Cryptic Diversity and Taxonomic Revision Within the Speciose Genus Hipposideros (Hipposideridae)
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Acta Chiropterologica, 19(1): 1–18, 2017 PL ISSN 1508-1109 © Museum and Institute of Zoology PAS doi: 10.3161/15081109ACC2017.19.1.001 Towards navigating the Minotaur’s labyrinth: cryptic diversity and taxonomic revision within the speciose genus Hipposideros (Hipposideridae) NICOLE M. FOLEY1, STEVEN M. GOODMAN2, 3, CONOR V. W HELAN1, SEBASTIEN J. PUECHMAILLE1, 4, and EMMA TEELING1, 5 1School of Biology and Environmental Science, University College Dublin, Belfield, Dublin 4, Ireland 2Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, IL, USA 3Association Vahatra, BP 3972, Antananarivo 101, Madagascar 4Applied Zoology and Nature Conservation, Greifswald University, Greifswald, Germany 5Corresponding author: E-mail: [email protected] Recent molecular evidence has shown that the largest genus of the family Hipposideridae, Hipposideros, is paraphyletic with respect to H. commersonii sensu lato and H. vittatus, both belonging to a species complex referred to as the commersonii group. The taxonomic issues at the generic level of certain species of Hipposideros remain unresolved in part related to insufficient material in previous molecular studies. Herein, we expand sampling of the commersonii group and include H. commersonii sensu stricto from its type locality, Madagascar. Our phylogenetic analysis revealed that the commersonii group forms a highly supported monophyletic clade with H. cyclops, which is sister taxa to Aselliscus and Coelops. A combination of phylogenetic and comparative morphological analyses, as well as divergence time estimates, were used to provide compelling evidence to support the placement of the clade containing the commersonii group and that with H. cyclops in two resurrected genera, Macronycteris and Doryrhina, respectively. Divergence time estimates indicated that Macronycteris and Doryrhina diverged 19 mya and separated from Coelops and Aselliscus in the Oligocene, about 31 mya. The commersonii group underwent a rapid radiation as recently as 3 mya likely in response to favourable climatic conditions during the Late Pliocene in Africa. Phylogenetic analysis of Cyt-b could not resolve relationships within this morphologically conserved complex. Further sampling is necessary to fully elucidate the evolutionary history of Doryrhina. Given that cryptic species are widespread among bats, including within the genus Hipposideros, this study highlights the shortcomings of current chiropteran taxonomy to describe hidden diversity. Key words: cryptic diversity, taxonomy, Doryrhina, Macronycteris, Hipposideros, phylogeny, molecular clock dating INTRODUCTION widespread in echolocating bats (Jones, 1997). In - deed, this has been found to be true of species across Morphologically similar or identical cryptic the bat phylogenetic tree, which despite cryptic taxa species pose a challenge to traditional systematics, being almost identical morphologically, have been which typically has relied on discrete morphological shown to be distinct at the molecular level (Castella differences to delimit species. However, since the et al., 2000; Khan et al., 2010; Puech maille et al., advent of PCR, DNA sequence data has meant that 2014b; Dool et al., 2016; Gager et al., 2016). Fur - the detection of speciation in the absence of evident thermore, these studies also highlight how current morphological change has become possible (Bick - taxonomy, which is often central to management ford et al., 2007; Tsang et al., 2016). Cryptic speci- and conservation planning, may be insufficient to ation is thought to be particularly prevalent in taxa describe the diversity of extant species (Bickford et which communicate by non-visual means or are al., 2007). subject to evolutionary constraints induced by ex- For many years the relationships within the treme environmental conditions (Bickford et al., Hipposideridae have been considered a grand chal- 2007). Particularly, due to their use of echoloca- lenge in chiropteran systematics with Bogdanowicz tion as a complex and non-visual means of com- and Owen (1998) comparing the phylogeny of munication (Schuchmann et al., 2012; Puechmaille the Hipposideridae with the mythological Mino- et al., 2014a), cryptic diversity is expected to be taur’s labyrinth of ancient Greece. Their seminal Acta Chiropterologica, 19(1): 19–39, 2017 PL ISSN 1508-1109 © Museum and Institute of Zoology PAS doi: 10.3161/15081109ACC2017.19.1.002 A taxonomic revision of the Kerivoula hardwickii complex (Chiroptera: Vespertilionidae) with the description of a new species HAO-CHIH KUO1, 6, PIPAT SOISOOK2, YING-YI HO3, GABOR CSORBA4, CHUN-NENG WANG1, and STEPHEN J. ROSSITER5 1Institute of Ecology and Evolutionary Biology, National Taiwan University, Taipei 10617, Taiwan 2Princess Maha Chakri Sirindhorn Natural History Museum, Faculty of Science, Prince of Songkla University, Hat Yai, Songkhla 90112, Thailand 3Department of Biological Sciences, National Sun Yat-sen University, Kaohsiung 80424, Taiwan 4Department of Zoology, Hungarian Natural History Museum, Baross u. 13, H-1088 Budapest, Hungary 5School of Biological and Chemical Sciences, Queen Mary University of London, London E1 4NS, United Kingdom 6Corresponding author: E-mail: [email protected] Since its discovery, the taxonomic status of the only species of Kerivoula (Chiroptera: Vespertilionidae: Kerivoulinae) to be found on Taiwan has been confused. Previous studies have assigned this species to either Kerivoula hardwickii or K. titania, both of which occur on continental SE Asia. This uncertainty supports repeated suggestions in the literature that specimens of K. hardwickii collected and/or sampled across SE Asia are likely to represent multiple cryptic taxa. To address these issues, we combined new and existing data from the genus Kerivoula on Taiwan and continental Asia, and performed diagnostic analyses in steps. First, phylogenetic reconstructions based on mitochondrial and nuclear DNA revealed a well-supported group comprising all taxa currently recognized as K. hardwickii, together with the Taiwanese Kerivoula and Kerivoula kachinensis to the exclusion of all other congeneric species. Second, focusing on all members of this monophyletic clade (i.e., K. hardwickii complex) together with K. titania, we used multivariate statistical methods to separate taxa based on morphometric data. Our results provide strong evidence that among these bats, the Taiwanese Kerivoula is a new species that also occurs on continental Asia, for which we provide a formal description and name. In addition, we show that the subspecies K. hardwickii depressa should be elevated to species status. We discuss our findings and the caveats of this and similar studies. Key words: Kerivoula, new species, systematics, taxonomic revision, woolly bats INTRODUCTION inventories until the introduction and establishment of the harp trap as the preferred method for survey- The genus Kerivoula contains species that are ing forest-interior bat species in the Old World commonly referred to as woolly bats. This genus, to- (Fran cis, 1989). gether with its sister genus Phoniscus, is classified Although the taxonomy and systematics of under the subfamily Kerivoulinae. Woolly bats Kerivoula species have remained poorly known for occur in both the Indomalaya-Australasia and Afro - many years, several recent studies have gathered tropic ecozones, where, respectively, 12 and seven morphological and/or molecular evidence from mul- distinct species were recognized by Simmons tiple Kerivoula specimens from Indo-Malaya, pro- (2005), although three additional species have been viding some valuable insights into species delimita- described from the former region since then (Bates tion. For example, the systematics and taxonomy of et al., 2004, 2007; Francis et al., 2007). All Keri - Kerivoula from peninsular Malaysia and Borneo voula species appear to forage in dense vegetation have been explored by combining evidence from using broadband calls (Kingston et al., 1999, 2003; mito chondrial (mt) DNA, nuclear (nc) DNA, kary- Schmieder et al., 2012) and roost in foliage or tree otypes and morphological characters (Khan et al., cavities (e.g., Rossiter et al., 2012). The apparent 2010) as well as by multivariate morphometric anal - ability of Kerivoula species to detect and avoid mist yses (Hasan and Abdullah, 2011). Similarly, Dou an g- nets explains their poor representation in species boubpha et al. (2016) combined mitochondrial DNA Acta Chiropterologica, 19(1): 41–50, 2017 PL ISSN 1508-1109 © Museum and Institute of Zoology PAS doi: 10.3161/15081109ACC2017.19.1.003 Comparative chromosomal studies in Rhinolophus formosae and R. luctus from China and Vietnam: elevation of R. l. lanosus to species rank MARIANNE VOLLETH1, 10, NGUYEN TRUONG SON2, YI WU3, YUCHUN LI4, WENHUA YU3, LIANG-KONG LIN5, SATORU ARAI6, VLADIMIR TRIFONOV7, THOMAS LIEHR8, and MASASHI HARADA9 1Department of Human Genetics, Otto von Guericke University, Leipziger Strasse 44, 39120 Magdeburg, Germany 2Department of Vertebrate Zoology, Institute of Ecology and Biological Resources and Graduate University of Sciences and Technology, Vietnam Academy of Sciences and Technology, 18 Hoang Quoc Viet, Cau Giay, Hanoi, Vietnam 3College of Life Sciences, Guangzhou University, 230 Wei Huan Xi Road, Guangzhou, 510006, China 4Marine College, Shandong University, Weihai, 264209, China 5Laboratory of Wildlife Ecology, Department of Biology, Tunghai University, No. 1727, Sec. 4. Taiwan Boulevard, Xitun District, Taichung 40704, Taiwan 6Infectious