from 2% and 11% (Baker & Bradley, be underestimated. 2006), the different lineages of Typhlomys (A–F, Figure 1A-a) In the present study, we integrated molecular and might represent distinct species. Among them, the genetic morphometric approaches to describe a new species from the distance between T. sp. 1 and T. cinereus was 14.2%–14.7% Huangshan and Qingliangfeng mountains in Anhui Province, (Supplementary Table S4), indicating species-level China. divergence. We also observed a single triplet insertion (T. Blind mouse specimens were collected from the Huangshan chapensis, T. nanus) and single triplet deletion (T. cinereus, T. and Qingliangfeng mountains (Anhui Province, China) and sp. 1, T. sp. 2) in the IRBP sequences. consisted of four adult males and six adult females. Tissue The topology of the species tree resembled the samples were extracted, amplified, and sequenced for the concatenated gene tree, and all relationships were strongly cytochrome b (cyt b) gene (1 070 bp), interphotoreceptor supported (Figure 1B). The time to the most recent common retinoid-binding protein (IRBP (1 052 bp)) gene, and growth ancestor (MRCA) of Typhlomys was estimated to be 16.94 hormone receptor (GHR (774 bp)). All DNA sequences million years ago (Ma) (95% CI=9.70–26.31). Furthermore, the generated are available in GenBank (Supplementary Table six putative species diverged between 6.90 and 11.49 Ma, and S1). Uncorrected pairwise genetic distances of the cyt b gene T. sp. 1 and T. cinereus diverged about 7.72 Ma were computed using the APE R package (Paradis et al., (95%CI=4.41–11.40). 2004). Bayesian phylogenetic analyses were conducted with The Poisson tree processes (PTP) model for species MrBayes v3.2.2, including each nuclear gene, cyt b gene, and delimitation recognized eight putative species (Figure 1B-a), concatenated mitochondrial and nuclear datasets (Ronquist et and the split results supported the specific status of T. al., 2012). The Poisson tree processes (PTP) model (Zhang et cinereus and T. sp. 1, with species partition support of 0.98 al., 2013) and BPP v3.4 (Yang & Rannala, 2010) were run to and 0.95, respectively (Figure 1B-a). Based on the results of infer putative species boundaries (see Supplementary Cheng et al. (2017), we used BPP to test a six species Materials and Methods). Divergence times among putative scenario (Figure 1B-b). The results supported the validity of all species were estimated with BEAST v1.7.4 based on the six species with high posterior probabilities (PP≥0.99, concatenated gene (Bouckaert et al., 2014). Specimens Supplementary Table S5) and the specific status of T. sp. 1 collected for morphometric analyses, combined with detailed (PP≥0.99). skull data from Cheng et al. (2017), included two T. cinereus, A summary of the descriptive morphometric variables is 29 T. daloushanensis, 21 T. chapensis, three T. nanus, and given in Supplementary Table S2. Based on principal nine T. sp. 1 specimens. Morphometric data were taken using component analysis of the 11 craniodental measurements, the digital calipers to the nearest 0.01 mm (Table 1), and following eigenvalues of two factors exceeded 1.0. The first principal the measurements described in Cheng et al. (2017) component (PC1) explained 63.52% of total variation, with an (Supplementary Materials and Methods). The skull of voucher eigenvalue of 6.987, which was dominated by ZMW, GLS, specimen AE1902HS04 was broken in transit, so its LUIM, CBL, BL, M1–M1, LNM–FLM, HCV, and UML associated morphometric data are missing from this study. (descriptions of all morphometric acronyms can be found in Principal component analysis (PCA) and canonical Table 1). The second principal component (PC2) explained discriminant function analysis (DFA) were used to compare 14.66% of total variation, with an
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