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Systematics of the Hipposideros turpis complex and a description of a new subspecies from Vietnam
Abstract
Hipposideros turpis is traditionally known as a species composed of three subspecies, H. t. turpis , H. t. alongensis and H. t. pendleburyi , distributed disjunctly in south‐west Japan, north‐east Vietnam and south‐west Thailand, respectively. Prior to the present study, the systematic status of forms within the species remained unclear.
Using morphological (external, bacular, cranial and dental characters), genetic and echolocation data, we demonstrate that turpis , alongensis and pendleburyi represent three distinct species, and that these species are endemic to Japan, Vietnam and Thailand, respectively. They are very distinct genetically and do not even form a monophyletic group.
We also prove that H. alongensis is composed of two subspecies, H. a. alongensis and H. a. sungi . The latter subspecies is described as new to science. To date, H. a. alongensis appears to be restricted to the Cat Ba Island of Cat Ba National Park, west Ha Long Bay, whereas H. a. sungi ssp. nov. is known from three localities in mainland northeast Vietnam. These two subspecies are distinguished by body size, molecular data and the frequency of the constant‐frequency component of their echolocation signals.
... Subsequently, bat surveys were carried out several times in the park between 1997 and 2001 (Bates et al., 1997;Bates et al., 1999;Hendrichsen et al., 2001). Specimen examinations and literature reviews for those surveys revealed that eight hipposiderid species were recorded by those surveys: Aselliscus stoliczkanus, Coelops frithii, Hipposideros armiger, Hipposideros bicolor, Hipposideros larvatus, Hipposideros lylei, Hipposideros pomona and Hipposideros turpis (Hendrichsen et al., 2001;Le Vu Khoi et al., 2001;Borrisenko & Kruskop, 2003;Dang Ngoc Can et al., 2008;Thong et al., 2012;Kruskop, 2013). However, echolocation calls of the bats from the park were almost undocumented in the past publications, although they are useful for acoustic identification, monitoring, and other research purposes (Schnitzler & Kalko, 1998;Furey et al., 2009;Schnitzler & Denzinger, 2011;Denzinger & Schnitzler, 2013;Denzinger et al., 2016). ...
... However, echolocation calls of the bats from the park were almost undocumented in the past publications, although they are useful for acoustic identification, monitoring, and other research purposes (Schnitzler & Kalko, 1998;Furey et al., 2009;Schnitzler & Denzinger, 2011;Denzinger & Schnitzler, 2013;Denzinger et al., 2016). was found to be The only publication containing a call parameter (the values of the constant-frequency modulated component) of Hipposideros alongensis was by Thong et al. (2012) which was subsequently cited by Kruskop (2013). To fill in this knowledge gap on echolocation research in the park, three field surveys were conducted between April 2021 and April 2022, and museum specimens were examined as well. ...
... Juveniles were released and excluded from the analyses of identification to reduce the influence of age variation. Four morphological measurements (forearm length -FA, Ear height -EH, Ear width -EW, and noseleaf width -NW) of every captured adult individual were taken using callipers, then identified through a comparison with the data of the species in the past publications (Bates et al., 1997;Bates et al., 1999;Hendrichsen et al., 2001;Borrisenko & Kruskop, 2003;Thong et al., 2012;Kruskop, 2013;Wilson & Mittermeier, 2019;Yuzefovich et al., 2021;Yuzefovich et al., 2022). A total of 238 bat individuals and 61 museum specimens were captured and examined, respectively. ...
Cuc Phuong is the oldest and most well-known National Park in Vietnam. With its large primary forest area and karst cave systems, it is assumed to be an ideal home to a highly diverse bat fauna. However, species diversity and echolocation of bats in this park are poorly characterized. Between April 2021 and April 2022, three bat surveys were conducted in the park with special attention on the species of the family Hipposideridae. The bat specimens collected previously from the park were also examined. According to past records, hipposiderids in the park comprised at least seven species: Aselliscus stoliczkanus, Coelops frithii, Hipposideros alongensis, Hipposideros armiger, Hipposideros gentilis, Hipposideros lylei and Hipposideros poutensis. In this series of field surveys, six of these seven species were captured while Coelops frithii was only confirmed from specimen examination. Each species is clearly distinguishable by their morphology and echolocation calls. This study provides the first comparison of echolocation calls of all seven species which will be useful for potential acoustic identification and monitoring bats in the park and surrounding areas in future.
... Among the protected area systems in Vietnam, Cat Ba National Park has received the highest number of bat surveys with records included in at least 26 publications . Of these, 19 contained bat records with references to specimens and/or relevant information sources [2][3][4][5][6][7][8][9][10][11][12][13][14][15][16][17][18][19][20] while remaining records were based primarily upon literature reviews [21][22][23][24][25][26][27] (Table 1). Before the present study, information on bat diversity of CBBR was not considered to be comprehensive because almost all previous bat surveys were conducted within the Cat Ba National Park with an emphasis on Cat Ba Island [5][6][7][8][9][10][11][12][13][15][16][17]20]. ...
... Of these, 19 contained bat records with references to specimens and/or relevant information sources [2][3][4][5][6][7][8][9][10][11][12][13][14][15][16][17][18][19][20] while remaining records were based primarily upon literature reviews [21][22][23][24][25][26][27] (Table 1). Before the present study, information on bat diversity of CBBR was not considered to be comprehensive because almost all previous bat surveys were conducted within the Cat Ba National Park with an emphasis on Cat Ba Island [5][6][7][8][9][10][11][12][13][15][16][17]20]. Apart from the unsurveyed islands, the mangrove areas within CBBR had not received attention from either bat experts or authorities for bat research and conservation by 2014. ...
... It was subsequently regarded as Hipposideros turpis alongensis [4,7]. Since 2012, its nomenclature has been confirmed as Hipposideros alongensis, which is endemic to Vietnam and comprises two subspecies: H. a. alongensis from the Ha Long Bay area including CBBR and H. a. sungi from the mainland area in northeastern Vietnam [11]. To date, records of this species from CBBR were included in 14 previous publications (Table 4). ...
The Cat Ba Biosphere Reserve is internationally renowned for its spectacular karst landscape. It covers a large area with hundreds of limestone islands and various ecosystems including caves, tropical forests, and mangroves. However, previous surveys were only conducted in terrestrial ecosystems on Cat Ba Island. Therefore, bats inhabiting mangroves and the remaining islands did not receive attention from scientists up to 2014. To initially fill in the gaps, we conducted ten bat surveys between 2015 and 2020 with an emphasis on mangroves and previously unsurveyed islands. Bats were captured using mist nets and harp traps. Twenty-three species belonging to 13 genera of six families were recorded during the surveys. Of these, four species (Macroglossus minimus, Myotis hasselti, Phoniscus jagorii, Tylonycteris fulvida) are new to the reserve. Remarkably, 15 species belonging to seven genera of five families were captured in mangrove, which is the highest species diversity for bats reported from any mangrove area in mainland Southeast Asia. Based on results from the surveys and literature review, we here provide the most updated bat diversity of the reserve with confirmed records of 32 bat species belonging to 16 genera of six families. Historical records of each species in the literature were reviewed. Two species, Scotophilus heathi and Scotophilus kuhlii, are unconfirmed because of unclear evidence in previous publications. Results of this study indicated that the mangrove ecosystem is important for bats but still poorly studied in Cat Ba Biosphere Reserve and Vietnam as a whole. In addition, morphological measurements, echolocation data, distributional records, and conservation status of each species are also given in this paper for potential research and conservation campaigns in the future
... Examples include Pteropodidae (Giannini andSimmons 2003, 2005;Giannini et al. 2006Giannini et al. , 2008Giannini et al. , 2009Esselstyn et al. 2008;Almeida et al. 2009Almeida et al. , 2011Almeida et al. , 2016Nesi et al. 2013;Hassanin 2014); Vespertilionidae Roehrs et al. 2010;Juste et al. 2013;Ruedi et al. 2013); Phyllostomidae (Baker et al. 2003Datzmann et al. 2010;Dumont et al. 2011;Rojas et al. 2016); Molossidae (Ammerman et al. 2012;Gregorin and Cirranello 2015); Mormoopidae (Simmons and Conway 2001;Van Den Bussche et al. 2002;Dávalos 2006;Thoisy et al. 2014); Emballonuridae (Lim et al. 2008;Goodman et al. 2012;Ruedi et al. 2012); Natalidae (Dávalos 2005;Tejedor 2011); Rhinolophidae (Guillén-Servent et al. 2003;Stoffberg et al. 2010;Foley et al. 2015;Bailey et al. 2016). Also, the phylogeny of speciose genera has been resolved to a significant degree of coverage; e.g., Myotis (Stadelmann et al. 2007;Larsen et al. 2012;Ruedi et al. 2013); Pteropus (Giannini et al. 2008;O'Brien et al. 2009;Almeida et al. 2014); Rhinolophus (Guillén-Servent et al. 2003;Zhou et al. 2009;Stoffberg et al. 2010); Hipposideros (Murray et al. 2012; Thong et al. 2012aThong et al. , 2012b; Artibeus (Lim et al. 2004;Redondo et al. 2008); Sturnira (Velazco and Patterson 2013). Systematic research in bats also made progress with the accelerated pace of new species discoveries (e.g., Xeronycteris vierai Gregorin and Ditchfield 2005; Hipposideros khaokhouayensis Guillén-Servent and Francis 2006; Desmalopex microleucopterus Esselstyn et al. 2008; Myotis phanluongi Borisenko et al. 2008; Rhinolophus xinanzhougguoensis Zhou et al. 2009;Glischropus bucephalus Csorba 2011;Dryadonycteris capixaba Nogueira et al. 2012; Myotis indochinensis Son et al. 2013;Histiotus diaphanopterus Feijó et al. 2015). ...
... The topology of this subgroup was congruent with that reported by Guillén-Servent and Francis (2006) with minor differences (position of H. pomona); within this subgroup, the relationships of H. pomona + (H. bicolor + H. cinerascens) to other Hipposideros were also present in Thong et al. (2012a). As shown by Guillén-Servent and Francis (2006), the morphologically similar H. ridleyi did not grouped with those species of the bicolor complex, but with H. ater instead (and here also Shi and Rabosky (2015) with H. fulvus). ...
... Alongensis and sungi) were mixed with species of the diadema group (including diadema, lekaguli, pelingensis), whereas the other former member of the complex (H. pendelburyi) appeared distantly located within the second subclade among species of the armiger (armiger, griffini) and larvatus (larvatus) species groups, as in Thong et al. (2012a). Rhinolophidae, as expected, included only the diverse Rhinolophus (>80 currently recognized species) and it was a supported major bat clade that diversified c. 14 mya (Table 6). ...
... Hipposideros, the most speciose genus of the family Hipposideridae is estimated to contain approximately 70 species (Simmons, 2005), and has extant taxa distributed throughout the Old World spanning Asia, Australia, Middle East and Africa (Nowak and Paradiso, 1999). The current number of recognized species represents an underestimate of the actual diversity of the genus, as in recent years it has been shown to be rife with cryptic diversity and several new taxa described since Simmons' tabulation (Thabah et al., 2006;Monadjem et al., 2010Monadjem et al., , 2012Monadjem et al., , 2013Murray et al.;Thong et al., 2012aThong et al., , 2012bRakotoarivelo et al., 2015). This genus has been further subdivided into nine different species groups (Simmons, 2005) based on morphological similarities; these species groups have yet to be thoroughly evaluated using molecular data (Bogdanowicz and Owen, 1998;Murray et al., 2012). ...
... The noseleaf of Doryrhina shows several particular aspects which differ from other hipposiderids, including Macronycteris. Members of the genus Doryrhina have two lat eral fleshy leaflets (Fig. 4), a common configuration in Hipposideros, although several members of this genus, as well as Macronycteris, have four leaflets (Andersen, 1905(Andersen, , 1906Payne et al., 1985;Strahan, 1995;Flannery, 1995aFlannery, , 1995bBates and Harrison, 1997;Francis, 2008;Thong et al., 2012aThong et al., , 2012bHappold, 2013c). The 2nd lateral leaflet in D. cyclops extends posteriorly and forms a continuous extension of the posterior leaf (Fig. 4). ...
... This study provides evidence from phylogenetic analysis, divergence time estimates, morphological and karyological data to support the resurrection of the genus Macronycteris for several species previously placed in the commersonii group and Doryrhina for H. cyclops. Given the cryptic nature of many taxa in the family Hipposideridae, molecular studies carried out in recent years have yielded taxonomic revisions at the level of family (Foley et al., 2015), genus (this study; Thong et al, 2012c), and in numerous cases species (Thabah et al., 2006;Monadjem et al., 2010;Murray et al., 2012;Thong et al., 2012aThong et al., , 2012bMonadjem et al., 2013;Rakotoarivelo et al., 2015;Tsang et al., 2016). While it is certainly no trivial undertaking, given the speciose nature of Hipposideros, the next step in navigating the Minotaur's labyrinth should focus on the evaluation and resolution of phylogenetic affinities between the Hipposideros species groups and species' delimitation. ...
... Hipposideros, the most speciose genus of the family Hipposideridae is estimated to contain approximately 70 species (Simmons, 2005), and has extant taxa distributed throughout the Old World spanning Asia, Australia, Middle East and Africa (Nowak and Paradiso, 1999). The current number of recognized species represents an underestimate of the actual diversity of the genus, as in recent years it has been shown to be rife with cryptic diversity and several new taxa described since Simmons' tabulation (Thabah et al., 2006;Monadjem et al., 2010Monadjem et al., , 2012Monadjem et al., , 2013Murray et al.;Thong et al., 2012aThong et al., , 2012bRakotoarivelo et al., 2015). This genus has been further subdivided into nine different species groups (Simmons, 2005) based on morphological similarities; these species groups have yet to be thoroughly evaluated using molecular data (Bogdanowicz and Owen, 1998;Murray et al., 2012). ...
... The noseleaf of Doryrhina shows several particular aspects which differ from other hipposiderids, including Macronycteris. Members of the genus Doryrhina have two lat eral fleshy leaflets (Fig. 4), a common configuration in Hipposideros, although several members of this genus, as well as Macronycteris, have four leaflets (Andersen, 1905(Andersen, , 1906Payne et al., 1985;Strahan, 1995;Flannery, 1995aFlannery, , 1995bBates and Harrison, 1997;Francis, 2008;Thong et al., 2012aThong et al., , 2012bHappold, 2013c). The 2nd lateral leaflet in D. cyclops extends posteriorly and forms a continuous extension of the posterior leaf (Fig. 4). ...
... This study provides evidence from phylogenetic analysis, divergence time estimates, morphological and karyological data to support the resurrection of the genus Macronycteris for several species previously placed in the commersonii group and Doryrhina for H. cyclops. Given the cryptic nature of many taxa in the family Hipposideridae, molecular studies carried out in recent years have yielded taxonomic revisions at the level of family (Foley et al., 2015), genus (this study; Thong et al, 2012c), and in numerous cases species (Thabah et al., 2006;Monadjem et al., 2010;Murray et al., 2012;Thong et al., 2012aThong et al., , 2012bMonadjem et al., 2013;Rakotoarivelo et al., 2015;Tsang et al., 2016). While it is certainly no trivial undertaking, given the speciose nature of Hipposideros, the next step in navigating the Minotaur's labyrinth should focus on the evaluation and resolution of phylogenetic affinities between the Hipposideros species groups and species' delimitation. ...
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.
... Examples include Pteropodidae (Giannini andSimmons 2003, 2005;Giannini et al. 2006Giannini et al. , 2008Giannini et al. , 2009Esselstyn et al. 2008;Almeida et al. 2009Almeida et al. , 2011Almeida et al. , 2016Nesi et al. 2013;Hassanin 2014); Vespertilionidae Roehrs et al. 2010;Juste et al. 2013;Ruedi et al. 2013); Phyllostomidae (Baker et al. 2003Datzmann et al. 2010;Dumont et al. 2011;Rojas et al. 2016); Molossidae (Ammerman et al. 2012;Gregorin and Cirranello 2015); Mormoopidae (Simmons and Conway 2001;Van Den Bussche et al. 2002;Dávalos 2006;Thoisy et al. 2014); Emballonuridae (Lim et al. 2008;Goodman et al. 2012;Ruedi et al. 2012); Natalidae (Dávalos 2005;Tejedor 2011); Rhinolophidae (Guillén-Servent et al. 2003;Stoffberg et al. 2010;Foley et al. 2015;Bailey et al. 2016). Also, the phylogeny of speciose genera has been resolved to a significant degree of coverage; e.g., Myotis (Stadelmann et al. 2007;Larsen et al. 2012;Ruedi et al. 2013); Pteropus (Giannini et al. 2008;O'Brien et al. 2009;Almeida et al. 2014); Rhinolophus (Guillén-Servent et al. 2003;Zhou et al. 2009;Stoffberg et al. 2010); Hipposideros (Murray et al. 2012; Thong et al. 2012aThong et al. , 2012b; Artibeus (Lim et al. 2004;Redondo et al. 2008); Sturnira (Velazco and Patterson 2013). Systematic research in bats also made progress with the accelerated pace of new species discoveries (e.g., Xeronycteris vierai Gregorin and Ditchfield 2005; Hipposideros khaokhouayensis Guillén-Servent and Francis 2006; Desmalopex microleucopterus Esselstyn et al. 2008; Myotis phanluongi Borisenko et al. 2008; Rhinolophus xinanzhougguoensis Zhou et al. 2009;Glischropus bucephalus Csorba 2011;Dryadonycteris capixaba Nogueira et al. 2012; Myotis indochinensis Son et al. 2013;Histiotus diaphanopterus Feijó et al. 2015). ...
... The topology of this subgroup was congruent with that reported by Guillén-Servent and Francis (2006) with minor differences (position of H. pomona); within this subgroup, the relationships of H. pomona + (H. bicolor + H. cinerascens) to other Hipposideros were also present in Thong et al. (2012a). As shown by Guillén-Servent and Francis (2006), the morphologically similar H. ridleyi did not grouped with those species of the bicolor complex, but with H. ater instead (and here also Shi and Rabosky (2015) with H. fulvus). ...
... Alongensis and sungi) were mixed with species of the diadema group (including diadema, lekaguli, pelingensis), whereas the other former member of the complex (H. pendelburyi) appeared distantly located within the second subclade among species of the armiger (armiger, griffini) and larvatus (larvatus) species groups, as in Thong et al. (2012a). Rhinolophidae, as expected, included only the diverse Rhinolophus (>80 currently recognized species) and it was a supported major bat clade that diversified c. 14 mya (Table 6). ...
Bats (Chiroptera) represent the largest diversification of extant mammals after rodents. Here we report the results of a large-scale phylogeny of bats based on unconstrained searches for a data matrix of 804 non-chimeric, taxonomically updated bat terminals (796 species represented by a single terminal plus three species represented by ≥2 genetically distinct subspecies), able to preliminary test the systematics of most groups simultaneously. We used nine nuclear and mitochondrial DNA sequence markers fragmentary represented for ingroups (c. 90% and 64% of extant diversity at genus and species level, respectively) and 20 diverse placental outgroups. Maximum Likelihood and Parsimony analyses applied to the concatenated dataset yielded a highly resolved, variously supported phylogeny that recovered the majority of currently recognized clades at all levels of the chiropteran tree. Calibration points based on 44 key fossils allowed the Bayesian dating of bat origins at c. 4 my after the K-Pg boundary, and the determination of stem and crown ages of intraordinal clades. As expected, bats appeared nested in Laurasiatheria and split into Yinpterochiroptera and Yangochiroptera. More remarkable, all polytypic, currently recognized families were monophyletic, including Miniopteridae, Cistugidae, and Rhinonycteridae, as well as most polytypic genera with few expected exceptions (e.g., Hipposideros). The controversial Myzopodidae appeared in a novel position as sister of Emballonuroidea―a result with interesting biogeographic implications. Most recently recognized subfamilies, genera, and species groups were supported or only minor adjustments to the current taxonomy would be required, except Molossidae, which should be revised thoroughly. In light of our analysis, current bat systematics is strongly supported at all levels; the emergent perception of a strong biogeographic imprint on many recovered bat clades is emphasized.
... Dool et al., 2013;Puechmaille, unpublished data), were used in the current study: mtDNA-R3-F, mtDNA-F2-R . Informative mammalian-specific intronic primers were available from previously published studies: ACOX2, ABHD11, COPS7A, ROGDI (designed based on whole genomic data; Igea et al., 2010;Salicini et al., 2011); BGN (Lyons et al., 1997); STAT5A (Eick et al., 2005;Matthee et al., 2001) and were chosen based on known variability within the order Chiroptera Salicini et al., 2011;Thong et al., 2012) or specifically within the family Rhinolophidae (Dool et al., 2013;Foley et al., 2015). Additionally, these markers were selected to give an independent representation of the nuclear genome; each is found on a different chromosome based on the human genome and codes for proteins in divergent pathways and therefore should not be under the same selective constraints. ...
... As successfully used in other species (e.g. Douangboubpha et al., 2016;Thong et al., 2012), a comprehensive sampling of this species group across its range and an integrative approach incorporating genetic, morphological, acoustic, and distributional data will be required to resolve the complex taxonomy of this group. A fully resolved taxonomy will greatly facilitate further phylogenetic investigations and enable meaningful comparisons between studies. ...
... When such 'pooled' species contain distantly related species (e.g. Soisook et al., 2015a;Thong et al., 2012), the phylogenetic position of a sample (attributed to the recognised species) will depend on which of these biological species has been sampled. Taking an example from the current study, if one was to sample R. swinnyi at the southern extremes of its range (in South Africa), it would be recovered as sister taxa to R. capensis (Figs. 2 and 3); if it was sampled in the middle of its range in Zimbabwe, it would be recovered as sister to R. simulator. ...
Despite many studies illustrating the perils of utilising mitochondrial DNA in phylogenetic studies, it remains one of the most widely used genetic markers for this purpose. Over the last decade, nuclear introns have been proposed as alternative markers for phylogenetic reconstruction. However, the resolution capabilities of mtDNA and nuclear introns have rarely been quantified and compared. In the current study we generated a novel ∼5kb dataset comprising six nuclear introns and a mtDNA fragment. We assessed the relative resolution capabilities of the six intronic fragments with respect to each other, when used in various combinations together, and when compared to the traditionally used mtDNA. We focused on a major clade in the horseshoe bat family (Afro-Palaearctic clade; Rhinolophidae) as our case study. This old, widely distributed and speciose group contains a high level of conserved morphology. This morphological stasis renders the reconstruction of the phylogeny of this group with traditional morphological characters complex. We sampled multiple individuals per species to represent their geographic distributions as best as possible (122 individuals, 24 species, 68 localities). We reconstructed the species phylogeny using several complementary methods (partitioned Maximum Likelihood and Bayesian and Bayesian multispecies-coalescent) and made inferences based on consensus across these methods. We computed pairwise comparisons based on Robinson-Foulds tree distance metric between all Bayesian topologies generated (27,000) for every gene(s) and visualised the tree space using multidimensional scaling (MDS) plots. Using our supported species phylogeny we estimated the ancestral state of key traits of interest within this group, e.g. echolocation peak frequency which has been implicated in speciation. Our results revealed many potential cryptic species within this group, even in taxa where this was not suspected a priori and also found evidence for mtDNA introgression. We demonstrated that by using just two introns one can recover a better supported species tree than when using the mtDNA alone, despite the shorter overall length of the combined introns. Additionally, when combining any single intron with mtDNA, we showed that the result is highly similar to the mtDNA gene tree and far from the true species tree and therefore this approach should be avoided. We caution against the indiscriminate use of mtDNA in phylogenetic studies and advocate for pilot studies to select nuclear introns. The selection of marker type and number is a crucial step that is best based on critical examination of preliminary or previously published data. Based on our findings and previous publications, we recommend the following markers to recover phylogenetic relationships between recently diverged taxa (<20 My) in bats and other mammals: ACOX2, COPS7A, BGN, ROGDI and STAT5A.
... Trong hơn 10 năm qua, khu hệ dơi của Việt Nam đã nhận được sự quan tâm đáng kể của các nhà khoa học ở trong và ngoài nước. Số lượng loài dơi ghi nhận ở Việt Nam ngày càng tăng; trong đó, có nhiều loài mới cho khoa học [32,35,36]. Đáng chú ý, một số loài dơi nếp mũi được ghi nhận ở Việt Nam trong nhiều công trình nghiên cứu trước đây là kết quả định loại sai hoặc chưa đủ cơ sở tin cậy. ...
... Thực tế, nhiều tài liệu công bố trước đây cũng không viện dẫn nguồn mẫu vật nghiên cứu của loài Dơi nếp mũi hai màu và Dơi nếp mũi lớn. Cho đến nay, chưa có thông tin chắc chắn về sự phân bố của hai loài dơi này ở Việt Nam nên chúng không được ghi trong bảng 1. Những ghi nhận về Dơi nếp mũi lông vàng (Hipposideros turpis) thực chất là kết quả định loại sai những mẫu vật thuộc loài Dơi nếp mũi hạ long (Hipposideros alongensis) [32,35]. Tất cả những tài liệu ghi nhận về Dơi nếp mũi việt nam (Paracoelops megalotis) đều căn cứ trên mô tả gốc bởi Dorst (1947) [15]. ...
... Tên khoa học Tên tiếng Việt Aselliscus stoliczkanus (Dobson, 1871) [13] Dơi nếp mũi ba lá Coelops frithii Blyth, 1848 [3] Dơi nếp mũi không đuôi Hipposideros alongensis alongensis Bourret, 1942a [6] Dơi nếp mũi bourret H. a. sungi Vu Dinh Thong et al., 2012 [35] Dơi nếp mũi sung H. armiger (Hodgson, 1835) [22] Dơi nếp mũi quạ H. ater (Templeton, 1848) [27] Dơi nếp mũi tro H. cineraceus (Blyth, 1853) [4] Dơi nếp mũi lông đen H. diadema (Geoffroy, 1813) [18] Dơi nếp mũi vương miện H. galeritus (Cantor, 1846) [9] Dơi nếp mũi nâu H. khaokhouayensis Guillén-Servent & Francis, 2006 [19] Dơi nếp mũi cát bà H. larvatus (Horsfield, 1823) [23] Dơi nếp mũi xám H. lylei Thomas, 1913 [29] Dơi nếp mũi khiên H. pomona Andersen, 1918 [1] Dơi nếp mũi xinh H. pratti Thomas, 1891 [28] Dơi nếp mũi prat H. scutinares Robinson et al., 2003 [25] Dơi nếp mũi đông dương Hipposideros griffini Vu Dinh Thong et al., 2012c [36] Dơi nếp mũi grip-phin ...
This paper provided a review of leaf-nosed bats (Hipposideridae) from Vietnam and important characteristics of a Vietnamese endemic bat species. In previous publications including bats of Vietnam, records of four species (Hipposideros bicolor, H. fulvus, H. turpis, Paracoelops megalotis) resulted from improper identification. Without doubt, records of Hipposideros turpis from Vietnam resulted from misidentification of materials of Ha Long Leaf-nosed Bat (Hipposideros alongensis), an endemic bat species to Vietnam. Its external features are similar to those of Horsfield's Leaf-nosed Bat (Hipposideros larvatus). However, Ha Long Leaf-nosed Bat and Horsfield's Leaf-nosed Bat are distinguished by body size, molecular data, and echolocation frequency. On the other hand, H. alongensis comprises two distinct subspecies: Bourret’s Leaf-nosed Bat (H. a. alongensis) and Sung’s Leaf-nosed Bat (H. a. sungi). Of which, H. a. sungi distributes in two national parks (Cuc Phuong and Ba Be) and two nature reserves (Huu Lien and Na Hang) whereas H. a. alongensis distributes in two national parks (Cat Ba and Bai Tu Long) and other islands within Ha Long Bay.
... Therefore, in this study, the echolocation calls of 133 individuals were recorded using the same methods as described by Sun et al. (2016). The resting frequency (RF) of the dominant second harmonic of the constant frequency component, which is mostly species-specific for CF-FM bats (Thong et al., 2012), was measured as a bioacoustic parameter (Appendix B). ...
... To reconstruct the changes of the effective population size over time, the extended Bayesian skyline plot (EBSP) (Heled and Drummond, 2008) was implemented in BEAST based on the Cyt-b gene and two nuclear introns. The mutation rate of 1.3×10 −8 per year for the Cyt-b gene (Nabholz et al., 2008;Thong et al., 2012) was used to calculate the time with a strict clock. The same mutation rate was also used in estimation of the time since the most recent common ancestor (TMRCA) of the main mitochondrial lineages in BEAST. ...
Species delimitation and evolutionary reconstruction remain challenging for non-model species that have experienced reticulate evolution and exhibit conflicting patterns of differentiation among multiple lines of evidence, such as mitochondrial and nuclear data and phenotypes. Here, we applied an integrative taxonomic approach to a case study of Rhinolophus macrotis complex, whose taxonomic status remains controversial, to provide insight into the systematics and evolutionary history of these species. By integrating traditional genetic markers with different modes of inheritance, genome-wide SNPs as well as phenotypic characteristics, we clarified the presence of three closely related species, R. episcopus, R. siamensis, and R. osgoodi, within this complex, and proposed a new taxonomic treatment for R. osgoodi. Our results suggested that hybridization and introgression are the main causes of low mtDNA divergence in these species. Combined with the demographic inference, we deduced that glacial-interglacial cycles drove geographic isolation and secondary contacts of these species, then promoted hybridization and lineage fusion among them, finally resulting in a reticulate evolutionary pattern. Overall, our study highlights the importance of combining multiple types of data to delimit species, especially those with conserved morphology, and to reveal the sophisticated processes of speciation.
... The PCRs were run in a thermal cycler with an amplification profile as follows. Cycling parameters for cytochrome-b gene were as Thong et al. (2012) follows: 94 C for 3 min for initial denaturation, 35 cycles of denaturation at 94 C for 30s, 72 C for 40 s for extension, and 3 min for final extension at 72 C. The PCR program used for the D-loop gene amplification consisted 35 cycles of denaturation for 1 min at 95 C, 1 min at 55 C and 1 min at 72 C. With initial denaturation step for 5 min at 94 C and a final extension step for 7 min at 72 C. Sequencing reactions were done by Macrogen Korea Laboratories. The partial mitochondrial Cytb gene and D-loop gene sequences of the bats were deposited in GenBank (Appendix 1). ...
... The dataset used in phylogenetic analyses comprised 62 specimens covering R. euryale geographical distribution in Iran and 21 sequences of the Dloop gene (Accession: AY923062, KF031268, KF031267, iKU53130, DQ417500-DQ417507, DQ417509, DQ417510, DQ417512-DQ417514, DQ417516-DQ417519) and three sequences of the Cytb gene (Accession: KU531305, KF031268, KF031267) from R. euryale in NCBI. Three species, Rhinolophus mehelyi (Accession: MH223453, MH223454, MH223434, MH223435), Rhinolophus blasii (Accession: KU531264), and Hipposideros turpis (Accession: JN247029) as closely related taxa were used as outgroups (Thong et al. 2012;Puechmaille and Emma 2014;Dool et al. 2016). This analysis was made using two markers: Cytb and D-loop genes. ...
Molecular phylogeography and species distribution modelling (SDM) suggest that late Quaternary glacial cycles have portrayed a significant role in structuring current population genetic structure and diversity. Based on phylogenetic relationships using Bayesian inference and maximum likelihood of 535 bp mtDNA (D-loop) and 745 bp mtDNA (Cytb) in 62 individuals of the Mediterranean Horseshoe Bat, Rhinolophus euryale, from 13 different localities in Iran we identified two subspecific populations with differing population genetic structure distributed in southern Zagros Mts. and northern Elburz Mts. Analysis of molecular variance (AMOVA) obtained from D-loop sequences indicates that 21.18% of sequence variation is distributed among populations and 10.84% within them. Moreover, a degree of genetic subdivision, mainly attributable to the existence of significant variance among the two regions is shown (θCT = 0.68, p = .005). The positive and significant correlation between geographic and genetic distances (R² = 0.28, r = 0.529, p = .000) is obtained following controlling for environmental distance. Spatial distribution of haplotypes indicates that marginal population of the species in southern part of the species range have occupied this section as a glacial refugia. However, this genetic variation, in conjunction with results of the SDM shows a massive postglacial range expansion for R. euryale towards higher latitudes in Iran.
... Trước nghiên cứu này, Kuznetsov (2000) [ 9] công bố danh sách 5 loài dơi thuộc 4 giống, 4 họ ở Cù Lao Chàm nhưng không cho biết cở sở thông tin cụ thể đã ghi nhận được chúng như thế nào. Trong những năm gần đây, vị trí phân loại của nhiều loài dơi hiện biết ở Việt Nam đã được tu chỉnh [ 12, 15,16]; trong đó bao gồm những loài được Kuznetsov (2000) [ 9] ghi nhận ở Cù Lao Chàm. Với mục đích góp phần đánh giá hiện trạng đa dạng sinh học của Cù Lao Chàm, tác giả đã thực hiện hai đợt khảo sát thực địa về khu hệ thú, trong đó tập trung nghiên cứu các loài dơi trong thời gian từ tháng 5 đến tháng 8 năm 2015. ...
... Trong đó, có 6 loài thuộc 3 giống, 3 họ được định loại căn cứ vào đặc điểm của những cá thể mắc lưới hoặc bẫy; 1 loài thuộc 1 giống, 1 họ được xác định căn cứ vào kết quả ghi tiếng kêu siêu âm trong sinh cảnh sống tự nhiên. [ 15,16]), đã chứng minh nhiều ghi nhận trước đây về các loài Hipposideros armiger hoặc H. larvatus ở Việt Nam là kết quả định loại sai những mẫu vật thuộc loài khác. Kết quả khảo sát thực địa trong năm 2015 không bắt gặp bằng chứng nào của cả 5 loài dơi đã được Kuznetsov (2000) [ 9] công bố ở Cù Lao Chàm. ...
Cu Lao Cham-Hoi An Biosphere Reserve, which is commly known as Cu Lao Cham, is a well-known locality in Vietnam. It has received attention from national and international scientists and public communities. However, biodiversity of the biosphere is still poorly studied. In order to provide a confirmed database of bats from Cu Lao Cham, the author conducted two bat surveys with emphases on taxonomy and echolocation between May and August 2015. The survey results indicate that Cu Lao Cham is a home to 7 species belonging to 4 genera, 4 families, 2 suborders: Cynopterus horsfieldii, Rhinolophus affinis, R. pusillus, Hipposideros galeritus, H. grandis, H. pomona và Pipistrellus abramus. Of which, H. grandis is the most common species throughout the reserve. The species was recorded during the whole surveys and at almost all forest habitats. There is not sufficient evidence to confirm the occurrence of the five bat species, which was listed in a previously published literature (Hipposideros armiger, H. bicolor, H. larvatus, Pipistrellus ceylonicus và P. javanucus) in Cu Lao Cham. This paper provides a confirmed data on diversity and conservation status of bats of the reserve.
... The genus Hipposideros currently consists of 71 species worldwide, including 16 species occurred in Vietnam [3,7,8,9,10]. The recent discovery of Griffin's Leaf-nosed bat from Vietnam has received special attention from both the public and scientific media. ...
... (2012) [9,10]. In the field, bats were captured using four-bank harp traps [6] and mist nets of various sizes (2.6 m [height], 3-12 m [length], mesh size: 16 mm × 16 mm). ...
Griffin’s Leaf-nosed bat (Hipposideros griffini) is one of the largest species of the family Hipposiderodae. In the field, it is recognisable from other hipposiderid species of Vietnam by body size, noseleaf structure, and echolocation frequency. Prior to this study, Hipposideros griffini was only known from two national parks (Cat Ba and Chu Mom Ray) in Vietnam. This paper provides new data recorded from Cat Tien national park, Southern Vietnam, indicating a more extensive distribution of Hipposideros griffini. Results from previous and current studies indicate that Griffin’s Leaf-nosed bat inhabits in various habitats ranging from flat/lowlands to offshore islands, mountainous and karst areas.
... In a recent summary, 70 species of Hipposideros were recognized [1], subsequently numerous other taxa have been described (e.g. [2][3][4][5]) and the taxonomy of the group, predominantly at the species level, is far from resolved. As a tool to understand the evolutionary history of members of this genus, closely related species are often placed in morphological species groups (e.g., [1,6]). ...
... The HKY + I substitution model was used, with the Yule speciation model as tree prior. As an alternative to fossil calibrated estimate of divergence times, an additional molecular clock analysis was conducted using a fixed mean substitution rate of 1.30 × 10 −8 subs/site/year [5,41]. This analysis was performed using the strict molecular clock model in BEAST. ...
Using a combination of molecular and morphological characters, this study presents evidence of cryptic diversity in H. commersoni on Madagascar.
... External and craniodental measurements were taken following Vu Dinh Thong (2011) [18], Vu Dinh Thong et al. (2012aThong et al. ( , 2012bThong et al. ( , 2012c) [19,20,21], Bates & Harrison (1997) [1] and Csorba et al. (2003) [7]. The measurements comprise FA, forearm length- from the extremity of the elbow to the extremity of the carpus with the wings folded; EH, ear height-length of ear conch; TIB, tibia length- from the knee joint to the ankle; HF, hind-foot length-from the extremity of the heel behind the os calcis to the extremity of the longest digit, excluding the hairs or claws; Tail: tail length, from the tip of the tail to its base adjacent to the body; SL, total length of skull-from occiput to the most anterior part of the canine; CCL, condylocanine length-from the exoccipital condyle to the most anterior part of the canine; IOW, interorbital width-the least width of the interorbital constriction; ZW, zygomatic width- the greatest width of the skull across the zygomatic arches; BW, width of braincase - greatest width of the braincase at the posterior roosts of the zygomatic arches; C1-C1, upper canine width-greatest width, taken across the outer borders of upper canines; M3-M3, upper molar width-greatest width, taken across the outer crowns of the last upper molars; C1-M3, maxillary toothrow length-from the front of upper canine to the back of the crown of the third molar; ml, mandible length-from the anterior rim of the alveolus of the first lower incisor to the most posterior part of the condyle; c1-m3, mandibular toothrow length-from the front of the lower canine to the back of the crown of the third lower molar. ...
... External and craniodental measurements were taken following Vu Dinh Thong (2011) [18], Vu Dinh Thong et al. (2012aThong et al. ( , 2012bThong et al. ( , 2012c) [19,20,21], Bates & Harrison (1997) [1] and Csorba et al. (2003) [7]. The measurements comprise FA, forearm length- from the extremity of the elbow to the extremity of the carpus with the wings folded; EH, ear height-length of ear conch; TIB, tibia length- from the knee joint to the ankle; HF, hind-foot length-from the extremity of the heel behind the os calcis to the extremity of the longest digit, excluding the hairs or claws; Tail: tail length, from the tip of the tail to its base adjacent to the body; SL, total length of skull-from occiput to the most anterior part of the canine; CCL, condylocanine length-from the exoccipital condyle to the most anterior part of the canine; IOW, interorbital width-the least width of the interorbital constriction; ZW, zygomatic width- the greatest width of the skull across the zygomatic arches; BW, width of braincase - greatest width of the braincase at the posterior roosts of the zygomatic arches; C1-C1, upper canine width-greatest width, taken across the outer borders of upper canines; M3-M3, upper molar width-greatest width, taken across the outer crowns of the last upper molars; C1-M3, maxillary toothrow length-from the front of upper canine to the back of the crown of the third molar; ml, mandible length-from the anterior rim of the alveolus of the first lower incisor to the most posterior part of the condyle; c1-m3, mandibular toothrow length-from the front of the lower canine to the back of the crown of the third lower molar. ...
To date, Wrinkle-lipped Bat (Chaerephon plicatus) is the only species of the family
Molossidae in Vietnam. It is found throughout much of Asia but rarely recorded in the country. Every published record of this species from Vietnam was only resulted from a single individual with little data on morphology. Particularly, the previous publications did not include any information about either colony size or roosting site of the species within Vietnam. Between 2001 and 2014, a series of field surveys was conducted throughout the country with an intensive search for free-tailed bat species. The obtained results indicate that Wrinkle-lipped Bat is a widespread bat
species but its known roosting sites in Vietnam are quite distjunct. Its colony size is in both seasonal and geographical variations ranging from several hundreds to over three million individuals. The species inhabits seasonally and permanently in northern and southern regions, respectively. This paper provides taxonomic and ecological assessments with an emphasis on morphological measurements, colony size, roosting habitats and national distributional range of Wrinkle-lipped Bat within Vietnam.
... We targeted one mitochondrial marker (mtDNA), including 1057 bp of cytochrome b (Cyt-b) and five nuclear markers (nDNA), consisting of 537 bp of acyl-coenzyme A oxidase 2 intron (ACOX), 618 bp of biglycan intron (BGN), 734 bp of COP9 signalsom subunit 7A intron (COPS), 493 bp of the rogdi atypical leucine zipper (ROGDI), 525 bp of the signal transducer and activator of transcription 5A intron (STAT), and 444 bp of thyrotropin beta chain precursor (THY). The primers used have been specifically designed for the order Chiroptera and provided good amplification in previous studies (see e.g., Dool et al. 2016;Jacobs et al. 2013;Puechmaille et al. 2011;Salicini et al. 2011;Thong et al. 2012). For the primer names, their sequences, and annealing temperatures, see Table S2. ...
The monophyletic Afro-Palaearctic clade of the horseshoe bats (Rhinolophus) comprises several species groups whose representatives can be morphologically similar to each other across groups. The only Rhinolophus species that occurs in Lesotho was traditionally attributed to the broadly distributed African desert- and savanna-dwelling bat, Rhinolophus clivosus, a member of the ferrumequinum group. In this study, we investigated the horseshoe bats from Lesotho with the help of molecular genetic and morphometric analyses to find their position within the group and the clade as well. The genetic analysis resulted in phylogenetic trees with two different topologies, although in both trees the Lesotho bats were a part of the fumigatus group instead of the ferrumequinum group. In the mitochondrial tree, the Lesotho bats were mixed with Rhinolophus damarensis. On the contrary, the Lesotho bats formed a single distinct lineage on the nuclear tree, closely related to Rhinolophus darlingi, R. fumigatus, and R. damarensis (in a single lineage each). These results indicate introgressions of mtDNA from the Lesotho bats to R. damarensis. Morphologically, the Lesotho bats grouped distinctly from other species of the fumigatus and ferrumequinum groups. We thus consider the Lesotho horseshoe bats to be a new separate species that is here described.
... Bats were captured and handled following guidelines recommended by the American Society of Mammalogists [7,8]. A mumber of field surveys at six localities including Cat Ba National Park, Ha Long Bay were conducted following Thong et al. [9][10][11] between May 2017 and October 2020. Four-bank harp traps and mist nets of 6.0 m (height) × 9.0-12.0 ...
Bat flies are highly specialized ectoparasites of the superfamily Hippoboscoidea and only associate with bats. They were rarely documented in Vietnam due to limited study in the country. Between 2017 and 2020, we conducted a series of field surveys in six localities in northern and central Vietnam with an emphasis on bat flies. Bats were captured using mist nets, harp traps, and handnets then morphologically identified following literatures relevant to the bats of each study site. Bat flies were collected using fine forceps and preserved in 70% alcohol for morphological identification. Twelve individuals of Brachytarsina cucullata and thirty-five individuals of Raymondia pseudopagodarum of the family Streblidae were collected over the surveys. Of which, B. cucullata is new to two localities in northern Vietnam (Nham Duong Mountain Area and Ha Long Bay) while R. pseudopagodarum is new to five localities in both northern and southern Vietnam (Bach Ma National Park, Cat Ba National Park, Ha Long Bay, Cu Lao Cham Island and Sop Cop Nature Reserve). Within Vietnam, B. cucullata and R. pseudopagodarum were only recorded from Cat Ba National Park and Vu Quang National Park, respectively. Notably, the previous records from Vietnam did not include either description or illustration. We here provide brief descriptions and illustrated photos of each species for morphological identification of these two bat fly species. A map showing the distributional records of each species is also included in this paper.
... Later it was shown, that H. alongensis, which was long regarded as one of H. larvatus subspecies, not belong to the latter species (Topal 1975(Topal , 1993 and represents a distinct phylogenetic lineage within the large Hipposideros (Thong et al. 2012;Yusefovich et al. 2020). Kitchener and Maryanto (1993) undertook a detailed study of the Sunda material of the H. larvatus species complex and reveal a quite high cryptic diversity within. ...
Hipposideros larvatus sensu lato constitutes a widespread species complex consisting of morphologically similar forms with a taxonomy that is in need of a revision. Here we present the results of a phylogenetic analysis of members of this species complex based on two mitochondrial (CytB and COI) and seven nuclear (ABHD11, ACOX2, COPS, RAG2, ROGDI2, SORBS2 and THY) genes, and a morphometric analysis. Morphological data, although showing certain diversity, does not allow an accurate delimitation of the taxonomic boundaries and occasionally contradict to genetic grouping. The molecular analyses based on mitochondrial data support the paraphyly of the H. larvatus species complex, with H. armiger recovered nested within. The nuclear data recovered all the lineages of H. larvatus sensu lato forming a monophyletic clade. Within it, apparently four different species-level clades could be revealed in Southeast Asia. One is distributed in northern Myanmar, southern China (including Hainan) and northern Vietnam, and also reaches into central Vietnam along the coast (Cham Islands). The valid name for this taxon must be H. poutensis Allen. The second clade is comprised by populations inhabiting the Malay Peninsula and the Sunda Islands, we identify this taxon as H. larvatus sensu stricto. The third taxon was identified only from southern Myanmar. The fourth taxon is distributed in southern and central Indochina. Its representatives were not related to any of the forms identified in Myanmar, and therefore, its previous identification with H. grandis sounds questionable. Since both the third and fourth taxa cannot now be unambiguously associated with a particular named form, we conventionally designate them as H. cf. grandis 1 and 2.
... The roost size varies according to regions, with an average of 16 individuals per roost in India, and maternity colonies of 100-200 mature individuals in Eastern Asia (Taiwan) (Huang et al. 2019b;Molur et al. 2002). In Southeast Asia, the species has been found to coexist with other cave-dwelling bat species, mainly Hipposideridae and Rhinolophidae (Fang and Cheng 2011;Thong et al. 2012). The species performs slow but highly maneuverable flight potentially impacting its ability to disperse and reportedly making captures in the field difficult (Furey et al. 2010). ...
Here, we report the rediscovery of Coelops frithii in the pristine mangrove forest of Sundarbans Forest Reserve in Khulna division of Bangladesh. A dead individual of adult female was collected and identified to species based on morphological features and skull measurements (FA: 41.28 mm, GTL: 17.52 mm, CCL: 15.58 mm). This finding represents the first record from the type locality one and a half century after Blyth (1848) first described the species. C. frithii is considered near threaten in the IUCN Red List. The confirmed occurrence through this record calls for future systematic surveys of this species within the Sundarbans.
... The Pendlebury's leaf-nosed bat (Hipposideros pendleburyi) was named by Chasen in 1936 but had long been included in Hipposideros turpis (Lekagul and McNeely 1977;Corbet and Hill 1992;Francis 2008). Only a decade ago, it has been regarded as a distinct species and known only from peninsular Thailand (Soisook 2011;Thong et al. 2012). This species was found in limestone areas of seven provinces in peninsular Thailand with a colony size of up to 800 individuals (Soisook 2019). ...
This study presents the first complete mitochondrial genome of the Hipposideros pendleburyi (Pendlebury's leaf-nosed bat), an endemic species in Thailand. The mitochondrial genome was 16,820 bp in length and contains 13 protein-coding genes, 2 ribosomal RNA genes, 22 transfer RNA genes, and a control region. The overall base composition was 31.5% A, 26.2% T, 28.3% C, and 14.0% G. A maximum-likelihood tree revealed that H. pendleburyi was grouped with Hipposideros armiger within the Hipposideridae clade, which has Rhinolophidae as a sister clade.
... Old World leaf-nosed bats, genus Hipposideros Gray, 1831, also known as roundleaf bats, are a highly speciose group of the family Hipposideridae, which exhibits a high level of cryptic diversity (Foley et al., 2015(Foley et al., , 2017Guillén-Servent & Francis, 2006;Kingston et al., 2001;Monadjem et al., 2013Monadjem et al., , 2019Thabah et al., 2006;Thong et al., 2012;Vallo et al., 2008). The Hipposideros caffer complex, which occurs throughout sub-Saharan Africa and in the southwestern part of the Arabian Peninsula, traditionally comprises two recognized, though cryptic, morphological species: ...
en Levels of biodiversity are globally underestimated, especially in tropical ecosystems. This is particularly so for bats compared to other mammalian taxa, due to morphological conservatism. Here, we investigate West African bats of the Hipposideros caffer complex, an insectivorous bat group occurring throughout the Afrotropics. From samples collected in Ghana, we aim to resolve the cryptic diversity identified by mitochondrial (mt) DNA using nuclear genetic, acoustic, and external morphometric data. We confirmed the presence of four previously established mtDNA lineages within the H. caffer complex and found significant genetic divergence among lineages based on nuclear microsatellite data and significant differences in frequencies of echolocation calls and morphometric measures. From these new data, we conclude that H. caffer complex in West Africa consists of at least four distinct species. While the small-sized species from coastal savanna could be assigned to H. caffer tephrus, the taxonomic identity of the three sympatric, similarly sized species pertaining to H. ruber from the forest zone of Central Ghana is yet to be assessed.
Zusammenfassung
de Die Artenvielfalt vieler Ökosysteme wird generell oft unterschätzt, insbesondere in den Tropen. Dies trifft besonders für Fledermäuse zu, bei denen sich, im Vergleich zu anderen Säugetiergruppen, zahlreiche morphologisch sehr ähnliche Arten finden. Wir untersuchten die westafrikanischen Vertreter des Hipposideros caffer - Komplexes, einer in der gesamten Afrotropis verbreiteten Gruppe insektivorer Fledermausarten. Basierend auf Material aus Ghana untersuchten wir vier über mtDNA zuvor bereits identifizierte Linien mittels Kernmikrosatelliten-Daten sowie akustischer und morphometrischer Daten. Unsere Ergebnisse bestätigen die Existenz von vier mtDNA-Linien innerhalb des H. caffer-Komplexes und zeigen nun auch anhand von Kernmikrosatellitendaten eine signifikante genetische Divergenz der einzelnen Linien, sowie signifikante Unterschiede in Echoortungsfrequenzen und morphometrischen Parametern. Unsere neuen Daten belegen, dass der H. caffer-Komplex in Westafrika aus mindestens vier Arten besteht: Während relativ kleine Individuen der Küstensavanne Ghanas wohl zur Art H. tephrus gehören, kann die taxonomische Identität der drei ähnlich großen, sympatrischen Arten aus der Waldzone von Zentralghana, die aktuell H. ruber zugeordnet werden, bislang noch nicht abschließend beurteilt werden.
... The u is equal to µgk, where µ is the mutation rate per nucleotide, g is the generation time and k is the sequence length. We used a mutation rate of 1.3 × 10 −8 per year for cytb based on previous studies on bats [40,41] and a generation time of two years based on data from a congeneric species [21]. ...
Determining the evolutionary history and population drivers, such as past large-scale climatic oscillations, stochastic processes and ecological adaptations, represents one of the aims of evolutionary biology. Hipposideros larvatus is a common bat species in Southern China, including Hainan Island. We examined genetic variation in H. larvatus using mitochondrial DNA and nuclear microsatellites. We found a population structure on both markers with a geographic pattern that corresponds well with the structure on mainland China and Hainan Island. To understand the contributions of geography, the environment and colonization history to the observed population structure, we tested isolation by distance (IBD), isolation by adaptation (IBA) and isolation by colonization (IBC) using serial Mantel tests and RDA analysis. The results showed significant impacts of IBD, IBA and IBC on neutral genetic variation, suggesting that genetic variation in H. larvatus is greatly affected by neutral processes, environmental adaptation and colonization history. This study enriches our understanding of the complex evolutionary forces that shape the distribution of genetic variation in bats.
... (Ronquist and Huelsenbeck, 2003). The dataset used in phylogenetic analyses comprised 46 specimens covering R. mehelyi geographical distribution in Iran and 13 sequences of the D-loop gene and 4 sequences of the Cytb gene (Puechmaille and Emma, 2014;Dool et al., 2016;Dragu and Borissov, 2011) from R. mehelyi in Spain, Tunisia and Romania and three outgroup species, R. euryale, R. blasii, and Hipposideros turpis as closely related taxa were used as outgroups (Najafi et al., 2018b;Dool et al., 2016;Thong et al., 2012). The most appropriate substitution model for BI and ML analysis was estimated with program jModelTest, version 0.1.1 (Posada, 2008) under the Akaike Information Criterion (AIC). ...
Mehely’s horseshoe bat, Rhinolophus mehelyi Matschie 1901, is a medium-sized rhinolophid with a discontinuous distribution from North Africa and southern Europe through Asia Minor, Anatolia, to Transcaucasia and Iran. Here, we present a detailed study of the phylogeography and population genetics of this species using 745 bp of the mitochondrial cytochrome b and 522 bp of the mitochondrial D-loop genes in 46 bats in eight localities in western and southwesternIran. Based on the mtDNA sequences, we found a low degree of genetic diversity in the Iranian populations of R. mehelyi (π = 0.0032 for Cytb and π = 0.0064 for D-loop gene), that show a close relationship among the haplotypes. With a K2P genetic distance (0.38%–0.97% on D-loop and 0.22%–0.69% on Cytb), and the phylogenetic reconstruction in the Eurasia lineage two major clades are introduced. Here, the phylogenetic trees and statistical parsimony network showed all Iranian samples were grouped in the same clade, but southern Europe and North Africa samples belonged to another clade. The average genetic divergence between reciprocally monophyletic clade of the R. mehelyi group in Iran and southern Europe and North Africa were 0.69% for Cytb and 4.09% for D-Loop respectively. The analysis of population structure suggests an incongruent pattern of genetic differentiation. Mismatch distributions and neutrality tests showed recent historical demographic events as indicated by significant deviations in Fu’s FS from neutrality. The hypothesis of sudden-expansion was not rejected by analyses of mismatch distribution as the Raggedness and SSD were insignificant (p(r) = 0.11 and p (SSD) = 0.07). Similarly, the Bayesian skyline plot suggested a population expansion scenario that took place in the past 4.000 years.
... Many bat species have evolved species-specific echolocation call structures to locate, navigate and communicate (Griffin 1958, Jones andSiemers 2010), thereby facilitating acoustic identification (Ahlen andBaagoøe 1999, Parsons andJones 2000). In addition, many cryptic species in various bat genera were initially identified based on acoustic divergence; these initial identifications were later confirmed using morphological and/or genetic data (Barratt et al. 1997, Soisook et al. 2008, Thong et al. 2012, Thoisy et al. 2014). In addition, divergences in acoustic signals play a key role in speciation (Jones 1997). ...
Bats play important roles in ecosystems, and are thus considered bioindicators. Libraries of echolocation calls provide huge potential resources for bat species identifications, ecological studies and conservation surveys. Here, the echolocation calls of two morphologically similar bat species ( Miniopterus magnater and Miniopterus fuliginosus ) were recorded and described in order to characterize vocal signatures for field identification in China. Both M. magnater and M. fuliginosus emitted short frequency modulated echolocation calls with narrow bandwidths. Each call of the former species included two harmonics, with the first harmonic being the strongest, whereas calls of the latter species normally contained one harmonic. Although call durations were similar between the two species, there were significant differences in start, end and peak frequencies between M. magnater and M. fuliginous . The results showed that 92.3% of all calls recorded in China were attributed to the correct species based on spectral features of echolocation calls. We concluded that echolocation calls are valuable characters for the identification of morphologically similar bat species.
... Trong những năm 2015 và 2017, chúng tôi đã thực hiện 2 đợt điều tra về các loài dơi và ngoại ký sinh ở dơi trong phạm vi Vườn Quốc gia Cát Bà và vùng phụ cận. Phương pháp thu mẫu dơi trên thực địa được thực hiện theo Vu Dinh Thong (2011), Vu Dinh Thong et al. (2012a, 2012b, Vũ Đình Thống và nnk. (2016). ...
Cat Ba National Park contains a high diversity fauna of bats including a species endemic to Vietnam. Since 1999, we conducted a series of bat surveys in the park with an investigation into bat files. All individuals of flies collected from each bat individual were preserved in a plastic tube filled with pure alcohol. They were analysed and identified at the Institute of Ecology and Biological Resources. Results from our research provide records of 8 bat fly species belonging to 4 genera, 2 families; of these, 3 species belong to the family Nycteribiidae (Basila roylii, B. burmensis, B. pundibunda) and 5 remaining ones belong the family Streblidae (Ascodipteron phyllorhinae, A. wenzeli, Brachytarsina amboiensis, B. cucullata, Maabella stomalata). These fly species parasitize 8 bat species belonging to 4 families: 5 species of Hipposideridae (Hipposideros alongensis, H. armiger, H. grandis, H. khoukhouayensis, H. pomona), 1 species of Miniopteridae (Miniopterus fuliginosus), 1 species of Rhinolophidae (Rhinolophus marshalli) and 1 species of Vespertilionidae (Hypsugo pulveratus). Basilia pundibunda was the most common bat fly species within the study area. The first data on ecological correlation between flies and bats from Vietnam were also recorded and given in this paper. Citation: Nguyen Thanh Luong, Ta Huy Thinh, Vu Dinh Thong, 2018. Diversity and ecology of bat flies (Diptera: Nycteribiidae, Streblidae) from Cat Ba National Park. Tap chi Sinh hoc, 40(1): x-xx. DOI: 10.15625/0866-7160/v40n1.10746. *Corresponding author: vudinhthong@hotmail.com Received 22 September 2017, accepted 2 December 2017
... We obtained body size data, in grams, for 751 of 799 bat species plus a few distinct subspecies (making up 804 bat terminals) represented in our phylogenetic hypothesis, from specific sources (Schober and Grimmberger 1997;Bonaccorso 1998;Churchill 1998;Smith et al. 2003;Gannon et al. 2005;Goodman et al. 2006;Aguirre 2007;Decher and Fahr 2007;dos Reis et al. 2007;Garbutt 2007;Pacheco et al. 2007;Zhang et al. 2007;Magalhaēs and Costa 2009;Lim et al. 2010;Harvey et al. 2011;Mendes 2011;Threlfall et al. 2011;Hasan et al. 2012;Patterson and Webala 2012;Thong et al. 2012;Kruskop 2013;Monadjem et al. 2013;Dammhahn and Goodman 2014;Huang et al. 2014;Kawai et al. 2014;Lu et al. 2014; Sedlock et al. 2014; Table SI.1). For each species, we averaged the values from all available sources, excluding some data judged unreliable (e.g., extreme values, juveniles, etc.). ...
Bats are atypical small mammals. Size is crucial for bats because it affects most aerodynamic variables and several key
echolocation parameters. In turn, scaling relationships of both flight and echolocation have been suggested to constrain bat body
size evolution. Previous studies have found a large phylogenetic effect and the inclusion of early Eocene fossil bats contributed to
recovering idiosyncratic body size change patterns in bats. Here, we test these previous hypotheses of bat body size evolution using a
large, comprehensive supermatrix phylogeny (+800 taxa) to optimize body size and examine changes reconstructed along
branches. Our analysis provides evidence of rapid stem phyletic nanism, an ancestral value stabilized at 12 g for crown-clade
Chiroptera followed by backbone stasis, low-magnitude changes inside established families, and massive body size increase at
accelerated rate in pteropodid subclades. Total variation amount explained by pteropodid subclades was 86.3%, with most
changes reconstructed as phyletic increases but also apomorphic decreases. We evaluate these macroevolutionary patterns in
light of the constraints hypothesis, and in terms of both neutral and adaptive evolutionary models. The reconstructed macroevolution
of bat body size led us to propose that echolocation and flight work as successive, nested constraints limiting bat evolution
along the body size scale.
... The topology of the phylogenetic tree based on the preliminary analysis of CytB gene (with only one specimen of the new subspecies available) is very similar to that of the COI, but with a distance between the two subspecies of 1.65%. Based on substitution rate, the divergence time can be estimated at approximately 1.2 million years ago (Thong et al. 2012) or during one of the Pleistocene glacial periods. Further genetic analysis with additional samples and nuclear markers for a more accurate divergence time is currently being carried out (P. Soisook, unpublished data). ...
The Great evening bat Ia io Thomas, 1902, previously considered as an endemic to the Indochinese subregion, is reported from the Sundaic subregion for the first time based on specimens collected from three localities in Surat Thani Province and Phang Nga Province, peninsular Thailand. It is described herein as a new subspecies based on its substantially larger body and skull size. The mitochondrial COI and cytochrome b genes reveal that the new subspecies has a genetic distance of 1.89% and 1.65%, respectively, from the nominate subspecies. Echolocation calls comprise four harmonics, with the maximum energy in the first harmonic (fmaxe) of 23.6–27.4 kHz. Notes on the population size as well as roosting and foraging behaviour are also provided.
... This species was regarded as one of the most common species of the genus in Indo-Malayan region with four assigned subspecies (Cobert and Hill 1992). In Indochina, two subspecies, Hipposideros larvatus alongensis and Hipposideros larvatus grandis, were elevated to species rank (Simmons 2005;Thong et al 2012), while H. larvatus sensu stricto is recently regarded as a cryptic species complex (Francis et al 2010). ...
Three short field surveys were conducted in the Phia Oac-Phia Den Nature Reserve to assess the species
diversity and endemism of local bat fauna. In combination with data from a previous study, 24 bat
species of 5 families, representing > 20% of the national bat diversity, were recorded in the study area.
The occurrence of several bat species restricted to montane forests, that is, Murina chrysochaetes,
Pipistrellus coromandra, and a potentially new species Rhinolophus cf. macrotis, suggests that Phia Oac is
an important area for bat conservation in Vietnam and thus more comprehensive studies need to be
performed.
... This species was regarded as one of the most common species of the genus in Indo-Malayan region with four assigned subspecies (Cobert and Hill 1992). In Indochina, two subspecies, Hipposideros larvatus alongensis and Hipposideros larvatus grandis, were elevated to species rank (Simmons 2005;Thong et al 2012), while H. larvatus sensu stricto is recently regarded as a cryptic species complex (Francis et al 2010). ...
Three short field surveys were conducted in the Phia Oac-Phia Den Nature Reserve to assess the species
diversity and endemism of local bat fauna. In combination with data from a previous study, 24 bat
species of 5 families, representing > 20% of the national bat diversity, were recorded in the study area.
The occurrence of several bat species restricted to montane forests, that is, Murina chrysochaetes,
Pipistrellus coromandra, and a potentially new species Rhinolophus cf. macrotis, suggests that Phia Oac is
an important area for bat conservation in Vietnam and thus more comprehensive studies need to be
performed.
... (Ruedi & Mayer, 2001), Hipposideros spp. (Douangboubpha et al., 2010;Rakotoarivelo, Willows-Munro, Schoeman, Lamb, & Goodman, 2015;Thong et al., 2012), and Rhinolophus spp. ...
... Bats were captured and handled in the field following the guidelines approved by the American Society of Mammalogists [11]. Fourbank harp traps [6] [19,20,21]. For taxonomic assessment, external measurements were taken in the field as follows: FA, forearm length: from the extremity of the elbow to the extremity of the carpus with the wings folded; EH, ear height: length of ear conch; TIB, tibia length: from the knee joint to the ankle; HF, hind-foot length: from the extremity of the heel behind the os calcis to the extremity of the longest digit, excluding the hairs or claws; Tail, tail length: from the tip of the tail to its base adjacent to the body. ...
Cat Tien National Park is a hotspot in Vietnam for biodiversity research and conservation. The park, with its extensive areas of primary forest, wetland habitats and large mammal populations, is known worldwide for its outstanding landscapes and biodiversity. Prior to 2007, several bat surveys were carried out in the park. However, data on the park’s bats is still limited and the status of previous records of a number of species is unclear. Between 2008 and 2015, the author conducted a series of bat surveys in the park with emphases on taxonomy and echolocation. Bats were captured using mist nets and four-bank harp traps. Echolocation calls were recorded from inside a flight tent and in natural habitats. Results from the surveys and a literature review indicated that Cat Tien National Park is currently known to be home to 47 bat species belonging to 22 genera and 7 families. Of these, 19 species belonging to 10 genera and 5 families were recorded during field surveys between 2008 and 2015. This paper provides the most recent review of bat species from Cat Tien National Park. Remarks on taxonomy and echolocation frequencies of species complexes are also given in order to assist further research, training, education, management and conservation.
... Cyt b gene was chosen to calculate TMRCA because of its moderate evolutionary rate. A mean substitution rate of 1.3% per million years (Nabholz, Glemin & Galtier, 2008), used in Hipposideros turpis complex (Thong et al., 2012), Hipposideros commersoni (Rakotoarivelo et al., 2015) and Myotis nattereri complex , was used in this analysis. ...
The greater horseshoe bat, Rhinolophus ferrumequinum, is an important model organism for studies on chiropteran phylogeographic patterns. Previous studies revealed the population history of R. ferrumequinum from Europe and most Asian regions, yet there continue to be arguments about their evolutionary process in Northeast Asia. In this study, we obtained mitochondrial DNA cyt b and D-loop data of R. ferrumequinum from Northeast China, South Korea and Japan to clarify their phylogenetic relationships and evolutionary process. Our results indicate a highly supported monophyletic group of Northeast Asian greater horseshoe bats, in which Japanese populations formed a single clade and clustered into the mixed branches of Northeast Chinese and South Korean populations. We infer that R. ferrumequinum in Northeast Asia originated in Northeast China and South Korea during a cold glacial period, while some ancestors likely arrived in Japan by flying or land bridge and subsequently adapted to the local environment. Consequently, during the warm Eemian interglaciation, the Korea Strait, between Japan and South Korea, became a geographical barrier to Japanese and inland populations, while the Changbai Mountains, between China and North Korea, did not play a significant role as a barrier between Northeast China and South Korea populations.
... Trees were collated using Tree Annotator 1.8 where Maximum clade credibility tree and Median heights were selected; and 10% (6,000 trees) sample trees were selected as burn in. To convert the estimates scaled by mutation rate to calendar years, we used the mean substitution rate of 1.30 × 10-8 subs/site/year which was previously used in hipposiderid bats (Thong et al., 2012; Lin et al., 2014). To calculate the genetic distance within and between clades, pairwise genetic distances (P-distance model) in MEGA 5.2.2 were computed. ...
Rhinolophus affinis sensu lato is a widespread bat species in South and Southeast Asia which shows considerable geographical variation in its morphology, echolocation call frequencies and genetics. The taxonomic status of the taxon in the Sundaic subregion remains uncertain however as the limited studies to date have been largely based on morphology. The aim of the present study was to determine the taxonomic status of subspecific forms recognized in the subregion and to evaluate phylogeographic distinctiveness between those occurring in Borneo and the Malay Peninsula using genetic, morphological and acoustic datasets. Two forms were confirmed: R. a. nesites from Borneo and R. a. superans from the peninsula. The previous recognition of a population from southernmost Sumatra as R. a. superans was not supported, however, as this form is likely R. a. affinis. Genetic divergence between these three forms is rather deep and is estimated to have occurred during the arid climatic period of the Pleistocene when suitable habitats were reduced to isolated pockets. Our results support the phylogeographic distinctiveness hypothesis as R. affinis sensu lato shows discrete affinities between Borneo and the Malay Peninsula. Discovery of new forms of R. affinis is likely with greater sampling effort throughout the region. Our study also demonstrates the importance of employing multiple datasets in taxonomic evaluations, as the use of morphological and/or acoustic datasets alone could lead to erroneous conclusions.
... Each captured bat was removed carefully from the trap or net and placed individually in a cotton bag. Their external measurements were taken following Bates & Harrison (1997) [ 1], Csorba et al. (2003) [ 6], Vu Dinh Thong (2011) [ 21] and Vu Dinh) [ 23, 24, 25]. The measurements comprise FA, forearm lengthfrom the extremity of the elbow to the extremity of the carpus with the wings folded; EH, ear height-length of ear conch; TIB, tibia lengthfrom the knee joint to the ankle; HF, hind-foot length-from the extremity of the heel behind the os calcis to the extremity of the longest digit, excluding the hairs or claws; Tail: tail length, from the tip of the tail to its base adjacent to the body. ...
Our survey in Mount Makiling Forest Reserve, Luzon Island, Philippines from April to May 2011 revealed new host records of bat fly species (Diptera: Nycteribiidae), including: Eucampsipoda philippinensis Ferris, Cyclopodia garrula Maa, C. horsfieldi de Mejeire, Phthiridium brachyacantha (Theodor) and Penicillidia acuminata Theodor. We also report C. garrula as a new record for Luzon Island. A checklist of the species known from the Philippines with the known distribution and bat host species was also provided.
... Moreover, the evolution of high-frequency echolocation in R. mehelyi can be also driven by female mate choice (Puechmaille et al., 2014). Together these findings indicate that the large shift in echolocation frequency may lead to barriers to intraspecific communication, and thus may lead to the 'harmonic hopping' (Kingston & Rossiter, 2004) or speciation (Thong et al., 2012). Finally, the allometric speciation hypothesis argues that the evolution of this species complex of horseshoe bats can also be attributed to divergence in echolocation frequency, which may originate from the allometric effect of adaptive divergence in skull size caused by paleoenvironmental changes (Taylor et al., 2012). ...
The evolution of acoustic signals and the morphological traits mediating its production and reception are often coupled. The echolocation call frequencies of horseshoe bats normally decline as body size increases, but remarkable exceptions to the rule have been observed, such as Rhinolophus macrotis, R. marshalli and R. rex, having lower echolocation call frequencies than expected for their body size. Forearm length is commonly used to scale allometric relationships across horseshoe bats. However, little is known about the allometric relationships between echolocation call frequencies and morphological traits mediating directly echolocation calls' production or reception, such as the nasal capsule, the cochlea or the pinna. Here we have tested the allometry hypothesis regarding the evolution of echolocation in 12 horseshoe bats distributed in China by integrating echolocation call frequencies, phylogeny, forearm length, cochlea size, pinna size and nasal capsule size. Our results showed no significant correlation between echolocation call frequency and forearm length across these species without considering the phylogeny of the group. However, ear length, ear width and nasal capsule size were significantly and negatively correlated with echolocation call frequencies among the studied species. The fit between the linear regression model and the data was much better for the relationships between echolocation call frequencies and pinna or nasal capsule size than for the relationship between echolocation call frequencies and forearm length. These findings illustrated that both pinna and nasal capsule size were better predictors of echolocation call frequencies than forearm length. Given that the echolocation call frequencies of horseshoe bats can play key roles in sexual selection and speciation, the divergence we observed among species may influence the evolution of echolocation calls across horseshoe bats in China.
... For echolocation, all species of Rhinolophus, and the sister genus Hipposideros, use a high duty cycle, long and narrow band, constant frequency (CF) com ponent, which is adapted for the detection of fluttering insects (Kalko and Schnitzler, 1998). Recent studies of the echolocation characters of the 'CF bats' strongly suggest that acoustic characters are useful for species identification (Francis and Haber setzer, 1998;Francis et al., 1999;Kingston et al., 2001;Thabah et al., 2006;Soisook et al., 2008;Hughes et al., 2010;Ith et al., 2011;Taylor et al., 2012;Thong et al., 2012). Moreover, acoustic divergence within species, which may result from the isolation of populations and adaptation due to local environment, can result in genetic drift and in some cases has led to speciation (Kingston and Rossiter, 2004;Chen et al., 2009;Taylor et al., 2012). ...
A new species of woolly horseshoe bat in the Rhinolophus trifoliatus species group is described from Sabah in Malaysian Borneo. Two specimens from Central and West Kalimantan, Indonesia are referred to this species. A fourth specimen from western Thailand is referable to this species but on the basis of ~10% genetic divergence at the cytochrome oxidase-I gene is described as a separate subspecies. Morphologically and acoustically the two subspecies are similar. With a forearm length of 52.90–54.70 mm, a skull length of 24.27–26.57 mm and a call frequency of 49.2–50.0 kHz, the new species overlaps in size and call frequency with the sympatric R. trifoliatus. However, it differs significantly in having a dark noseleaf and a uniformly dark brown pelage, resembling, but being intermediate in size between R. sedulus and R. luctus, which have a skull length of 18.99–20.17 and 26.35–32.07 mm, respectively. It also differs from R. trifoliatus in the shape and size of the rostral inflation. It can be distinguished from R. beddomei (forearm length 55.00–63.44 mm) and R. formosae (forearm length 53.85–62.40 mm), which are endemic to the Indian Subcontinent and Taiwan, respectively, by its relatively smaller body size. Acoustic and genetic data are included in the comparison between the species. Both character states support the conclusions based on morphology. Further surveys in intact evergreen forest together with a re-examination of museum specimens may reveal that this species is widespread in Southeast Asia.
... Reference source not found.]. Bats were captured and handled in the field following the guidelines approved by the American Society of Mammalogists [ 15] [ 21] and Vu Dinh [ 23,24,25]. The measurements comprise FA, forearm lengthfrom the extremity of the elbow to the extremity of the carpus with the wings folded; EH, ear height-length of ear conch; TIB, tibia lengthfrom the knee joint to the ankle; HF, hind-foot length-from the extremity of the heel behind the os calcis to the extremity of the longest digit, excluding the hairs or claws; Tail: tail length, from the tip of the tail to its base adjacent to the body. Reproductive status and age were assessed following Racey (2009) [ 14] and Brunet-Rossinni and Wilkinson (2009) [ 4], respectively. ...
Hipposiderids and rhinolophids are referred to all taxa of the two families Hipposideridae and Rhinolophidae, respectively. Their echolocation signals are diagnostic by a dominant “constant frequency” (CF) segment. Each echolocation signal of leaf-nosed bat species consists of two segments (“constant-frequency” and “terminal frequency-modulated”) while that of horseshoe bat species comprises three segments (“initial frequency-modulated”, “constant frequency” and “terminal frequency-modulated”). Between 2008 and 2014, a series of field surveys was conducted in Tam Dao National Park (TDNP) with particular emphases on taxonomy and echolocation of CF bat species. Results from the surveys indicated that TDNP is a home to three species of Hipposideridae (Hipposideros armiger, H. larvatus and H. pomona) and five species of Rhinolophidae (Rhinolophus affinis, R. luctus, R. macrotis, R. pearsonii and R. pusillus). During the present study, R. luctus was only detected in the field based on a poor echolocation call while all seven remaining species were captured. The CF of the second harmonic and morphological features of each species are clearly distinguished from the respective ones of the remaining species. This paper provides the external and acoustic diagnoses of each species for identification in the field to strengthen survey achievements, monitoring and conservation of CF bats in the park in coming time.
Background
Biodiversity surveys are essential for both academic research and conservation. Integrative approaches that combine morphological, genetic and acoustic aspects for species identification can provide reliable information in taxonomy and evolution. This is especially relevant for those groups with a high degree of cryptic diversity such as bats.
New information
Here, we present the results from a field survey carried out in the Cuc Phuong National Park (CPNP) during 2019 as part of the VIETBIO project and from the examination of specimen collections preserved at the museums of CPNP and the Institute of Ecology and Biological Resources (IEBR). In addition, we include an annotated species list, based on this survey and a literature review. We here confirm that CPNP is home to at least 47 bat species belonging to 23 genera and seven families. We recorded ten of these bat species during our field survey. Obtained data in genetics (sequencing a fragment of the mitochondrial gene COI) supported the morphological identification of the recorded species for which we were able to produce these data. In addition, we include echolocation recordings obtained during our field training with the hope that they may contribute valuable insights to future work concerning the surveyed species. Results from the field survey represent a relevant contribution to biodiversity assessment efforts and, thus, support conservation and management efforts to maintain bat diversity in Vietnam.
The horseshoe bats of the Rhinolophus ferrumequinum group form a well‐defined lineage within the Afro‐Palaearctic clade of the genus Rhinolophus . The group currently comprises four species widely distributed across the Palaearctic and Afrotropic regions: R. bocharicus (Central Asia), R. clivosus (from northern Africa and the Levant through Arabian Peninsula and eastern Africa to southern Africa), R. ferrumequinum (from western Europe and northern Africa through the Balkans and Middle East to Central Asia and India) and R. nippon (southern and central China, Korea, and Japan). The broad ranges and geographical variations within these species have led to the proposal of numerous subspecies. The phylogenetic relationships and intraspecific variation of the R. ferrumequinum group were investigated using a genetic approach. One mitochondrial marker and five nuclear markers were sequenced and supplemented with available sequences for all four species of the group. Our study revealed five major lineages within the R. ferrumequinum group, resulting in the recognition of four currently known species and identification of a new species. The prior name available for this lineage/species is R. acrotis . The relationships between the lineages varied depending on the chosen marker, leaving the interspecific relations within the ferrumequinum group unresolved. In addition, the results indicated that R. clivosus experienced historic introgression from northern Africa and the Levant, resulting in replacement of its mtDNA by that of R. ferrumequinum . Together, this study introduces a new Rhinolophus species, which increases the number of species in the ferrumequinum group to five.
The endangerment mechanisms of various species are a focus of studies on biodiversity and conservation biology. Hipposideros pomona is an endangered species, but the reasons behind its endangerment remain unclear. We investigated the endangerment mechanisms of H. pomona using mitochondrial DNA, nuclear DNA, and microsatellite loci markers. The results showed that the nucleotide diversity of mitochondria DNA and heterozygosity of microsatellite markers were high ( π = 0.04615, H O = 0.7115), whereas the nucleotide diversity of the nuclear genes was low ( THY : π = 0.00508, SORBS2 : π = 0.00677, ACOX2 : π = 0.00462, COPS7A : π = 0.00679). The phylogenetic tree and median‐joining network based on mitochondrial DNA sequences clustered the species into three clades, namely North Vietnam‐Fujian, Myanmar‐West Yunnan, and Laos‐Hainan clades. However, joint analysis of nuclear genes did not exhibit clustering. Analysis of molecular variance revealed a strong population genetic structure; IMa2 analysis did not reveal significant gene flow between all groups ( p > .05), and isolation‐by‐distance analysis revealed a significant positive correlation between genetic and geographic distances ( p < .05). The mismatch distribution analysis, neutral test, and Bayesian skyline plots revealed that the H. pomona population were relatively stable and exhibited a contraction trend. The results implied that H. pomona exhibits female philopatry and male‐biased dispersal. The Hengduan Mountains could have acted as a geographical barrier for gene flow between the North Vietnam‐Fujian clade and the Myanmar‐West Yunnan clade, whereas the Qiongzhou Strait may have limited interaction between the Hainan populations and other clades. The warm climate during the second interglacial Quaternary period ( c . 0.33 Mya) could have been responsible for species differentiation, whereas the cold climate during the late Quaternary last glacial maximum ( c . 10 ka BP) might have caused the overall contraction of species. The lack of significant gene flow in nuclear microsatellite loci markers among the different populations investigated reflects recent habitat fragmentation due to anthropogenic activities; thus, on‐site conservation of the species and restoration of gene flow corridors among populations need immediate implementation.
Initially, the Rhinolophus hipposideros group was defined by two morphological traits, the structure of the nose-leaf and the shape of basioccipital bone of the skull. Originally, it consisted of two species, R. hipposideros and R. midas, whereas currently it is considered to contain a single species, R. hipposideros, under whose rank both original species have been joined. The interpretation of geographic variability within the group has traditionally been based on variation in body and skull size, nose-leaf shape, and several selected skull and tooth characters. This approach resulted in delimitations of up to seven subspecies, mostly in the Mediterranean area, a conception introduced more than a hundred years ago and accepted by many authors till today. We investigated the phylogenetic relationships among populations of R. hipposideros with the help of molecular genetic, morphological, and acoustic examinations. Our analysis uncovered the existence of an unexpected diversity within the R. hipposideros group, challenging its current phylogenetic and taxonomic arrangements. The molecular genetic analysis of almost 100 samples and morphological examinations of about 300 specimens showed two main, geographically exclusive, phylogenetic lineages within the group, well delimited by molecular characteristics and possessing two distinct morphotypes and two distinct echotypes. These two lineages are isolated deep enough to be considered separate species. One of them, R. hipposideros s.str., is widespread over the south-western Eurasia and north-western and north-eastern Africa, and the other, R. midas, is distributed in a small range around the Strait of Hormuz and Gulf of Oman. The extensive range of R. hipposideros s.str. is inhabited at least by two subspecies, separated mainly by the genetic characters, whereas the morphological and echolocation traits do not distinguish the populations sufficiently. The western R. h. hipposideros occurs in the Maghreb and Europe west of the Dnieper River, Bosporus, and the Strait of Karpathos, and the eastern R. h. minimus lives east of this boundary, including the populations of Crimea, Caucasus, the Middle East, and north-eastern Africa (Sudan to Djibouti). The two subspecies also differ in karyotype, with 2n = 58 in R. h. minimus and 2n = 54–56 in R. h. hipposideros. The taxonomic position of the easternmost populations of R. hipposideros s.str. (West Turkestan, Afghanistan, Kashmir) remains unresolved and has to be investigated more elaborately and using a more extensive sample set.
Bats (Chiroptera) constitute the second largest order of mammals and have several distinctive features, such as true self-powered flight and strong immunity. The Pendlebury's roundleaf bat, Hipposideros pendleburyi, is endemic to Thailand and listed as a vulnerable species. We employed the 10× Genomics linked-read technology to obtain a genome assembly of H. pendleburyi. The assembly size was 2.17 Gb with a scaffold N50 length of 15,398,518 bases. Our phylogenetic analysis placed H. pendleburyi within the rhinolophoid clade of the suborder Yinpterochiroptera. A synteny analysis showed that H. pendleburyi shared conserved chromosome segments (up to 105 Mb) with Rhinolophus ferrumequinum and Phyllostomus discolor albeit having different chromosome numbers and belonging different families. We found positive selection signals in genes involved in inflammation, spermatogenesis and Wnt signalling. The analyses of transposable elements suggested the contraction of short interspersed nuclear elements (SINEs) and the accumulation of young mariner DNA transposons in the analysed hipposiderids. Distinct mariners were likely horizontally transferred to hipposiderid genomes over the evolution of this family. The lineage-specific profiles of SINEs and mariners might involve in the evolution of hipposiderids and be associated with the phylogenetic separations of these bats from other bat families.
Cat Ba National Park is the core zone of the Cat Ba Archipelago Biosphere Reserve. It contains quite diverse and unique ecosystems including 776 ha of mangrove forest. Although bats of the park were included in many publications, none were recorded from the mangrove ecosystem. We recently conducted field surveys through the wetland areas of the park and recorded three horseshoe bat species: Marshall's horseshoe bat (Rhinolophus marshalli), Pearson’s horseshoe bat (Rhinolophus pearsonii), and the least horseshoe bat (R. pusillus). Of these, R. pearsonii is the most common species. We here provide morpholocal and acoustic features of each species with notes on the importance of the mangrove forest in the park for bat research and conservation.
Historical forest contractions may have restricted the distributions of forest-utilizing fauna while providing opportunities for range expansions for open-habitat species. We aimed to test if habitat associations have played an important role in determining population genetic structure and demographic responses of six bats to oscillations in forest extent since the Last Glacial Maximum (LGM). We hypothesized that forest-associated species would display high levels of population structure and past population contractions as their distribution is dependent on fragmented forests. By contrast, habitat generalists would demonstrate low geographical structuring and historical population stability as suitable habitats are widely available. We used mitochondrial DNA to generate genetic diversity and population structure metrics of three forest-associated species and three habitat generalists in South Africa. Neutrality tests and Bayesian skyline plots were used to investigate demographic histories. A forest habitat association did not inform the population genetics of the study species. Rather, species-specific traits of roosting requirements, philopatry to the natal range and dispersal ability informed the observed structure. All species demonstrated population expansions during the Pleistocene, with no apparent decline during the LGM. It appears that the lower climate change footprint and refuge-status of eastern South Africa prevented population declines of insectivorous bats during the LGM.
The Old World leaf-nosed bats (Hipposideridae) are aerial and gleaning insectivores that occur throughout the Paleotropics. Both their taxonomic and phylogenetic histories are confused. Until recently, the family included genera now allocated to the Rhinonycteridae and was recognized as a subfamily of Rhinolophidae. Evidence that Hipposideridae diverged from both Rhinolophidae and Rhinonycteridae in the Eocene confirmed their family rank, but their intrafamilial relationships remain poorly resolved. We examined genetic variation in the Afrotropical hipposiderids Doryrhina , Hipposideros , and Macronycteris using relatively dense taxon-sampling throughout East Africa and neighboring regions. Variation in both mitochondrial (cyt-b) and four nuclear intron sequences (ACOX2, COPS, ROGDI, STAT5) were analyzed using both maximum likelihood and Bayesian inference methods. We used intron sequences and the lineage delimitation method BPP—a multilocus, multi-species coalescent approach—on supported mitochondrial clades to identify those acting as independent evolutionary lineages. The program StarBEAST was used on the intron sequences to produce a species tree of the sampled Afrotropical hipposiderids. All genetic analyses strongly support generic monophyly, with Doryrhina and Macronycteris as Afrotropical sister genera distinct from a Paleotropical Hipposideros ; mitochondrial analyses interpose the genera Aselliscus , Coelops , and Asellia between these clades. Mitochondrial analyses also suggest at least two separate colonizations of Africa by Asian groups of Hipposideros , but the actual number and direction of faunal interchanges will hinge on placement of the unsampled African-Arabian species H. megalotis . Mitochondrial sequences further identify a large number of geographically structured clades within species of all three genera. However, in sharp contrast to this pattern, the four nuclear introns fail to distinguish many of these groups and their geographic structuring disappears. Various distinctive mitochondrial clades are consolidated in the intron-based gene trees and delimitation analyses, calling into question their evolutionary independence or else indicating their very recent divergence. At the same time, there is now compelling genetic evidence in both mitochondrial and nuclear sequences for several additional unnamed species among the Afrotropical Hipposideros . Conflicting appraisals of differentiation among the Afrotropical hipposiderids based on mitochondrial and nuclear loci must be adjudicated by large-scale integrative analyses of echolocation calls, quantitative morphology, and geometric morphometrics. Integrative analyses will also help to resolve the challenging taxonomic issues posed by the diversification of the many lineages associated with H. caffer and H. ruber .
Noninvasive genetic methods and genomics have been able to provide important insights into the distribution, ecology, and evolution of the snow leopard. Scat sampling has yielded quantitative population size estimates using surveys that can be implemented over areas larger than can be done with more traditional methods. Scat has also been used to better understand the diet of this species. It has been found that in many regions snow leopards frequently consume livestock. New molecular markers enable studies to understand the spatial and temporal variation in depredation and to evaluate conservation actions that seek to reduce it. Scats also represent important population samples that have been used to provide insights into the phylogeography and population structure of the snow leopard. Patterns in genetic variation indicate several barriers leading to three primary clusters, while also identifying broader regions where landscape connectivity maintains metapopulations. Next-generation sequencing of 5 snow leopard whole genomes identified 257,780 SNPs that can be genotyped to acquire finer resolution of structure and understand genomic differences. Genome-wide analysis has enabled a closer examination of the two candidate genes, EGLN1 and EPAS1, which likely play an important role in the high-altitude adaptation of snow leopards by modulating the cellular response to hypoxia. There is additional evidence that one target gene, VEGFA, has higher expression in snow leopard lung compared to tiger, potentially leading to improved ventilation. More in-depth studies are needed to generate rigorous population estimates, understand factors that drive livestock depredation, identify the important corridors for connectivity, and elucidate the high-altitude physiological adaptations of this species. The resulting information will contribute to designing effective conservation and management initiatives that ensure long-term stability of snow leopards throughout their range.
Macronycteris commersoni (Hipposideridae), a bat species endemic to Madagascar, is widespread across the island and utilizes a range of habitat types including open woodland, degraded habitats, and forested areas from sea level to 1,325 m. Despite being widely distributed, there is evidence that M. commersoni exhibits morphological and bioacoustic variation across its geographical range. We investigated the fine-scale phylogeographic structure of populations in the western half of the island using extensive spatial sampling and sequence data from two mitochondrial DNA regions. Our results indicated several lineages within M. commersoni. Individuals collected from northern Madagascar formed a single monophyletic clade (clade C). A second clade (clade B) included individuals collected from the southwestern portion of the island. This second clade displayed more phylogeographical partitioning with differences in mtDNA haplotypes frequency detected between populations collected in different bioclimatic regions. Lineage dispersal, genetic divergence, and timing of expansion events of M. commersoni were probably associated with Pleistocene climate fluctuations. Our data suggest that the northern and the central western regions of Madagascar may have acted as refugia for this species during periods of cooler and drier climate conditions associated with the Pleistocene.
Populations of the Malagasy Hipposideros commersoni (family Hipposideridae) are threatened by deforestation andhunting. Maximum likelihood and Bayesian analysis of 148 cytochrome b sequences found this species to be paraphyletic and composed of three well-supported monophyletic clades. Clades B and C form a monophyletic lineage that can be referred to H. commersoni; these two clades are separated by 6% sequence variation. Clade A represents a distinct evolutionary lineage separate (9–11% average sequence divergence) from H. commersoni (clades B and C) and is named herein as a new species, Hipposideros cryptovalorona sp. nov. In the phylogeny presented herein, this species is strongly associated with the outgroup taxa Hipposideros gigas and Hipposideros vittatus, both restricted
to Africa. External, cranial and dental measurements taken from the same individuals used in the molecular study indicate no clear distinction in morphology amongst these three clades; this includes noseleaf structure and craniodental characteristics. Principal component analyses showed limited separation of the three clades. Comparison to a Quaternary fossil species from north-west Madagascar, Hipposideros besaoka, found little morphological overlap between any of the three clades and this extinct species. Hence, at least three species of Hipposideros have occurred on Madagascar since the Late Pleistocene, two extant (H. commersoni s.s. and H. cryptovalorona sp. nov.) and one extinct (H. besaoka).
Background
The Commerson’s leaf-nosed bat, Hipposideros commersoni sensu stricto, is endemic to Madagascar and is relatively common in the western portion of the island, where it is found in areas, including forested zones, from sea level to 1325 m. A previous study on morphological patterns of geographic variation within the species highlighted the presence of two distinct morphotypes; larger individuals in the north portion of the island and smaller individuals in the south. The main aim of this study was to use a combination of craniodental morphology and molecular data (mitochondrial and nuclear) to test previous hypotheses based on morphology and clarify the evolutionary history of the species group.
Methods
We sequenced mitochondrial and nuclear genes from Hipposideros commersoni obtained from the western portion of Madagascar, and compared them with other African species as outgroups. We analyzed the sequence data using Maximum Likelihood and Bayesian phylogenetic inference. Divergence dates were estimated using Bayesian molecular clock approach. Variation in craniodental variables was also assessed from sequenced individuals.
Results
The molecular analyses suggest that H. commersoni is not monophyletic, with strong support for the presence of several independently evolving lineages. Two individuals amongst those sequenced from Isalo (south central) and Itampolo (southwest) form a separate clade (Clade A), distinct from other H. commersoni , and sister to continental African H. vittatus and H. gigas. Within the H. commersoni clade, the molecular data support two geographically distributed clades; one from the south (Clade B) and the other from the north (Clade C), which diverged approximately 3.38 million years ago. Morphometric data were consistent with the molecular analyses, suggesting a north–south break within H. commersoni . However, at some localities, animals from both clades occurred in sympatry and these individuals could not be differentiated based on external and craniodental measurements.
Conclusions
Using a combination of molecular and morphological characters, this study presents evidence of cryptic diversity in H. commersoni on Madagascar. Further fine-scale phylogeographic studies are needed to fully resolve the systematics of H. commersoni . This study highlights the utility of the combined approach in employing both morphological and molecular data to provide insights into the evolutionary history of Malagasy population currently assigned to H. commersoni .
Previous studies conducted on morphological variation of the endemic Malagasy bat Hipposideros commersoni sensu stricto (Hipposideridae) revealed a north-south morphological cline, with larger individuals present in the north. Little is known about potential sexual differences in the echolocation calls of this species. We captured 59 adult individuals (24 males and 35 females) at different sites spanning the western half of Madagascar, measured their forearm length and recorded echolocation calls. These data were used to examine possible variation in echolocation calls and body size, which showed statistically significant differences. Male H. commersoni have an average forearm length of 93.1 mm and emit calls at 68.6 kHz, while the average measurements for females are 83.9 mm and about 72.9 kHz, respectively. Principal component analysis revealed variation in morphological and bioacoustic parameters, suggesting a high intraspecific variation. Regression analysis of intersexual data showed that females from the far north (Ankarana) significantly deviate from the allometric relationship by emitting echolocation calls lower than predicted by their size. These divergences may be associated with phenotypic variation, migratory movements or presence of a possible cryptic species. Detailed phylogenetic and phylogeographical analyses of the H. commersoni complex are needed to address these questions.
The phylogenetic and taxonomic relationships among the Old World leaf-nosed bats (Hipposideridae) and the closely related horseshoe bats (Rhinolophidae) remain unresolved. In this study, we generated a novel approximately 10-kb molecular data set of 19 nuclear exon and intron gene fragments for 40 bat species to elucidate the phylogenetic relationships within the families Rhinolophidae and Hipposideridae. We estimated divergence times and explored potential reasons for any incongruent phylogenetic signal. We demonstrated the effects of outlier taxa and genes on phylogenetic reconstructions and compared the relative performance of intron and exon data to resolve phylogenetic relationships. Phylogenetic analyses produced a well-resolved phylogeny, supporting the familial status of Hipposideridae and demonstrated the paraphyly of the largest genus, Hipposideros. A fossil-calibrated timetree and biogeographical analyses estimated that Rhinolophidae and Hipposideridae diverged in Africa during the Eocene approximately 42 Ma. The phylogram, the timetree, and a unique retrotransposon insertion supported the elevation of the subtribe Rhinonycterina to family level and which is diagnosed herein. Comparative analysis of diversification rates showed that the speciose genera Rhinolophus and Hipposideros underwent diversification during the Mid-Miocene Climatic Optimum. The intron versus exon analyses demonstrated the improved nodal support provided by introns for our optimal tree, an important finding for large-scale phylogenomic studies, which typically rely on exon data alone. With the recent outbreak of Middle East respiratory syndrome, caused by a novel coronavirus, the study of these species is urgent as they are considered the natural reservoir for emergent severe acute respiratory syndrome (SARS)-like coronaviruses. It has been shown that host phylogeny is the primary factor that determines a virus's persistence, replicative ability, and can act as a predictor of new emerging disease. Therefore, this newly resolved phylogeny can be used to direct future assessments of viral diversity and to elucidate the origin and development of SARS-like coronaviruses in mammals.
In this study we explored quantitatively the relationships between the size of bats, the frequencies in their echolocation calls, and the incidence of moths and beetles in their diets. We focused on the predictions of the allotonic frequency hypothesis which states that some insectivorous bats increase their access to moths that can hear echolocation calls by shifting to frequencies to which the ears of these insects are less sensitive. The hypothesis predicts that the frequencies dominating the echolocation calls of bats may be correlated with the incidence of moths in their diets. We collected data for 62 species of bats that take airborne prey, usually flying insects, 25 species of high duty cycle echolocating bats (Rhinolophidae and Hipposideridae) and 37 species that are low duty cycle echolocators (Vespertilionidae and Molossidae). For bats whose echolocation calls are dominated by frequencies < 100 kHz our regression analyses showed a parabolic dependency between moth consumption (% volume or % frequency) and echolocation call frequency (kHz), supporting the allotonic frequency hypothesis. The use of echolocation calls dominated by frequencies outside the range of best hearing by moths may indeed increase the availability of these insects to the bats. However, when the same analysis was performed with only the bat species using echolocation calls dominated by sounds > 100 kHz, the relationship was not statistically significant, suggesting that morphological characteristics rather than echolocation call frequency may limit the range of potential prey items. Our analyses also demonstrate the importance of jaw morphology as a predictor of the incidence of beetles or moths in the diets of bats, and reveal that generally bigger species (as defined by forearm length) use echolocation calls dominated by lower frequencies than smaller species. In both high duty and low duty cycle echolocating bats the relationship between body size and dominant call frequency was best described by a linear model. We also propose that perch hunting was central in the development of the high duty cycle approach to echolocation.
Efforts for the conservation of the endangered bat species Hipposideros turpis turpis in southern Japan are hampered by a lack of information about its biology and natural history and by the increasing effect of human activities. In an attempt to address some of the conservation challenges faced by this species, we studied the genetic structure and dispersal of intra- and interisland populations using six species-specific microsatellite markers. In particular, we sought to establish the relationship between island populations and to define effective management units for conservation. Pairwise co-ancestry index (F
ST) analysis, analysis of molecular variance, and Bayesian clustering suggested the presence of significant genetic differentiation between islands but little differentiation within them. The small Yonaguni Island population appeared to be not only geographically isolated, but also genetically isolated. This population is at the greatest risk of extinction, considering its size and low genetic variation. The larger populations on Iriomote and Ishigaki Islands are genetically related to each other to a greater degree and exhibit higher genetic variation than the Yonaguni Island population. This suggests that these two island populations should be included in a single management unit, while bats from Yonaguni Island should be managed independently and given higher priority for conservation. Actions such as defining vegetation corridors between colonies, as well as building gates at the entrance of the largest known colony, should be included in the conservation agenda of this still poorly known species.
In the Constant Frequency portions of the orientation calls of various Rhinolophus and Hipposideros species, the frequency with the strongest amplitude was studied comparatively. (1) In the five European species of the genus Rhinolophus call frequencies are either species-specific (R. ferrumequinum, R. blasii and R. euryale) or they overlap (R. hipposideros and R. mehelyi). The call frequency distributions are approximately 5–9 kHz wide, thus their ranges spead less than 5% from the mean (Fig. 1). Frequency distributions are considerably narrower within smaller geographic areas. (2) As in other bat groups, call frequencies of the Rhinolophoidea are negatively correlated with body size (Fig. 3). Regression lines for the genera Rhinolophus and Rhinolophus, species from dryer climates have on the average higher call frequencies than species from tropical rain forests. (4) The Krau Game Reserve, a still largely intact rain forest area in Malaysia, harbours at least 12 syntopic Rhinolophus and Hipposiderso species. Their call frequencies lie between 40 and 200 kHz (Fig. 2). Distribution over the available frequency range is significantly more even than could be expected from chance alone. Two different null hypotheses to test for random character distribution were derived from frequency-size-relations and by sampling species assemblages from a species pool (Monte Carlo method); both were rejected. In particular, call frequencies lying close together are avoided (Figs. 4, 5). Conversely, the distribution of size ratios complied with a corresponding null hypothesis. This even distribution may be a consequence of resource partitioning with respect to prey type. Alternatively, the importance of these calls as social signals (e.g. recognition of conspecifics) might have necessitated a communication channel partitioning.
A new species of Hipposideros is described from Vietnam. Morphologically, it is similar to taxa in the Hipposideros armiger complex but is substantially smaller. The new species, which has been found living sympatrically with H. armiger in Cat Ba National Park, is distinguished from it by size, acoustic characters, and differences in the mitochondrial DNA. Currently, the new taxon is known from Cat Ba Island in Ha Long Bay in northern Vietnam and from Chu Mom Ray National Park, which is situated on the mainland some 1,000 km to the south. It was collected in disturbed and primary forests.
The sensory drive theory of speciation predicts that populations of the same species inhabiting different environments can differ in sensory traits, and that this sensory difference can ultimately drive speciation. However, even in the best-known examples of sensory ecology driven speciation, it is uncertain whether the variation in sensory traits is the cause or the consequence of a reduction in levels of gene flow. Here we show strong genetic differentiation, no gene flow and large echolocation differences between the allopatric Myanmar and Thai populations of the world's smallest mammal, Craseonycteris thonglongyai, and suggest that geographic isolation most likely preceded sensory divergence. Within the geographically continuous Thai population, we show that geographic distance has a primary role in limiting gene flow rather than echolocation divergence. In line with sensory-driven speciation models, we suggest that in C. thonglongyai, limited gene flow creates the suitable conditions that favour the evolution of sensory divergence via local adaptation.
Mitochondrial DNA (mtDNA) is the most popular marker of molecular diversity in animals, primarily because of its elevated mutation rate. After .20 years of intensive usage, the extent of mitochondrial evolutionary rate variations across species, their practical consequences on sequence analysis methods, and the ultimate reasons for mtDNA hypermutability are still largely unresolved issues. Using an extensive cytochrome b data set, fossil data, and taking advantage of the decoupled dynamics of synonymous and nonsynonymous substitutions, we measure the lineage-specific mitochondrial mutation rate across 1,696 mammalian species and compare it with the nuclear rate. We report an unexpected 2 orders of magnitude mitochondrial mutation rate variation between lineages: cytochrome b third codon positions are renewed every 1–2 Myr, in average, in the fastest evolving mammals, whereas it takes .100 Myr in slow-evolving lineages. This result has obvious implications in the fields of molecular phylogeny, molecular dating, and population genetics. Variations of mitochondrial substitution rate across species are partly explained by body mass, longevity, and age of female sexual maturity. The classical metabolic rate and generation time hypothesis, however, do not fully explain the observed patterns, especially a stronger effect of longevity in long-lived than in short-lived species. We propose that natural selection tends to decrease the mitochondrial mutation rate in long-lived species, in agreement with the mitochondrial theory of aging.
The program MODELTEST uses log likelihood scores to establish the model of DNA evolution that best fits the data.
AVAILABILITY: The MODELTEST package, including the source code and some documentation is available at http://bioag.byu. edu/zoology/crandall_lab/modeltest.html.
I investigated the scaling of echolocation call parameters (frequency, duration and repetition rate) in bats in a functional context. Low-duty-cycle bats operate with search phase cycles of usually less than 20 %. They process echoes in the time domain and are therefore intolerant of pulse-echo overlap. High-duty-cycle (>30 %) species use Doppler shift compensation, and they separate pulse and echo in the frequency domain. Call frequency scales negatively with body mass in at least five bat families. Pulse duration scales positively with mass in low-duty-cycle quasi-constant-frequency (QCF) species because the large aerial-hawking species that emit these signals fly fast in open habitats. They therefore detect distant targets and experience pulse-echo overlap later than do smaller bats. Pulse duration also scales positively with mass in the Hipposideridae, which show at least partial Doppler shift compensation. Pulse repetition rate corresponds closely with wingbeat frequency in QCF bat species that fly relatively slowly. Larger, fast-flying species often skip pulses when detecting distant targets. There is probably a trade-off between call intensity and repetition rate because 'whispering' bats (and hipposiderids) produce several calls per predicted wingbeat and because batches of calls are emitted per wingbeat during terminal buzzes. Severe atmospheric attenuation at high frequencies limits the range of high-frequency calls. Low-duty-cycle bats that call at high frequencies must therefore use short pulses to avoid pulse-echo overlap. Rhinolophids escape this constraint by Doppler shift compensation and, importantly, can exploit advantages associated with the emission of both high-frequency and long-duration calls. Low frequencies are unsuited for the detection of small prey, and low repetition rates may limit prey detection rates. Echolocation parameters may therefore constrain maximum body size in aerial-hawking bats.
We announce the release of the fourth version of MEGA software, which expands on the existing facilities for editing DNA sequence data from autosequencers, mining Web-databases, performing automatic and manual sequence alignment, analyzing sequence alignments to estimate evolutionary distances, inferring phylogenetic trees, and testing evolutionary hypotheses. Version 4 includes a unique facility to generate captions, written in figure legend format, in order to provide natural language descriptions of the models and methods used in the analyses. This facility aims to promote a better understanding of the underlying assumptions used in analyses, and of the results generated. Another new feature is the Maximum Composite Likelihood (MCL) method for estimating evolutionary distances between all pairs of sequences simultaneously, with and without incorporating rate variation among sites and substitution pattern heterogeneities among lineages. This MCL method also can be used to estimate transition/transversion bias and nucleotide substitution pattern without knowledge of the phylogenetic tree. This new version is a native 32-bit Windows application with multi-threading and multi-user supports, and it is also available to run in a Linux desktop environment (via the Wine compatibility layer) and on Intel-based Macintosh computers under the Parallels program. The current version of MEGA is available free of charge at (http://www.megasoftware.net).
The evolutionary analysis of molecular sequence variation is a statistical enterprise. This is reflected in the increased use of probabilistic models for phylogenetic inference, multiple sequence alignment, and molecular population genetics. Here we present BEAST: a fast, flexible software architecture for Bayesian analysis of molecular sequences related by an evolutionary tree. A large number of popular stochastic models of sequence evolution are provided and tree-based models suitable for both within- and between-species sequence data are implemented.
BEAST version 1.4.6 consists of 81000 lines of Java source code, 779 classes and 81 packages. It provides models for DNA and protein sequence evolution, highly parametric coalescent analysis, relaxed clock phylogenetics, non-contemporaneous sequence data, statistical alignment and a wide range of options for prior distributions. BEAST source code is object-oriented, modular in design and freely available at http://beast-mcmc.googlecode.com/ under the GNU LGPL license.
BEAST is a powerful and flexible evolutionary analysis package for molecular sequence variation. It also provides a resource for the further development of new models and statistical methods of evolutionary analysis.
Mitochondrial DNA (mtDNA) is the most popular marker of molecular diversity in animals, primarily because of its elevated mutation rate. After >20 years of intensive usage, the extent of mitochondrial evolutionary rate variations across species, their practical consequences on sequence analysis methods, and the ultimate reasons for mtDNA hypermutability are still largely unresolved issues. Using an extensive cytochrome b data set, fossil data, and taking advantage of the decoupled dynamics of synonymous and nonsynonymous substitutions, we measure the lineage-specific mitochondrial mutation rate across 1,696 mammalian species and compare it with the nuclear rate. We report an unexpected 2 orders of magnitude mitochondrial mutation rate variation between lineages: cytochrome b third codon positions are renewed every 1-2 Myr, in average, in the fastest evolving mammals, whereas it takes >100 Myr in slow-evolving lineages. This result has obvious implications in the fields of molecular phylogeny, molecular dating, and population genetics. Variations of mitochondrial substitution rate across species are partly explained by body mass, longevity, and age of female sexual maturity. The classical metabolic rate and generation time hypothesis, however, do not fully explain the observed patterns, especially a stronger effect of longevity in long-lived than in short-lived species. We propose that natural selection tends to decrease the mitochondrial mutation rate in long-lived species, in agreement with the mitochondrial theory of aging.
Despite hundreds of reports involving both plants and animals, the mechanisms underlying introgression remain obscure, even if some form of selection is frequently invoked. Introgression has repeatedly been reported in species that have recently colonized a new habitat, suggesting that demographic processes should be given more attention for understanding the mechanisms of introgression. Here we show by spatially explicit simulations that massive introgression of neutral genes takes place during the invasion of an occupied territory if interbreeding is not severely prevented between the invading and the local species. We also demonstrate that introgression occurs almost exclusively from the local to the invading species, especially for populations located far away from the source of the invasion, and this irrespective of the relative densities of the two species. This pattern is strongest at markers experiencing reduced gene flow, in keeping with the observation that organelle genes are often preferentially introgressed across species boundaries. A survey of the literature shows that a majority of published empirical studies of introgression during range expansions, in animals and in plants, follow the predictions of our model. Our results imply that speciation genes can be identified by comparing genomes of interfertile native and invading species pairs.
Since the Frascati meeting in 1966, there has been considerable expansion in our understanding of the acoustic structures used by bats and birds for echolocation in air. In part this has been due to the development of instrumental techniques which were already undergoing something of a revolution at the time. Highspeed tape-recorders suitable for bat recording had only become available a few years previously and their use in conjunction with Sonagraph sound spectrum analysers was then becoming widespread. This combination was rapidly replacing the analysis of waveforms by photographic sampling in real time from an oscilloscope screen which, due to complex phase changes, is open to ambiguous interpretation of harmonics or frequency changes.
We investigate the contribution of the Iberian bat fauna to the cryptic diversity in Europe using mitochondrial (cytb and ND1) and nuclear (RAG2) DNA sequences. For each of the 28 bat species known for Iberia, samples covering a wide geographic range within Spain were compared to samples from the rest of Europe. In this general screening, almost 20% of the Iberian species showed important mitochondrial discontinuities (K2P distance values > 5%) either within the Iberian or between Iberian and other European samples. Within Eptesicus serotinus and Myotis nattereri, levels of genetic divergence between lineages exceeded 16%, indicating that these taxa represent a complex of several biological species. Other well-differentiated lineages (K2P distances between 5–10%) appeared within Hypsugo savii, Pipistrellus kuhlii and Plecotus auritus, suggesting the existence of further cryptic diversity. Most unsuspected lineages seem restricted to Iberia, although two have crossed the Pyrenees to reach, at leas...
This is a reference book about wild mammals in Japan, including both terrestrial and marine species.
(Because this is a "book", I cannot send a copy of this if requested.)
The Bang's leaf-nose bat, Hipposideros turpis, is an endangered cave-dwelling species inhabiting the southwesternmost islands of Japan. We isolated six dinucleotide microsatellite markers from the partial genomic library of the bat, and examined their allelic variation using a sample (N = 33) from the largest colony in Japan. All the loci showed a moderate allelic variation ranging from two to eight alleles, with the observed heterozygosities from 0.33 to 0.73, and conformed to Hardy–Weinberg expectations. The present microsatellite markers will be useful in assessing population genetic structure and gene flow among populations of this species.
The importance and abundance of cryptic species among invertebrate taxa is well documented. Nowadays, taxonomic, phylogenetic and conservation biological studies frequently use molecular markers to delineate cryptic taxa. Such studies, however, often face the problem of the differential resolution of the molecular markers and techniques involved. This issue is explored in the present study of cryptic taxa within the terrestrial slug complex Arion subfuscus/fuscus in continental north-west Europe. To this end, morphological, allozyme and mitochondrial 16S rDNA sequence data have been jointly evaluated. Using allozyme data and gonad type, two distinct groups were consistently delineated, even under sympatric conditions. The 16S rDNA data strongly supported both those groups and even suggested the presence of three distinct taxa within one of them. However, in view of: (1) the allopatric distribution of three OTUs, (2) the lack of allozyme or morphological differentiation, and (3) the extremely high degree of intraspecific mtDNA variation reported in pulmonate gastropods, they are, for the time being, not regarded as valid species under the biological species concept. By means of 16S rDNA and allozyme data, the position of type and topotype material of A. subfuscus s.s. and A. fuscus relative to the newly defined OTUs was determined, thus clarifying the nomenclature of this species complex. Additionally, gonad type proved to be a useful character for distinguishing the two species in north-west Europe. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 83, 23–38.
The population size, distribution, threats and conservation status of 2 bat species included as 'endangered' in the IUCN Red List were assessed in Thailand and Myanmar. Craseonyc- teris thonglongyai Hill, 1974 and Hipposideros turpis Bangs, 1901 are both rare and poorly known cave-dwelling species, which have restricted distributions and small population sizes. Surveys of the 2 species were conducted in a large number of locations including previously reported sites and potential new locations. Colony size was counted at currently known localities, and population size was estimated. The known distribution and population are larger than in previous estimates, but both species still remain threatened by roost disturbance and the destruction of foraging habitat. Clarifi- cation of the taxonomic status of allopatric populations within each species is urgently required.
Based on recent field surveys in Thailand, Myanmar, and northern peninsular Malaysia, this paper reviews the taxonomy, morphometric and acoustic characters, distribution and ecology of the little known, globally endangered species Hipposideros halophyllus. It lists nine new localities records, including the first from northern and peninsular Thailand, which represent a substantial increase in the species' known range; it confirms the record from northern peninsular Malaysia. In addition, it provides further information on two other small species of the Hipposideros bicolor group, H. ater and H. cineraceus.
In this article we discuss our experience designing and implementing a statistical computing language. In developing this new language, we sought to combine what we felt were useful features from two existing computer languages. We feel that the new language provides advantages in the areas of portability, computational efficiency, memory management, and scoping.
Rhythmical modulations in insect echoes caused by the moving wings of fluttering insects are behaviourally relevant information for bats emitting CF-FM signals with a high duty cycle. Transmitter and receiver of the echolocation system in flutter detecting foragers are especially adapted for the processing of flutter information. The adaptations of the transmitter are indicated by a flutter induced increase in duty cycle, and by Doppler shift compensation (DSC) that keeps the carrier frequency of the insect echoes near a reference frequency. An adaptation of the receiver is the auditory fovea on the basilar membrane, a highly expanded frequency representation centred to the reference frequency. The afferent projections from the fovea lead to foveal areas with an overrepresentation of sharply tuned neurons with best frequencies near the reference frequency throughout the entire auditory pathway. These foveal neurons are very sensitive to stimuli with natural and simulated flutter information. The frequency range of the foveal areas with their flutter processing neurons overlaps exactly with the frequency range where DS compensating bats most likely receive echoes from fluttering insects. This tight match indicates that auditory fovea and DSC are adaptations for the detection and evaluation of insects flying in clutter.
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Some simple formulae were obtained which enable us to estimate evolutionary distances in terms of the number of nucleotide substitutions (and, also, the evolutionary rates when the divergence times are known). In comparing a pair of nucleotide sequences, we distinguish two types of differences; if homologous sites are occupied by different nucleotide bases but both are purines or both pyrimidines, the difference is called type I (or "transition" type), while, if one of the two is a purine and the other is a pyrimidine, the difference is called type II (or "transversion" type). Letting P and Q be respectively the fractions of nucleotide sites showing type I and type II differences between two sequences compared, then the evolutionary distance per site is K = -(1/2) ln [(1-2P-Q) square root of 1-2Q]. The evolutionary rate per year is then given by k = K/(2T), where T is the time since the divergence of the two sequences. If only the third codon positions are compared, the synonymous component of the evolutionary base substitutions per site is estimated by K'S = -(1/2) ln (1-2P-Q). Also, formulae for standard errors were obtained. Some examples were worked out using reported globin sequences to show that synonymous substitutions occur at much higher rates than amino acid-altering substitutions in evolution.
Precise comparisons of mammalian gene maps require common anchor loci as landmarks for conserved chromosomal segments. Using a computer script that automates DNA sequence database alignments, we designed 410 evolutionarily conserved primer pair sequences which are specific for anchor locus gene amplification from any mammalian species' DNA. Primer pairs were designed to span introns for polymorphism ascertainment, and to include sufficient exonic sequence (25-400 bp) to allow for gene identification. A total of 318 primer pairs were optimized for domestic cats, and 86% of the sequenced feline PCR products showed homology to the gene of primer origin. A screen of 20 mammals from 11 orders revealed that 35-52% of the 318 primers yielded a single PCR product without further optimization suggesting that nearly 75% can be optimized for any eutherian mammal.
Based on extensive phenetic analyses, bats of the genus Myotis have been classically subdivided into four major subgenera each of which comprise many species with similar morphological and ecological adaptations. Each subgenus thus corresponds to a distinct "ecomorph" encompassing bat species exploiting their environment in a similar fashion. As three of these subgenera are cosmopolitan, regional species assemblages of Myotis usually include sympatric representatives of each ecomorph. If species within these ecomorphs are monophyletic, such assemblages would suggest extensive secondary dispersal across geographic areas. Conversely, these ecomorphological adaptations may have evolved independently through deterministic processes, such as adaptive radiation. In this case, phylogenetic reconstructions are not expected to sort species of the same ecomorph into monophyletic clades. To test these predictions, we reconstructed the phylogenetic history of 13 American, 11 Palaearctic, and 6 other Myotis species, using sequence data obtained from nearly 2 kb of mitochondrial genes (cytochrome b and nd1). Separate or combined analyses of these sequences clearly demonstrate the existence of several pairs of morphologically very similar species (i.e., sibling species) which are phylogenetically not closely related. None of the three tested subgenera constitute monophyletic units. For instance, Nearctic and Neotropical species currently classified into the three subgenera were clustered in a single, well-supported monophyletic clade. These species thus evolved independently of their ecological equivalents from the Palaearctic region. Independent adaptive radiations among species of the genus Myotis therefore produced strikingly similar evolutionary solutions in different parts of the world. Furthermore, all phylogenetic reconstructions based on mtDNA strongly supported the existence of an unsuspected monophyletic clade which included all assayed New World species plus M. brandtii (from the Palaearctic Region). This "American" clade thus radiated into a morphologically diverse species assemblage which evolved after the first Myotis species colonized the Americas. Molecular reconstructions support paleontological evidence that species of the genus Myotis had a burst of diversification during the late Miocene-early Pliocene epoch.
Recent studies have shown that species in the genus Myotis have evolved a number of convergent morphological traits, many of which are more related to their mode of food procurement than to their phylogeny. Surprisingly, the biogeographic origins of these species are a much better predictor of phylogenetic relationships, than their morphology. In particular, a monophyletic clade that includes all New World species was apparent, but only a third of the 38 species have been analysed. In order to better understand the evolution of this clade, we present phylogenetic reconstructions of 17 Nearctic and 13 Neotropical species of Myotis compared to a number of Old World congeners. These reconstructions are based on mitochondrial cytochrome b (1140 bp), and nuclear Rag 2 genes (1148 bp). Monophyly of the New World clade is strongly supported in all analyses. Two Palaearctic sister species, one from the west (M. brandtii) and one from the east (M. gracilis), are embedded within the New World clade, suggesting that they either moved across the Bering Strait, or that they descended from the same ancestor that reached the New World. An emerging feature of these phylogenetic reconstructions is that limited faunal exchanges have occurred, including between the North and South American continents, further emphasizing the importance of biogeography in the radiation of Myotis. A fossil-calibrated, relaxed molecular-clock model was used to estimate the divergence time of New World lineages to 12.2+/-2.0 MYA. Early diversification of New World Myotis coincides with the sharp global cooling of the Middle Miocene. Radiation of the temperate-adapted Myotis may have been triggered by these climatic changes. The relative paucity of species currently found in South America might result from a combination of factors including the early presence of competitors better adapted to tropical habitats.
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