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Evolutionary relationships and population genetics of the Afrotropical leaf-nosed bats (, )
DOI 10.3897/zookeys.929.50240, Volume: 929,
Abstract

The Old World leaf-nosed bats () 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 and was recognized as a subfamily of . Evidence that diverged from both and in the Eocene confirmed their family rank, but their intrafamilial relationships remain poorly resolved. We examined genetic variation in the Afrotropical hipposiderids , , and 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 and as Afrotropical sister genera distinct from a Paleotropical ; mitochondrial analyses interpose the genera , , and between these clades. Mitochondrial analyses also suggest at least two separate colonizations of Africa by Asian groups of , but the actual number and direction of faunal interchanges will hinge on placement of the unsampled African-Arabian species . 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 . 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 and .

Keywords
Patterson, Webala, Lavery, Agwanda, Goodman, Peterhans, and Demos: Evolutionary relationships and population genetics of the Afrotropical leaf-nosed bats (Chiroptera, Hipposideridae)

Introduction

The Old World leaf-nosed bats, family Hipposideridae, currently include seven genera and 90 species of insectivorous bats distributed over much of the Paleotropics (Monadjem 2019; Simmons and Cirranello 2019). Both the taxonomic and phylogenetic histories of this family are confused. Throughout much of its history (e.g., Koopman 1989), Hipposideridae was considered either a subfamily of the Rhinolophidae (the horseshoe bats) or as its sister family within the Rhinolophoidea. Recently, however, the “trident bats” (Cloeotis, Paratriaenops, Rhinonicteris, and Triaenops) were shown to comprise a family-ranked group, the Rhinonycteridae, which is separate from and sister to the Hipposideridae (Foley et al. 2015; Armstrong et al. 2016). Even the genus Hipposideros Gray, 1831, as it was traditionally understood, appears paraphyletic with respect to the allied genera Asellia, Aselliscus, Coelops, and Anthops (Foley et al. 2015; Amador et al. 2018). Re-validation of Macronycteris Gray, 1866 and Doryrhina Peters, 1871 for groups of Afrotropical endemic species more closely related to each other than to African and Asian members of Hipposideros sensu stricto resolved a number of those issues (Foley et al. 2017).

The species richness of Doryrhina, Macronycteris, and Hipposideros differs widely. Most authors recognize two species of Doryrhina (D.cyclops and D.camerunensis), five species of Macronycteris (M.commersoni, M.cryptovalorona, M.gigas, M.thomensis, and M.vittata), and 83 species of Hipposideros , 10 of which occur in Africa (Monadjem 2019; Simmons and Cirranello 2019). These are H.beatus, H.caffer, H.curtus, H.fuliginosus, H.lamottei, H.ruber, and H.tephrus in the bicolor group of Hipposideros; H.jonesi and H.marisae in the speoris group, and H.megalotis in the megalotis group (Hill 1963; Murray et al. 2012; Monadjem 2019). In addition, three extinct species of hipposiderid are known from the region: †Macronycterisbesaoka (Madagascar), †Hipposiderosamenhotepos (Egypt), and †H.kaumbului (Ethiopia). Type localities for valid species, subspecies, and synonyms for these three genera in Africa and Madagascar appear in Figure 1; after the removal of Doryrhina and Macronycteris taxa, group assignments for the species remaining in Hipposideros appear in Table 1.

Figure 1.
Type localities for Afrotropical hipposiderids: Doryrhina, blue symbols; Hipposideros, white symbols; Macronycteris , black symbols. Stars denote valid species, whereas circles indicate taxa considered as subspecies or synonyms. Localities are projected onto the biome map of Olson et al. (2001). Taxa depicted are: Hipposiderosabae J. A. Allen,1917; †Hipposideros (Pseudorhinolophus) amenhotepos Gunnell, Winkler, Miller, Head, El-Barkooky, Gawad, Sanders & Gingerich, 2015; Phyllorhinaangolensis Seabra, 1898; Hipposideroscaffervar.aurantiaca De Beaux, 1924; Hipposiderosbeatus K. Andersen, 1906; †Hipposiderosbesaoka Samonds, 2007; Phyllorrhinabicornis Heuglin, 1861; Hipposiderosbraima Monard, 1939; Hipposideroscaffer Sundevall, 1846; Phyllorhinacaffra Peters, 1852; Hipposideroscamerunensis Eisentraut, 1956; Hipposideroscaffercentralis K. Andersen, 1906; Rhinolophus Commersonii É. Geoffroy, 1813; Hipposideroscryptovalorona Goodman, Schoeman, Rakotoarivelo & Willows-Munro, 2016; Hipposideroscurtus G. M. Allen, 1921; Phyllorrhinacyclops Temminck, 1853; Phyllorrhinafuliginosa Temminck, 1853; Hipposiderosgigasgambiensis K. Andersen, 1906; Rhinolophusgigas Wagner, 1845; Phyllorrhinagracilis Peters, 1852; Hipposideroscafferguineensis K. Andersen, 1906; Hipposiderosjonesi Hayman, 1947; †Hipposideroskaumbului Wesselman, 1984; Hipposideroslamottei Brosset, 1985; Hipposideroslangi J. A. Allen, 1917; Hipposiderosmarisae Aellen, 1954; PhyllorhinaCommersoni, var. marungensis Noack, 1887; Hipposiderosbeatusmaximus Verschuren, 1957; Phyllorrhinamegalotis Heuglin, 1861; Rhinolophusmicaceus de Winton, 1897; HipposiderosCommersoni mostellum Thomas, 1904; Hipposiderosnanus J. A. Allen, 1917; Hipposiderosgigasniangarae J. A. Allen, 1917; Hipposideroscafferniapu J. A. Allen, 1917; Phyllorrhinarubra Noack, 1893; Hipposiderossandersoni Sanderson, 1937; Hipposiderostephrus Cabrera, 1906; PhyllorhinaCommersoni, var. thomensis Bocage, 1891; Hipposiderosgigasviegasi Monard, 1939; Phyllorhinavittata Peters, 1852.
Table 1.
Species groups of Hipposideros (modified from Murray et al. 2012 to include newly recognized forms and to remove species now recognized in Doryrhina and Macronycteris).
Armiger groupcalcaratus subgroupH.macrobullatusH.lankadiva
H.alongensisH.calcaratus cH.maggietayloraeH.lekaguli
H.armigerH.cervinus cH.nequamH.pelingensis
H.griffini aH.coxi cH.obscurusLarvatus group
H.pendelburyi aH.galeritus cH.orbiculusH.grandis
H.turpisruber subgroupH.papuaH.khasiana” a,g
Bicolor groupH.abae dH.pygmaeusH.larvatus
ater subgroupH.beatus eBoeadii groupH.madurae
H.ater bH.caffer eH.boeadiiH.sorenseni
H.atrox aH.fuliginosus eCyclops group fH.sumbae
H.bicolor bH.lamottei eH.corynophyllusMegalotis group
H.breviceps bH.ruber eH.edwardshilliH.megalotis
H.cineraceus bH.tephrus a,eH.muscinusPratti group
H.coronatus bsubgroup uncertainH.semoniH.lylei
H.dyacorum bH.cruminiferusH.stenotisH.pratti
H.einnaythu a,bH.curtusH.wollastoniH.scutinares
H.halophyllus bH.doriaeDiadema groupSpeoris group
H.khaokhouayensis bH.durgadasiH.demissusH.jonesi h
H.nicobarulae a,bH.fulvusH.diademaH.marisae g
H.pomona bH.gentilis aH.dinopsH.speoris
H.ridleyi bH.hypophyllusH.inexpectatus
H.rotalis bH.kunzi aH.inornatus
(Endnotes) a Added to species list subsequent to Murray et al. (2012) b Recognized in the Ater species group by Monadjem (2019) c Recognized in the Calcaratus species group by Monadjem (2019) d Formerly listed in the Speoris group but transferred to the Ruber group by Monadjem (2019) e Recognized in the Ruber species group by Monadjem (2019) f H.cyclops and H.camerunensis are now recognized as members of Doryrhina; listed species were treated as Doryrhina in Monadjem (2019) on the basis of similar morphology but were recognized as the Muscinus group by Tate (1941); they might represent an unnamed genus or subgenus. g Invalid name accorded to what is likely a real biological entity (cf. Monadjem 2019) h Formerly in the Bicolor species group but transferred to the Speoris group by Monadjem (2019).

As suggested by their checkered taxonomic history, phylogenetic understanding of the Hipposideridae has slowly come into focus. Doryrhina and Macronycteris are two of a dozen generic-group names that were synonymized with Hipposideros for all of the 20th century (Miller 1907; Allen 1939; Koopman 1994). Instead of subgenera, taxonomists used the species groups delineated by Andersen (1918) and refined by Tate (1941) and Hill (1963) in their generic revisions based on morphology. Assessment of rhinolophoid relationships using an intron supermatrix (Eick et al. 2005) confirmed the early divergence of hipposiderids and rhinolophids (estimated at 41 Ma), thereby substantiating their rank as a separate families. Despite earlier suppositions that the area of origin for Hipposideridae was in Asia (Koopman 1970; Bogdanowicz and Owen 1998) or Australia (Hand and Kirsch 1998), Eick et al. (2005) clearly demonstrated the ancestry of the family (and superfamily) was in Africa. A recent supermatrix analysis with the most comprehensive taxonomic sampling (42 species; Amador et al. 2018) confirmed the early divergence of hipposiderids and rhinolophids at 41.3 Ma, but this analysis questioned the validity of both Doryrhina and Macronycteris. Amador et al. attributed the paraphyly of Hipposideros sensu lato documented by Foley et al. (2015) to their limited taxonomic sampling. Amador et al. (2018) also challenged the integrity of the commersoni, cyclops, speoris, and bicolor species groups, arguing that all African species save for H.jonesi belonged in a single, exclusively African species group.

Although new species of hipposiderids are regularly discovered and described in Asia (Robinson et al. 2003; Guillen-Servent and Francis 2006; Bates et al. 2007; Douangboubpha et al. 2011; Thong et al. 2012; Murray et al. 2018), the pace of discovery has been much slower in Africa. Only one extant species has been described since the recognition of Hipposideroslamottei (Brosset 1985 [“1984”]), and that one was from Madagascar (Goodman et al. 2016). Surveys of mitochondrial sequences from African hipposiderids have strongly suggested that supposedly widespread species such as Hipposideroscaffer and H.ruber actually represent complexes of cryptic species (Vallo et al. 2008, 2011; Monadjem et al. 2013). Phylogenetic analyses (e.g., Vallo et al. 2008) show that these named species complexes are not monophyletic, resolving clades comprised of bats identified as both H.caffer and H.ruber . These studies have characterized the clades in both morphological and genetic terms, even establishing them in sympatry (see also Vallo et al. 2011). However, the uncertain relationship of the identified clades to the many names already proposed for Afrotropical hipposiderids, many based on incomplete or formalin-preserved specimens, has precluded formally naming them. Incomplete geographic sampling and the lack of evidence from nuclear genes for these populations has also clouded interpretations of this mitochondrial diversity.

Our field surveys in Eastern Africa and adjoining regions offer a new basis for considering the taxonomy and phylogenetics of Afrotropical hipposiderids. We sought to answer these questions: (1) Is there compelling evidence to support the recognition of Doryrhina and Macronycteris as distinct Afrotropical genera alongside the Paleotropical Hipposideros? (2) Which species belong to these groups? (3) Are the traditional species groups of African hipposiderids monophyletic? Using both mitochondrial and nuclear intron sequences, we also evaluate the question of cryptic species among African hipposiderids and the possibility of mitochondrial-nuclear discordance.

Material and methods

Selection of taxa and sampling

Our genetic dataset is based on 453 hipposiderid individuals, the vast majority being represented by museum vouchers. We generated original genetic data from 319 individuals collected at 102 georeferenced localities, and complemented them with 134 mitochondrial sequences from 90 localities downloaded from GenBank (we obtained new sequence data for five individuals with prior GenBank records; see Suppl. material 1: Figure S1 and Appendix I). All individuals were sequenced for Cytochrome-b (cyt-b) in order to maximize assessment of genetic diversity; however, redundant haplotypes were removed for subsequent phylogenetic analyses (see Appendix I for complete list of individuals sequenced). The bats newly sequenced for this study were obtained over several decades in the course of small mammal surveys across sub-Saharan Africa and Madagascar, with relatively dense sampling in East Africa. Initial assignment of East African individuals to species was determined using meristic, mensural, and qualitative characters published in the bat keys of Thorn et al. (2009) and Patterson and Webala (2012). Collection methods followed mammal guidelines for the use of wild mammals in research and education (Sikes and the Animal Care and Use Committee of the American Society of Mammalogists 2016) and the most recent collections were approved under Field Museum of Natural History’s IACUC #2012-003. Only GenBank records for cyt-b were available for records of the Arabian-North African hipposiderid Asellia, which was included for context in the phylogenetic analyses. Lacking information from nuclear introns, we draw no firm conclusions from their placement and do not discuss Asellia in this paper (see Benda et al. 2011; Bray and Benda 2016).

Appendix I contains the institutions and voucher numbers, GenBank accession numbers, and locality information for our samples. The fact that museum voucher specimens were used wherever possible for the genetic analyses permits the genetic analysis to serve as a foundation for integrative taxonomic analyses of dental, cranial, and skeletal variation, using the same specimens. To avoid adding to current taxonomic confusion, we take a conservative approach in assigning names to clades in our analyses. Where a clade’s taxonomic identity was ambiguous or unknown, we referred to it simply as a numbered clade. Integrative taxonomic diagnoses of the various clades supported by our analyses will be necessary to determine which, if any, existing names may apply to them. However, to relate our results to those of earlier studies of African Hipposideros (Vallo et al. 2008, 2011; Monadjem et al. 2013), we cross-referenced specimens used in two or more analyses to equate the various non-binomial names that have been applied to these cryptic lineages.

DNA extraction, amplification, and sequencing

Genomic DNA from preserved tissue samples was extracted using the Wizard SV 96 Genomic DNA Purification System (Promega Corporation, WI, USA). Fresh specimens were sequenced for mitochondrial cytochrome-b (cyt-b), using the primer pair LGL 765F and LGL 766R (Bickham et al. 1995; Bickham et al. 2004), and four unlinked autosomal nuclear introns: ACOX2 intron 3, COPS7A intron 4, ROGDI intron 7 (Salicini et al. 2011), and STAT5B (Matthee et al. 2001) for hipposiderid specimens and the sister group Triaenopsafer (Rhinonycteridae; see Table 1 for primer information). PCR amplification, thermocycler conditions, and sequencing were identical to Patterson et al. (2018) and Demos et al. (2018). Sequences were assembled and edited using GENEIOUS PRO v.11.1.5 (Biomatters Ltd). Sequence alignments were made using MUSCLE (Edgar 2004) with default settings in GENEIOUS. Protein coding data from cyt-b were translated to amino acids to determine codon positions and confirm the absence of premature stop codons, deletions, and insertions. Several gaps were incorporated in the nuclear intron alignments, but their positions were unambiguous.

Sequence alignments used in this study have been deposited on the FIGSHARE data repository (https://doi.org/10.6084/m9.figshare.11936250). All newly generated sequences were deposited in GenBank with accession numbers MT149315–MT149893 (see also Appendix I).

Phylogenetic analyses

jMODELTEST2 (Darriba et al. 2012) on CIPRES Science Gateway v. 3.3 (Miller et al. 2010) was used to determine the sequence substitution models that best fit the data using the Bayesian Information Criterion (BIC) for cyt-b and the four nuclear introns. PARTITIONFINDER2 (Lanfear et al. 2016) on CIPRES was used to determine the sequence substitution models for the concatenated alignment of four nuclear introns using the Bayesian Information Criterion (BIC) with the ‘greedy’ search algorithm. Uncorrected sequence divergences (p -distances) between and within species/clades were calculated for cyt-b using MEGA X v. 10.0.5 (Kumar et al. 2018). Maximum-likelihood (ML) analyses were performed using the program IQ-TREE v. 1.6.10 (Chernomor et al. 2016; Nguyen et al. 2015) on the CIPRES portal for separate gene trees (cyt-b, ACOX2, COPS7A, ROGDI, and STAT5B) and a concatenated alignment, partitioned by gene, using the four nuclear introns. As in Hillis and Bull (1993), nodes supported by bootstrap values (BP) ≥ 70% were considered strongly supported. Gene tree analyses under a Bayesian Inference (BI) framework were inferred in MRBAYES v. 3.2.7 (Ronquist et al. 2012) on the CIPRES portal for the same set of genes as the ML analyses. Two independent runs were conducted in MrBayes, and nucleotide substitution models were unlinked across partitions for each nuclear locus in the concatenated alignment. Four Markov chains were run for 1 × 108 generations for individual gene trees, and 2 × 107 generations for the concatenated analysis, using default heating values and sampled every 1000th generation. A conservative 25% burn-in was applied and stationarity of the MRBAYES results was assessed in Tracer v. 1.7 (Rambaut et al. 2018). Majority-rule consensus trees were constructed for each Bayesian analysis. Following Erixon et al. (2003), nodes supported by posterior probabilities (PP) ≥0.95 were considered strongly supported.

Haplotype networks for cyt-b were inferred using the median-joining network algorithm in PopArt v. 1.7 (Leigh and Bryant 2015). Separate analyses were carried out for the following clades, each consisting of four subclades: (1) Doryhina (D.camerunensis, D.cf.camerunensis, D.cyclops1, and D.cyclops2); (2) Macronycteris (M.commersoni, M.cryptovalorona, M.gigas, and M.vittata); (3) Hipposideroscaffer1–4; (4) Hipposideroscaffer5–8; and (5) Hipposiderosruber1–4.

Hipposiderid taxa included in the species tree analyses were assigned to either species or numbered clades based on clade support in the ML and BI gene-tree analyses of the cyt-b dataset. This in turn identified populations to be used as ‘candidate species’ in a coalescent-based species-tree approach implemented in StarBEAST2 (Ogilvie et al. 2017), an extension of BEAST v. 2.5.1 (Drummond et al. 2012; Bouckaert et al. 2014). Species tree analysis was conducted using the four nuclear intron alignments. Substitution, clock, and tree models were unlinked across all loci. A lognormal relaxed-clock model was applied to each locus under a Yule tree prior and a linear with constant root population size model. Four independent replicates were run with random starting seeds, and chain lengths of 1 × 108 generations and parameters were sampled every 5,000 steps. For the StarBEAST2 analyses, evidence of convergence and stationarity of posterior distributions of model parameters was assessed based on ESS values >200 and examination of trace files in Tracer v. 1.7. The burn-in was set at 10% and separate runs were assembled using LOGCOMBINER v. 2.5.1 and TREEANNOTATOR v. 2.5.1 (Rambaut et al. 2018).

Coalescent lineage delimitation

Based on the well supported clades obtained in the cyt-b gene tree analyses and available intron samples, a lineage delimitation scenario with 18 candidate species was tested. We inferred the evolutionary isolation of their gene pools using the phased nuclear DNA dataset (ACOX2, COPS7A, ROGDI, and STAT5A; 104 individuals) for joint independent lineage delimitation and species-tree estimation evaluated under the multi-species coalescent model using the program BPP v. 3.3 (Yang and Rannala 2014; Rannala and Yang 2017). This analysis was carried out to guide future investigations of the species status of evolutionarily isolated lineages inferred here. Supported lineages will be examined using an integrative species taxonomic approach, including morphological, morphometric, and acoustic characters, as well as ectoparasite associations and distributional data. Species/clade memberships for BPP were identical to individuals assigned to lineages in the species tree analyses. The validity of our assignment of individuals to populations was tested using the guide-tree-free algorithm (A11) in BPP. Because the probability of delimitation by BPP is sensitive to selected parameters (Leaché and Fujita 2010; Yang 2015), we evaluated two independent runs for each of four different combinations of divergence depth and effective population sizes priors (τ and θ , respectively; Table 2). Two independent MCMC chains were run for 5 × 104 generations. The burn-in was 20% and samples drawn every 50th generation. In total, eight BPP runs were carried out using four phased nuclear intron alignments. Lineages were considered to be statistically well supported when the delimitation posterior probabilities generated were ≥0.95 under all four combinations of priors.

Table 2.
Primer information and chosen substitution models for regions amplified in this study. Substitution models before “/” are the best-supported models inferred by jMODELTEST2 and models after “/” indicate those inferred by PARTITIONFINDER2 for the concatenated intron alignment.
Primer nameSequencePrimer publicationSubstitution model
ACOX2-3-F5’-CCTSGGCTCDGAGGAGCAGAT-3’Salicini et al. 2011K80+G / K81+G
ACOX2-3-R5’-GGGCTGTGHAYCACAAACTCCT-3’
COPS7A-4-F5’-TACAGCATYGGRCGRGACATCCA-3’Salicini et al. 2011HKY / K80
COPS7A-4-R5’-TCACYTGCTCCTCRATGCCKGACA-3’
ROGDI-7-F5’-CTGATGGAYGCYGTGATGCTGCA-3’Salicini et al. 2011K80+G / K81+G
ROGDI-7-R5’-CACGGTGAGGCASAGCTTGTTGA-3’
STAT5B-16-F5’--CTGCTCATCAACAAGCCCGA-3’Matthee et al. 2001GTR+G / K81+G
STAT5B-16-R5’-GGCTTCAGGTTCCACAGGTTGC-3’
cyt-b-LGL-765-F5’-GGCTTCAGGTTCCACAGGTTGC-3’Trujillo et al. 2009GTR+I+G
cyt-b -LGL-766-R5’-GTTTAATTAGAATYTYAGCTTTGGG-3’
Table 3.
Prior Schemes (PS) used in BPP analyses. Prior distributions on τ represent two relative divergence depths (deep and shallow) and on θ represent two relative effective population sizes (large and small) scaling mutation rates.
PSEffective pop. sizeDivergence depthGamma distribution for prior
1LargeDeepθ = Γ [1, 10] and τ = Γ [1, 10]
2LargeShallowθ = Γ [1, 10] and τ = Γ [2, 2000]
3SmallShallowθ = Γ [2, 2000] and τ = Γ [2, 2000]
4SmallDeepθ = Γ [2, 2000] and τ = Γ [1, 10]

Results

In terms of cyt-b sequence divergence, clades within Doryrhina are separated by 3.0–5.7% genetic distances, whereas less than 3% separates the four recognized species of Macronycteris. Between Afrotropical Hipposideros, the greatest distances separate H.jonesi from other lineages (13.4–16.1%). The various numbered clades allied to Hipposideroscaffer differ from one another in cyt-b sequences by 2.5–10.3% and clades allied to H.ruber differ by 3.0–8.2% (Table 4).

Table 4.
Uncorrected cyt-b p-distances between (off diagonal) and within (on diagonal) Afrotropical hipposiderid clades, showing the number of base differences per site averaged over all sequence pairs between groups. The analysis involved 386 nucleotide sequences and all ambiguous positions were removed; na (not available) reflects a sample size of one individual.
[1][2][3][4][5][6][7][8][9][10][11][12][13][14][15]
[1]Doryrhinacamerunensis0.003
[2]Doryrhinacf.camerunensis0.055na
[3]Doryrhinacyclops 10.0570.0480.008
[4]Doryrhinacyclops 20.0550.0410.0300.006
[5]Hipposiderosabae0.1760.1730.1680.1660.033
[6]Hipposiderosbeatus 10.1520.1560.1600.1520.1160.007
[7]Hipposiderosbeatus 20.1460.1490.1510.1470.1170.0440.006
[8]Hipposideroscaffer 10.1570.1540.1500.1480.1080.1030.1060.006
[9]Hipposideroscaffer 20.1530.1500.1500.1470.1060.0960.1080.0450.01
[10]Hipposideroscaffer 30.1520.1480.1500.1490.1080.1100.1110.0460.0520.011
[11]Hipposideroscaffer 40.1620.1590.1600.1540.1060.1050.1140.0770.0780.0790.018
[12]Hipposideroscaffer 50.1500.1550.1590.1480.1130.0910.0960.0950.1010.1030.0980.005
[13]Hipposideroscaffer 60.1550.1560.1640.1530.1120.0930.1020.0900.0970.0990.0940.0280.011
[14]Hipposideroscaffer 70.1510.1540.1610.1480.1080.0840.0940.0940.0940.0980.0960.0250.0320.011
[15]Hipposideroscaffer 80.1540.1550.1600.1520.1110.0900.0920.0920.0950.1020.0930.0330.0390.0290.021
[16]Hipposiderosfuliginosus0.1550.1490.1540.1420.1010.0950.0960.0780.0840.0870.0940.0880.0860.0800.085
[17]Hipposiderosjonesi0.1530.1430.1540.1470.1600.1450.1380.1350.1400.1400.1390.1340.1340.1370.139
[18]Hipposideroslamottei0.1710.1730.1740.1630.1060.0970.1180.0940.0860.0950.0970.0570.0590.0520.060
[19]Hipposideroscf.lamottei0.1580.1580.1560.1490.1070.1030.1070.0910.0990.0950.0970.0530.0580.0520.054
[20]Hipposiderosmarisae0.1770.1800.1780.1720.1590.1530.1530.1440.1480.1400.1520.1480.1440.1540.159
[21]Hipposiderosruber 10.1550.1510.1520.1420.1040.0990.1010.0810.0840.0850.0860.0900.0810.0820.082
[22]Hipposiderosruber 20.1550.1550.1560.1420.1030.0970.1020.0810.0820.0890.0890.0860.0780.0830.081
[23]Hipposiderosruber 30.1590.1490.1550.1470.1050.0940.1010.0840.0820.0960.0880.0900.0830.0820.082
[24]Hipposiderosruber 40.1530.1470.1510.1410.1000.0940.0970.0730.0730.0850.0820.0830.0770.0780.078
[25]Hipposideroscf.ruber0.1640.1610.1610.1530.0990.0940.1000.0860.0840.0950.0930.0810.0800.0800.083
[26]Macronycteriscommersoni0.1570.1560.1550.1450.1640.1590.1540.1640.1690.1680.1710.1660.1700.1670.162
[27]Macronycteriscryptovalorona0.1470.1430.1470.1420.1570.1520.1460.1560.1620.1610.1650.1590.1640.1580.157
[28]Macronycterisgigas0.1510.1490.1540.1440.1640.1630.1580.1620.1680.1650.1700.1650.1710.1640.165
[29]Macronycterisvittata0.1470.1480.1490.1400.1620.1580.1470.1600.1610.1660.1650.1640.1690.1640.163
Table 4.
Continued.
[16][17][18][19][20][21][22][23][24][25][26][27][28][29]
[16]Hipposiderosfuliginosus0.003
[17]Hipposiderosjonesi0.1370.008
[18]Hipposideroslamottei0.1000.1610.038
[19]Hipposideroscf.lamottei0.0910.1420.0540.006
[20]Hipposiderosmarisae0.1450.0920.1560.158na
[21]Hipposiderosruber 10.0820.1440.0930.0870.1520.013
[22]Hipposiderosruber 20.0840.1470.0930.0910.1570.0300.007
[23]Hipposiderosruber 30.0820.1420.0850.0880.1580.0520.0570.022
[24]Hipposiderosruber 40.0780.1400.0870.0880.1540.0530.0510.057na
[25]Hipposideroscf.ruber0.0840.1420.0940.0890.1570.0810.0810.0820.0720.033
[26]Macronycteriscommersoni0.1550.1860.1830.1670.1930.1630.1620.1610.1680.1740.012
[27]Macronycteriscryptovalorona0.1490.1760.1700.1630.1850.1610.1610.1580.1600.1620.0280.003
[28]Macronycterisgigas0.1530.1790.1780.1690.1900.1650.1650.1610.1650.1690.0260.0290.012
[29]Macronycterisvittata0.1500.1810.1800.1680.1920.1580.1590.1580.1590.1640.0260.0290.0270.006

Maximum likelihood and Bayesian phylogenies from a 452-individual alignment of cyt-b are shown in Suppl. material 2: Figures S2, Suppl. material 3: Figures S3. Identical haplotypes were pruned from this tree to produce the 303 unique-haplotype alignment shown in Figure 2. The 303 haplotype alignment used in the ML and BI gene tree analyses ranged from 413 to 1140 base pairs (bp) in length (89.9% complete matrix). Only the Bayesian topology is shown, but both posterior probabilities and bootstrap values are depicted at common, well supported nodes. Multiple, geographically cohesive clades are evident for the three widely distributed Afrotropical Hippposideros, H.beatus, H.caffer, and H.ruber.

Figure 2.
Parts A and B. Phylogeny of Hipposideridae based on Bayesian analysis of 303 cyt-b sequences. Colored lines denote well supported clades and symbols denote nodal support: red circles, BS ≥ 70%, PP ≥ 0.95; black circles BS ≥ 70%, PP ≤ 0.95; open circles BS ≤ 70%, PP ≥ 0.95.

Substitution networks for cyt-b haplotypes for Doryrhina, Macronycteris, and Hipposideros are shown in Figures 3, 4, showing the genetic and geographic relationships of the clades identified in Figure 2.

Maximum likelihood and Bayesian phylogenies from a 103-individual alignment of four concatenated introns for Doryrhina, Macronycteris, and Hipposideros are shown in Figure 5. Many of the numbered clades in Figures 24 are jumbled in Figure 5; they are not recovered as monophyletic units and the geographic structure evident in mtDNA analyses disappears.

A species tree generated using StarBEAST from the four introns appears in Figure 6. It depicts well-supported relationships among the various clades allied with H.caffer, H.ruber, and H.beatus. Remarkably, and in contrast with the concatenated analyses, it shows support for the Asian dyad H.diadema and H.larvatus as sister to these ruber subgroup members, with the Asian ater subgroup outside this pairing. There is little support for the deeper phylogenetic nodes.

Figure 3.
Substitution network plots for Afrotropical hipposiderids ADoryrhinaBMacronycteris.
Figure 4.
Substitution network plots for Afrotropical hipposiderids AHipposideroscaffer clades 1–4 BHipposideroscaffer clades 5–8 CH.ruber clades.
Figure 5.
Phylogeny of Hipposideridae based on Bayesian analysis of 103 concatenated nuclear intron sequences. Numbers denote posterior probabilities (BI) and bootstrap percentages (ML); red circles at more terminal nodes indicate BS ≥ 70%, PP ≥ 0.95.
Figure 6.
Species tree Hipposideridae based on StarBEAST analysis of four introns. Posterior probabilities appear at all nodes.

Discussion

Overall genetic variability

The three Afrotropical hipposiderid genera differ substantially in terms of their internal genetic differentiation. Clades of Hipposideros are separated by cyt-b p-distances averaging 9.7% (2.5–16.1%), whereas Doryrhina clades average p-distances of 4.8% (3.0–5.7%) and Macronycteris clades 2.7% (2.6–2.9%). Distance values for these genera tend to fall at the lower end of values obtained with similar sampling intensity for species-ranked clades in other Afrotropical bat genera: 2.5% for Otomops (Patterson et al. 2018), 9.3% for Miniopterus (Demos et al. 2020), 10% for Scotophilus and Rhinolophus (Demos et al. 2018, 2019a), 13.5% for Myotis (Patterson et al. 2019), and 17% for Nycteris (Demos et al. 2019b). Fewer cyt-b substitutions on average for these hipposiderids does not limit support for individual clades, and because distances do not approach those characteristic of substitutional saturation, the cyt-b tree recovers much of the deeper phylogenetic structure evident with nuclear intron sequences (compare Figs 2, 5).

Phylogenetics

Both cyt-b and intron analyses securely recovered Doryrhina, Macronycteris, and Hipposideros as monophyletic. Doryrhina + Macronycteris are sister to the remaining hipposiderids. However, only the cyt-b analysis included the hipposiderid genera Aselliscus, Coelops, and Asellia alongside Hipposideros. That analysis recovered all four genera as monophyletic with strong support. Aselliscus and Coelops were recovered as sister to Hipposideros, with Asellia joining later, but these relationships lacked confident support.

Using a supermatrix approach on exemplars of 46 species of hipposiderids, Amador et al. (2018) found Hipposideros sensu stricto to be paraphyletic. They recovered a mostly Asian group of Hipposideros as sister to two subclades, Coelops + Aselliscus and Asellia + African hipposiderids excluding H.jonesi, which was recovered with the Asian taxa. Paraphyly in this molecular analysis echoed earlier indications of Hipposideros paraphyly from morphology (Bogdanowicz and Owen 1998; Hand and Kirsch 1998, 2003). In another supermatrix analysis of exemplars belonging to 49 hipposiderid species, Shi and Rabosky (2015) failed to recover Macronycteris as monophyletic; M.commersoni was sister to all remaining hipposiderids, but strangely it did not group with M.gigas. When the anomalous position of M.commersoni in their tree is ignored, their topology is highly similar to that of Figure 2, except that Asellia (Aselliscus, Coelops) become the sister of Hipposideros (Macronycteris, Doryrhina), rather than sister of just Hipposideros . Using both mitochondrial and nuclear loci, Lavery et al. (2014) found that 17 species of Asian, Oceanian and Australasian Hipposideros were monophyletic with respect to the genera Aselliscus, Coelops, and Anthops. Clearly, missing data and missing taxa compromise all of these phylogenetic appraisals, so that the question of hipposiderid and Hipposideros monophyly remains open. However, subject to its sampling limitations, there is clear support in our analyses of monophyly for Doryrhina, Macronycteris, and Hipposideros as we apply these names.

Despite employing different mitochondrial and nuclear loci and using different sets of taxa, the phylogeny recovered by Lavery et al. (2014) is largely congruent with that in Figure 5. Their earliest diverging species group of Hipposideros is the calcaratus group, not represented in our tree unless H.obscurus is a member (Table 1). Their next diverging unit is the diadema group, which is also positioned near the base of our tree. Their other two groups are paired: the galeritus group (which includes H.cervinus, indicating that this species is misclassified as calcaratus member) joined with the bicolor/ater group. In our intron analysis (Fig. 5), members of the larvatus and diadema groups join H.obscurus as sister to all remaining Hipposideros groups. The remainder form a trichotomy: H.coronatus, typically considered in the bicolor group; H.pygmaeus and H.cervinus, which are listed in different groups but were both considered members of the galeritus unit by Tate (1941); and the erstwhile bicolor group (sensu Hill 1963), which was subdivided into the ater subgroup (for Asian, Oceanian, and Australasian species) and the ruber subgroup (for Atrotropical ones) by Monadjem (2019).

The ater subgroup members included in our mitochondrial analysis (Fig. 2) form a well-supported clade consisting of H.bicolor, H.cineraceus, H.pomona, H.doriae, H.ater, H.khaokhouayensis, H.rotalis, H.halophyllusH.dyacorum, H.ridley, and H.durgadasi. This group is sister to all analyzed members of the ruber subgroup: the various clades allied with Hipposiderosbeatus, H.caffer, and H.ruber, as well as individuals of the Afrotropical species H.lamottei and H.fuliginosus. H.abae, which was previously considered in the speoris group (Simmons 2005; Murray et al. 2012), is clearly a member of the ruber group. Outside this pairing are the Asian species H.cervinus, H.coronatus, H.coxi, H.obscurus, and H.pygmaeus. Two Afrotropical species also lie outside the ruber + ater clade: H.jonesi and H.marisae, both thought to belong to the speoris group, appear as sisters in Figure 2A.

Parsimony, topological position, and the strong support of branching relationships in the mitochondrial and intron trees (Fig. 5; also Lavery et al. 2014) make it clear that the Afrotropical ruber group represents a comparatively recent colonization event from Asian ancestors–the ruber group is sister to the ater group and this pair has Asian sisters. However, although the basal dichotomy within Hipposideros includes an all Asian clade, lack of support for its sister(s) clouds the phylogenetic position of the H.jonesi-H.marisae clade–possibly sister to all sampled Hipposideros but more likely sandwiched between Asian clades. In any case, Figure 2 suggests that the H.jonesi-H.marisae clade resulted from an earlier African-Asian colonization event.

The lack of agreement in the phylogenetic position of H.diadema and H.larvatus between the concatenated intron tree (Fig. 5) and the species tree (Fig. 6) deserves comment, as both analyses were based on the same genetic dataset. The position of H.diadema-H.larvatus as sister to the ruber group (Fig. 6) runs counter to both our other genetic analyses (Figs 2, 5) and morphological assessments (Hill 1963; Murray et al. 2012; Table 1). This discrepancy is likely due to the generally weaker support for deep nodes within the tree; in the absence of saturation, this is often taken as evidence of rapid evolutionary radiations (e.g., Almeida et al. 2011). Lanier and Knowles (2014) used simulated data on deep phylogenies to show that species-tree methods do account for coalescent variance at deep nodes but that mutational variance among lineages poses the primary challenge for accurate reconstruction. In either case, vastly expanded genetic sampling via NGS techniques offers the most plausible avenues to clearer resolution.

However, the highly distinctive species H.megalotis belongs to its own species group (Table 1) and has not been included in any genetic analysis. Distributed in the Horn of Africa and the Arabian Peninsula, H.megalotis is the only hipposiderid with a fold of skin joining the base of the ear pinnae. Its uniquely specialized auditory system and derived dentition (e.g., loss of anterior premolars and enlargement of outer lower incisors), led Hill (1963) to regard it as a species that diverged early from the other groups of African Hipposideros. Including this species in future analyses would shed light on the group’s biogeography. Were there three colonizations of Africa by Asian groups of Hipposideros or could H.megalotis be sister to all Asian lineages of this genus? This information would greatly clarify ancestral geographic range inference.

Species limits

The lineage delimitation analyses indicate that a number of hipposiderid lineages are either unnamed or unidentified, and also that a number of recognized species may not be genetically and evolutionarily independent.

Previous studies had indicated that both Hipposideroscaffer (Vallo et al. 2008) and H.ruber (Vallo et al. 2011) appear to be complexes of cryptic species. The two are traditionally distinguished on the basis of size and pelage color, H.ruber being the larger and more brightly colored form, but this distinction is clouded by geographic variation in size and the presence of both reddish and gray-brown phases in both species. Our mitochondrial analyses identified four H.ruber lineages and eight H.caffer lineages in two distinct groupings among the sampled populations (Fig. 2). Four of the caffer lineages and three of the ruber clades were identified as putative species by the BPP analyses (Table 5). The large number of clades in East Africa is remarkable: Kenya and Tanzania each support four of the eight clades allied with H.caffer , and all but one of the eight clades known from throughout the continent occur in one or the other East African country. This undoubtedly reflects the region’s great landscape diversity, where West and Central African rainforests reach their eastern limit, southern savannas reach their northern limits, the Sahel reaches its southern limits, and all are riven by the African Rift Valley. It also is a product of our sampling intensity (see Suppl. material 1: Fig. S1).

Table 5.
Lineage delimitation results from BPP based on the four intron dataset for mtDNA-supported clades of Afrotropical Hipposideridae. PS1-PS4 refer to four different prior schemes based on population size and age of divergence priors (see Table 3 for parameter details). Bold font indicates that the putative species was delimited under all parameter settings.
Putative SpeciesPS1PS2PS3PS4
Doryrhinacamerunensis0.300.760.950.51
D.cf.camerunensis0.320.730.970.79
D.cyclops 20.230.680.950.51
Hipposiderosbeatus 21111
H.caffer 10.990.990.990.99
H.caffer 20.99111
H.caffer 30.990.990.990.99
H.caffer 50.140.180.110.08
H.caffer 60.560.610.850.82
H.caffer 70.140.180.110.08
H.caffer 80.990.990.990.99
H.ruber 10.990.990.990.99
H.ruber 210.9910.99
H.ruber 40.990.990.990.99
Macronycteriscommersoni0.240.720.940.52
M.cryptovalorona0.350.810.970.76
M.gigas0.090.430.910.38
M.vittata0.110.440.900.34

Because some cyt-b sequences were used in multiple studies of this group, it is possible to relate our clade labels to those used by earlier studies (Table 6). Based on attributions made on morphological grounds by Vallo et al. (2008) and Monadjem et al. (2013), some well-supported but unnamed clades in our analysis can be identified. For instance, caffer1 has a distributional range and includes specimens previously identified as Hipposiderostephrus (Appendix I), while specimens of caffer4 come from near the type locality of H.caffer Sundevall, 1846, and may well represent that species. However, no samples confidently identified as H.ruber from the vicinity of its type locality have been sequenced, leaving the application of that name to clades in any of these trees purely conjectural. Applying formal names only after integrative taxonomic assessment is a responsible course as multispecies coalescent models like BPP can lead to over-splitting of species, especially when applied to geographically variable species complexes with parapatric distributions (Chambers and Hillis 2020).

Table 6.
Clade names and associated binomials (if used) for three analyses of cryptic lineages within the ruber species group of Hipposideros. No genetic analysis of this group has included type material; consequently, the application of binomials hinges on the robustness of ancillary morphological analyses, which were not conducted in our study. Boldfaced names denote clades supported by all four prior schemes in our BPP delimitation analyses.
Vallo et al. (2008)Monadjem et al. (2013)This paper
A1H.caffercaffer 4
A1aH.caffercaffer 4
A1bH.caffercaffer 4
A2H.cafferH.caffertephruscaffer 1
BH.rubercaffer 5
B1H.rubercf. lamottei
B2H.rubercaffer 7
C1H.ruberruber 1, ruber 2
C1aH.cf.ruberruber 1
C1bH.cf.ruberruber 1
C2H.ruberC2H.cf.ruberruber 3
ruber 4
DH.ruberH.cf.rubercf. ruber
D1H.cf.rubercf. ruber
D2H.cf.rubercf. ruber
E1H.cf.rubercf. ruber
E2H.cf.rubercf. ruber
caffer 2
caffer 3
caffer 6
caffer 8
abaeH.abaeabaeH.abaeabae
beatusH.beatusbeatusH.beatusbeatus1, beatus 2
fuliginosusH.fuliginosusfuliginosusH.fuliginosusfuliginosus
lamotteiH.lamotteilamotteiH.lamotteilamottei

Doryrhina is a poorly known genus characterized morphologically by the peculiar club-shaped processes on the central and posterior nose leaves. This trait is shared by the two recognized African species, D.cyclops and D.camerunensis, which differ chiefly in size (the latter is larger, with forearm lengths >75 mm). Although D.cyclops is considered to be monotypic, mitochondrial sequences clearly separate West African populations in Liberia and Senegal (cyclops1) from Central African populations in Gabon and Central African Republic (cyclops2), and these are substantially separated from D.camerunensis and a specimen referred to that species from Tanzania (Figs 2, 3). However, both the intron analysis (Fig. 5) and the species tree (Fig. 6) show little or no geographic structure. The BPP analyses confirm that none of the mitochondrial clades is behaving as an independent evolutionary lineage (Table 5). Geographic structure in mtDNA but continent-wide admixture in the nuclear genome could result from either male-biased dispersal with female philopatry or highly structured seasonal migrations, which are known in other hipposiderids. In any case, the genetic patterns of Doryrhina are hard to reconcile with its space-use behavior; individuals appear to have very small home ranges, on the order of a few hectares (Monadjem 2019). An integrative taxonomic review of the genus Doryrhina is needed to determine the validity of D.cyclops and D.camerunensis . It would also shed light on whether six Australo-Papuan species tentatively allocated to that genus (cf. Monadjem 2019) belong there or elsewhere. Tate (1941) had earlier allocated those species to the Australasian muscinus group, convergent on but separate from his Afrotropical cyclops group, but Hill (1963) later united these groups.

Our analysis included four of the five recognized species of Macronycteris, lacking only M.thomensis, which is endemic to São Tomé Island in the Gulf of Guinea. Two species, M.gigas and M.vittata, occur on the African mainland and two others, M.commersoni and M.cryptovalorona, occur on Madagascar. Macronycteriscryptovalorona was named only in 2016, on the basis of its strong genetic divergence from M.commersoni ; it appears in Figure 2 as sister to all three remaining species of Macronycteris . Despite a search for diagnostic characters, Goodman et al. (2016) could not distinguish it morphologically from M.commersoni . Both species are known to occur in the same caves in south central and southwestern Madagascar (Goodman et al. 2016; Rakotoarivelo et al. 2019). On the other hand, M.vittata and M.gigas are distinguished typically on the basis of size and pelage color (cf. Monadjem 2019). They are also known to occur together in the same cave (Shimoni Cave in Kwale, Kenya; Webala et al. 2019), where they utilize echolocation calls with different peak frequencies: vittata at 64–70 kHz and gigas at 53.4–54.8 kHz. Both in Africa and on Madagascar, these pairs of taxa appear to act as distinct species, but the monophyly evident in the cyt-b sequences (Figs 2, 4) disappears in the nuclear intron analyses. BPP analyses fail to resolve any of the Macronycteris species, and none appear as monophyletic in the concatenated intron analyses.

Our results clearly underscore the importance of using multilocus datasets to evaluate phylogenetic and phylogeographic relationships at the genus and species level in mammals. Use of a single genetic system may lead to widely divergent conclusions regarding species identity and distribution. Toews and Brelsford (2012) reviewed cases of mito-nuclear discordance in animals generally. Fully 18% of the cases they reviewed had discordant patterns of mitochondrial and nuclear DNA. In most cases, such patterns are attributable to adaptive introgression of mtDNA, demographic disparities, and sex-biased asymmetries; in some cases they found evidence for hybrid zone movement or human agency. Discordant patterns of variation between mitochondrial and nuclear DNA have been reported in at least six other families of bats (Nesi et al. 2011; Furman et al. 2014; Naidoo et al. 2016; Hassanin et al. 2018; Demos et al. 2019a; Gürün et al. 2019). Gürün et al. (2019) implicated the role of sex-biased dispersal in causing such discordance, male dispersal spreading nuclear variation farther and faster than the movement of mitochondria. This may be a more general pattern in bats (see also Demos et al. 2019b). To understand the processes responsible for these discordant patterns of genome evolution, extensive genomic sampling and far fuller knowledge of natural history will be required.

Acknowledgments

We thank Michael Bartonjo, Carl Dick, Ruth Makena, Beryl Makori, David Wechuli, Richard Yego, and Aziza Zuhura for help in obtaining specimens in the field. We acknowledge with special thanks the assistance of Simon Musila (National Museums of Kenya), Donna Dittman and Jacob Esselstyn (Louisiana State University) and Maria Eifler (University of Kansas) for loans of material. We also appreciate the efforts of curators and collection managers in all the institutions cited in Appendix I for maintaining the museum voucher specimens that enable integrative taxonomic studies to confidently name our numbered lineages. Fieldwork in eastern and southern Africa was funded by various agencies in cooperation with the Field Museum, especially the JRS Biodiversity Foundation. Field Museum’s Council on Africa, Marshall Field III Fund, and Barbara E. Brown Fund for Mammal Research were critical to fieldwork and analyses, as were supporters Bud and Onnolee Trapp and Walt and Ellen Newsom. The John D. and Catherine T. MacArthur Foundation, Fulbright Program of US Department of State, Wildlife Conservation Society, and the Centers for Disease Control and Prevention sponsored and/or assisted in providing samples from DRC, Malawi, Mozambique, and Uganda. WWF Gabon supported fieldwork in Gabon, as did the Partenariat Mozambique-Réunion dans la Recherche en Santé: pour une approche intégrée d’étude des maladies infectieuses à risque épidémique (MoZaR; Fond Européen de Développement Régional, Programme Opérationnel de Coopération Territoriale) in Mozambique. We thank Ara Monadjem and Daniela Rossoni for reviews of an earlier draft of this manuscript.

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Appendices

Appendix I

Genetic sampling of Hipposideridae. Wherever possible, the voucher numbers associated with the genetic samples are specified. Accession numbers identify sequences downloaded from GenBank or accessioned to Genbank for this study. The designation 'redundant' indicates a cyt-b sequence that was omitted from the 303 individual alignment because of its identity to another. Institutional acronyms are as follows: AMNH – American Museum of Natural History, New York; CM – Carnegie Museum, Pittsburgh; CVVD – ?; DM – Durban Natural Science Museum, Durban; EBD – Estación Biológica de Doñana, Sevilla; FMNH – Field Museum of Natural History, Chicago; IEBR-T – Thong collection at Institute of Ecology and Biological Resources, Hanoi; IVB – Institute of Vertebrate Biology, Brno; KU – Biodiversity Institute and Natural History Museum, University of Kansas, Lawrence; Czech Academy of Sciences, Prague; LSUMZ – Lousiana State University Museum of Natural Science-Mammal Tissues, Baton Rouge; NHMOU – Natural History Museum of Osmania University, Hyderabad; NMK – National Museums of Kenya, Nairobi; NMP – National Museum, Prague; PSUZC – Princess Maha Chakri Sirindhorn Natural History Museum, Songkhla; ROM – Royal Ontario Museum, Toronto; SMF – Senckenberg Museum, Frankfurt; TM – Transvaal Museum, Pretoria; TTU – Texas Tech University Museum, Lubbock; UADBA – Université d'Antananarivo, Département de Biologie Animale, Antananarivo; UNIMAS – University of Malaysia Sarawak Natural History Museum, Kuching.
Vouchercyt-bACOX2COPSROGDISTAT5ScientificNameCountryLatitudeLongitude
KU316954AselliaarabicaOman17.10054.080
KU316958AselliaitalosomalicaYemen12.67054.120
JF438999AselliatridensLibya24.93310.167
IEBR-TKU161572AselliscusdongbacanaVietnam22.360105.395
LC426460AselliscusstoliczkanusChina
DQ888675AselliscustricuspidatusVanuatu-15.307166.926
DM 8021FJ457616CloeotispercivaliSwaziland-25.81731.283
DM 8026FJ457615CloeotispercivaliSwaziland-25.81731.283
DQ888674CoelopsfrithiTaiwan21.948120.780
FMNH 148981redundantDoryrhinacamerunensisBurundi-2.10029.383
FMNH 148982MT149719MT149615MT149513MT149418MT149317DoryrhinacamerunensisBurundi-2.85029.400
NMK 187403redundantMT149616MT149514MT149419MT149318DoryrhinacamerunensisKenya0.34434.857
NMK 187418MT149720DoryrhinacamerunensisKenya0.34434.857
FMNH 165159MT149721DoryrhinacamerunensisUganda1.68331.533
FMNH 165160MT149722DoryrhinacamerunensisUganda1.68331.533
FMNH 223198MT149723DoryrhinacamerunensisUganda0.44532.889
FMNH 223551redundantMT149617MT149515MT149420MT149319DoryrhinacamerunensisUganda0.44532.889
FMNH 224066MT149724DoryrhinacamerunensisUganda0.50130.426
FMNH 224068MT149725DoryrhinacamerunensisUganda0.50130.426
FMNH 153929MT149726MT149618MT149516MT149421MT149320Doryrhinacf.camerunensisTanzania-4.94238.733
DM 12626KF551833Doryrhina cyclops1Liberia7.553-8.492
IVB S261EU934465Doryrhina cyclops1Senegal12.883-12.717
IVB S747EU934466Doryrhina cyclops1Senegal13.333-13.217
FMNH 227409MT149727MT149619MT149517MT149422MT149321Doryrhina cyclops2Central African Republic13.03316.410
FMNH 227410MT149728MT149620MT149518MT149423MT149322Doryrhina cyclops2Central African Republic3.03316.410
FMNH 167772MT149729MT149621MT149519MT149424MT149323Doryrhina cyclops2Gabon-2.28310.497
FMNH 167773MT149730MT149622MT149520MT149425MT149324Doryrhina cyclops2Gabon-2.28310.497
NMP 91850EU934446HipposiderosabaeBenin7.7832.267
NMP 91851EU934447HipposiderosabaeBenin7.7832.267
IVB S822EU934448HipposiderosabaeSenegal12.350-12.317
IEBR-T 90806.7JN247006HipposiderosalongensisVietnam
YN07C123JX849159HipposiderosarmigerChina23.600102.002
UNIMAS 729EF108140 redundantHipposiderosaterMalaysia1.407110.169
UNIMAS 1577EF108139 redundantHipposiderosaterMalaysia3.801113.785
KU 164242MT149731MT149623MT149521MT149426MT149325HipposiderosaterPhilippines13.796120.159
KU 164243MT149732MT149624MT149522MT149427MT149326HipposiderosaterPhilippines13.796120.159
KU 164712MT149733MT149625MT149523MT149428MT149327HipposiderosaterPhilippines19.085121.241
ROM 100579FJ347975Hipposideros beatus1Ivory Coast6.930-7.217
DM 13241KF551829Hipposideros beatus1Liberia7.553-8.492
DM 13242KF551830Hipposideros beatus1Liberia7.553-8.492
FMNH 227406MT149734MT149613MT149524MT149429MT149328Hipposideros beatus2Central African Republic3.03316.410
FMNH 149406FJ347976Hipposideros beatus2Democratic Republic of Congo-1.41728.583
FMNH 215440MT149735MT149626MT149525MT149430MT149329Hipposideros beatus2Kenya0.35234.865
NMK 184861MT149736MT149627MT149526MT149431MT149330Hipposideros beatus2Kenya0.35634.861
NMK 184864redundantHipposideros beatus2Kenya0.36034.861
NMK 184870MT149737Hipposideros beatus2Kenya0.35234.865
FMNH 192931MT149738Hipposideros beatus2Tanzania-1.09431.515
FMNH 192932MT149739Hipposideros beatus2Tanzania-1.09431.515
FMNH 192933redundantMT149628MT149527MT149432MT149331Hipposideros beatus2Tanzania-1.09431.515
FMNH 164972MT149740Hipposideros beatus2Uganda1.73331.467
FMNH 165157redundantMT149629MT149528MT149433MT149332Hipposideros beatus2Uganda1.68331.533
LSUMZ MT-4482MT149741MT149630MT149529MT149434MT149333HipposiderosbicolorMalaysia1.970103.500
LSUMZ MT-4489MT149742MT149631MT149530MT149334HipposiderosbicolorMalaysia1.970103.500
FMNH 215441redundantMT149632MT149531MT149435MT149335Hipposideros caffer1Kenya-0.34636.119
FMNH 215442redundantHipposideros caffer1Kenya-0.34636.119
FMNH 215443redundantHipposideros caffer1Kenya-0.34636.119
FMNH 215444MT149743Hipposideros caffer1Kenya-0.34636.119
FMNH 215445redundantHipposideros caffer1Kenya-0.34636.119
FMNH 215446redundantHipposideros caffer1Kenya-0.34636.119
FMNH 215447redundantHipposideros caffer1Kenya-0.34636.119
FMNH 216628redundantHipposideros caffer1Kenya-0.34636.119
FMNH 216629redundantHipposideros caffer1Kenya-0.34636.119
FMNH 216630redundantHipposideros caffer1Kenya-0.34636.119
FMNH 216631redundantHipposideros caffer1Kenya-0.34636.119
FMNH 216632redundantHipposideros caffer1Kenya-0.34636.119
FMNH 216645redundantHipposideros caffer1Kenya-0.34636.119
FMNH 216646redundantHipposideros caffer1Kenya-0.34636.119
FMNH 216647redundantHipposideros caffer1Kenya-0.34636.119
FMNH 216648redundantMT149633MT149532MT149436MT149336Hipposideros caffer1Kenya-0.34636.119
FMNH 225346redundantHipposideros caffer1Kenya-0.34636.119
FMNH 225747redundantHipposideros caffer1Kenya-0.56436.254
FMNH 225748redundantHipposideros caffer1Kenya-0.56436.254
FMNH 225749redundantHipposideros caffer1Kenya-0.56436.254
FMNH 225750redundantHipposideros caffer1Kenya-0.56436.254
FMNH 225751redundantHipposideros caffer1Kenya-0.56436.254
NMK 184726MT149744Hipposideros caffer1Kenya-0.56436.254
NMK 184727redundantHipposideros caffer1Kenya-0.56436.254
NMK 184728redundantHipposideros caffer1Kenya-0.56436.254
NMK 184729redundantHipposideros caffer1Kenya-0.56436.254
NMK 184730MT149745Hipposideros caffer1Kenya-0.56436.254
NMK 184760redundantHipposideros caffer1Kenya-0.43036.174
NMK 184842redundantHipposideros caffer1Kenya-0.53936.294
NMK 184843redundantHipposideros caffer1Kenya-0.53936.294
NMK 187310MT149718Hipposideros caffer1Kenya-0.53936.294
NMK 187311redundantHipposideros caffer1Kenya-0.53936.294
NMK 187312redundantHipposideros caffer1Kenya-0.53936.294
NMK 187323redundantHipposideros caffer1Kenya-0.34636.119
NMK 187324redundantHipposideros caffer1Kenya-0.34636.119
NMK 187325redundantMT149634MT149533MT149437MT149337Hipposideros caffer1Kenya-0.34636.119
NMK 187326redundantHipposideros caffer1Kenya-0.34636.119
EBD 23262FJ347977Hipposideros caffer1Morocco30.6309.830
NMPEU934449Hipposideros caffer1Morocco3.801113.785
FMNH 223196MT149746MT149635MT149534MT149438MT149338Hipposideros caffer1Uganda0.44532.889
FMNH 223197MT149747Hipposideros caffer1Uganda0.44532.889
NMPEU934463Hipposideros caffer1Yemen15.28344.167
FMNH 220955redundantMT149639MT149538MT149441MT149342Hipposideros caffer2Kenya-2.20337.714
FMNH 220956redundantHipposideros caffer2Kenya-2.20337.714
FMNH 220957MT149753Hipposideros caffer2Kenya-2.20337.714
FMNH 220958redundantHipposideros caffer2Kenya-2.20337.714
FMNH 225347redundantMT149640MT149539MT149442MT149343Hipposideros caffer2Kenya-1.54735.306
FMNH 225348redundantHipposideros caffer2Kenya-1.53135.320
FMNH 225349MT149754Hipposideros caffer2Kenya-1.53135.320
FMNH 225350MT149755MT149641MT149540MT149443Hipposideros caffer2Kenya-1.53135.320
FMNH 225351MT149756Hipposideros caffer2Kenya-1.53135.320
FMNH 225352redundantHipposideros caffer2Kenya-1.53135.320
NMK 184977MT149749Hipposideros caffer2Kenya-0.11734.541
NMK 184978MT149750MT149637MT149536MT149440MT149340Hipposideros caffer2Kenya-0.11734.541
NMK 184979MT149751Hipposideros caffer2Kenya-0.11734.541
NMK 184981redundantHipposideros caffer2Kenya-0.11734.541
NMK 184982MT149752MT149638MT149537MT149341Hipposideros caffer2Kenya-0.11734.541
NMK 184999MT149748MT149636MT149535MT149439MT149339Hipposideros caffer2Kenya-0.55537.388
FMNH 215914MT149768Hipposideros caffer3Kenya-3.70638.776
FMNH 215915redundantHipposideros caffer3Kenya-3.70638.776
FMNH 215916MT149769Hipposideros caffer3Kenya-3.70638.776
FMNH 215917redundantMT149646MT149545MT149448MT149348Hipposideros caffer3Kenya-3.70638.776
FMNH 215918redundantHipposideros caffer3Kenya-3.70638.776
FMNH 215921redundantHipposideros caffer3Kenya-3.07639.217
FMNH 215922MT149770Hipposideros caffer3Kenya-3.07639.217
FMNH 215923MT149771Hipposideros caffer3Kenya-3.07639.217
FMNH 215924redundantHipposideros caffer3Kenya-3.07639.217
FMNH 215925MT149772MT149647MT149546MT149449MT149349Hipposideros caffer3Kenya-3.07639.217
FMNH 220648MT149766Hipposideros caffer3Kenya0.17038.194
FMNH 220669MT149767MT149645MT149544MT149447MT149347Hipposideros caffer3Kenya0.02438.066
FMNH 234022MT149757Hipposideros caffer3Kenya-1.01938.326
FMNH 234023MT149758Hipposideros caffer3Kenya-0.99238.330
NMK 184226MT149762MT149644MT149543MT149446MT149346Hipposideros caffer3Kenya2.32037.994
NMK 184238MT149763Hipposideros caffer3Kenya2.32037.994
NMK 184284MT149764Hipposideros caffer3Kenya2.32037.994
NMK 184287MT149765Hipposideros caffer3Kenya2.28337.954
NMK 184425MT149761MT149643MT149542MT149445MT149345Hipposideros caffer3Kenya0.22837.113
NMK 185050redundantMT149642MT149541MT149444MT149344Hipposideros caffer3Kenya-0.99238.330
NMK 185051redundantHipposideros caffer3Kenya-0.99238.330
NMK 185052MT149759Hipposideros caffer3Kenya-0.99238.330
NMK 185053redundantHipposideros caffer3Kenya-0.99238.330
NMK 185054MT149760Hipposideros caffer3Kenya-0.99238.330
DM 8587KF551805Hipposideros caffer4Mozambique-23.20532.499
DM 8590KF551810Hipposideros caffer4Mozambique-12.18237.550
TM 48051EU934451Hipposideros caffer4Mozambique-21.51735.100
DM 11007KF551806 redundantHipposideros caffer4South Africa-27.59632.220
FJ347979Hipposideros caffer4South Africa-27.66032.251
EU934452Hipposideros caffer4South Africa-23.99931.645
DM 7920EU934458Hipposideros caffer4Swaziland-26.87031.463
FMNH 215941redundantHipposideros caffer5Kenya-3.30039.995
FMNH 220176MT149780Hipposideros caffer5Kenya-4.59039.331
FMNH 220177MT149781Hipposideros caffer5Kenya-4.59039.331
FMNH 220178redundantHipposideros caffer5Kenya-4.59039.331
FMNH 220179MT149782Hipposideros caffer5Kenya-4.59039.331
FMNH 220180MT149783Hipposideros caffer5Kenya-4.59039.331
FMNH 220182MT149784Hipposideros caffer5Kenya-4.08239.483
FMNH 220183MT149785Hipposideros caffer5Kenya-4.08239.483
FMNH 220184MT149786Hipposideros caffer5Kenya-4.08239.483
FMNH 220185redundantHipposideros caffer5Kenya-4.08239.483
FMNH 220186redundantHipposideros caffer5Kenya-4.08239.483
FMNH 220202MT149773Hipposideros caffer5Kenya-3.30039.995
FMNH 220203redundantHipposideros caffer5Kenya-3.30039.995
FMNH 220204redundantMT149648MT149547MT149450MT149350Hipposideros caffer5Kenya-3.30039.995
FMNH 220205redundantHipposideros caffer5Kenya-3.32340.042
FMNH 220206MT149774Hipposideros caffer5Kenya-3.32340.042
FMNH 220207redundantMT149649MT149548MT149451MT149351Hipposideros caffer5Kenya-3.32340.042
FMNH 220208redundantMT149650MT149549MT149452MT149352Hipposideros caffer5Kenya-3.32340.042
FMNH 220209MT149775Hipposideros caffer5Kenya-3.32340.042
FMNH 233985redundantHipposideros caffer5Kenya-3.33540.031
NMK 187199MT149776Hipposideros caffer5Kenya-3.32340.042
NMK 187200redundantHipposideros caffer5Kenya-3.32340.042
NMK 187201MT149777Hipposideros caffer5Kenya-3.32340.042
NMK 187202MT149778Hipposideros caffer5Kenya-3.32340.042
NMK 187203MT149779Hipposideros caffer5Kenya-3.32340.042
CM 97957FJ347980Hipposideros caffer5Kenya-4.25039.383
FMNH 192789MT149787MT149651MT149550MT149453MT149353Hipposideros caffer5Tanzania-4.90239.688
FMNH 192855redundantMT149652MT149551MT149454MT149354Hipposideros caffer5Tanzania-4.90239.688
FMNH 187385redundantMT149653MT149552MT149455MT149355Hipposideros caffer6Tanzania-8.00339.762
FMNH 187386MT149788MT149654MT149553MT149456Hipposideros caffer6Tanzania-8.00339.762
FMNH 187387MT149789Hipposideros caffer6Tanzania-7.99339.792
FMNH 187388redundantHipposideros caffer6Tanzania-7.99339.792
FMNH 187417MT149790Hipposideros caffer6Tanzania-7.89139.843
FMNH 187418MT149791Hipposideros caffer6Tanzania-7.89139.843
FMNH 187426MT149792Hipposideros caffer6Tanzania-7.89139.843
FMNH 187428redundantHipposideros caffer6Tanzania-7.99339.792
FMNH 198066MT149793MT149655MT149554MT149457MT149356Hipposideros caffer6Tanzania-5.87839.311
FMNH 198067MT149794Hipposideros caffer6Tanzania-5.87839.311
FMNH 198072redundantMT149656MT149555MT149458MT149357Hipposideros caffer6Tanzania-6.24439.320
FMNH 198073redundantHipposideros caffer6Tanzania-6.24439.320
FMNH 198074MT149795MT149657MT149556MT149459MT149358Hipposideros caffer6Tanzania-6.24439.320
FMNH 198075MT149796Hipposideros caffer6Tanzania-6.24439.320
FMNH 198076redundantHipposideros caffer6Tanzania-6.24439.320
FMNH 198082redundantHipposideros caffer6Tanzania-6.28039.451
FMNH 198083MT149797Hipposideros caffer6Tanzania-6.28039.451
FMNH 198084MT149798Hipposideros caffer6Tanzania-6.28039.451
FMNH 198131redundantHipposideros caffer6Tanzania-5.87839.311
FMNH 198132MT149799Hipposideros caffer6Tanzania-5.87839.311
FMNH 198133MT149800Hipposideros caffer6Tanzania-5.87839.311
NMPEU934460Hipposideros caffer6Tanzania-5.99839.187
NMPEU934477Hipposideros caffer7Malawi-16.03335.500
DM 8528KF551817Hipposideros caffer7Mozambique-13.40134.870
DM 8550KF551816 redundantHipposideros caffer7Mozambique-13.40134.870
FMNH 155554MT149801MT149658MT149557MT149460MT149359Hipposideros caffer7Tanzania-8.51935.904
FMNH 192790redundantMT149659MT149558MT149461MT149360Hipposideros caffer7Tanzania-4.90239.688
FMNH 192792MT149802Hipposideros caffer7Tanzania-5.36739.645
FMNH 192793redundantHipposideros caffer7Tanzania-5.36739.645
FMNH 192794redundantHipposideros caffer7Tanzania-5.36739.645
FMNH 192795redundantHipposideros caffer7Tanzania-5.36739.645
FMNH 192796MT149803Hipposideros caffer7Tanzania-5.36739.645
FMNH 192849MT149804MT149660MT149559MT149462MT149361Hipposideros caffer7Tanzania-4.90239.688
FMNH 187140MT149805MT149661MT149560MT149463MT149362Hipposideros caffer8Tanzania-3.79836.069
FMNH 219065MT149806MT149662MT149561MT149464MT149363Hipposideros caffer8Tanzania-8.03734.502
FMNH 219241MT149807Hipposideros caffer8Tanzania-8.03734.502
FMNH 219242MT149808Hipposideros caffer8Tanzania-7.70734.031
FMNH 232868redundantHipposideros caffer8Uganda2.24031.688
FMNH 232869MT149809MT149663MT149562MT149465MT149364Hipposideros caffer8Uganda2.24031.688
FMNH 232874redundantMT149664MT149563MT149416MT149365Hipposideros caffer8Uganda2.24031.688
FMNH 232875MT149810MT149665MT149564MT149366Hipposideros caffer8Uganda2.24031.688
LSUMZ MT-4480redundantMT149666MT149466MT149367HipposideroscervinusMalaysia1.970103.500
LSUMZ MT-4481MT149811MT149667MT149565MT149467MT149368HipposideroscervinusMalaysia1.970103.500
LSUMZ MT-4500MT149812MT149668MT149566MT149468MT149369HipposideroscervinusMalaysia1.970103.500
UNIMAS 787EF108144HipposideroscervinusMalaysia3.316113.125
UNIMAS 788EF108146HipposideroscervinusMalaysia3.316113.125
LSUMZ MT-4495MT149813MT149669MT149469MT149370Hipposideroscf.bicolorMalaysia1.970103.500
UNIMAS 1459EF108142Hipposideroscf.bicolorMalaysia1.716110.467
UNIMAS 1474EF108143Hipposideroscf.bicolorMalaysia1.716110.467
FMNH 235856MT149814MT149670MT149567MT149470MT149371Hipposideroscf.cervinusSolomon Islands-10.569161.913
FMNH 235857MT149815MT149671MT149568MT149471MT149372Hipposideroscf.cervinusSolomon Islands-10.569161.913
NMP 91848EU934474Hipposideroscf.lamotteiBenin7.7832.267
NMP 91849EU934475Hipposideroscf.lamotteiBenin7.7832.267
IVB S862EU934453Hipposideroscf.lamotteiSenegal12.350-12.317
IVB PV56HQ343266Hipposideroscf.ruberGhana7.668-1.962
DM 12598KF551812Hipposideroscf.ruberLiberia7.553-8.492
DM 12620KF551811Hipposideroscf.ruberLiberia7.553-8.492
IVB S119EU934478Hipposideroscf.ruberSenegal13.050-13.083
IVB S132HQ343242Hipposideroscf.ruberSenegal14.071-12.572
IVB S1374EU934479Hipposideroscf.ruberSenegal13.250-13.217
IVB S8HQ343240Hipposideroscf.ruberSenegal12.884-12.755
LSUMZ MT-4423DQ054809HipposideroscineraceusMalaysia3.717102.167
FMNH 190042JQ915701HipposideroscoronatusPhilippines9.097125.705
FMNH 202631JQ915702HipposideroscoronatusPhilippines9.764124.266
KU 166444MT149672MT149472MT149373HipposideroscoronatusPhilippines11.813125.278
EF108148HipposideroscoxiMalaysia1.378110.120
EF108147 redundantHipposideroscoxiMalaysia1.378110.120
UNIMAS 1424EF108149HipposiderosdiademaMalaysia5.531118.072
KU 164028MT149816MT149673MT149569MT149473MT149374HipposiderosdiademaPhilippines19.331121.439
KU 164029MT149817MT149674MT149570MT149474MT149375HipposiderosdiademaPhilippines19.331121.439
KU 164245MT149818MT149675MT149571MT149475HipposiderosdiademaPhilippines13.796120.159
FJ460489HipposiderosdoriaeMalaysia1.117110.217
NHMOU.CHI MP4.2016KY176014HipposiderosdurgadasiIndia23.31778.414
UNIMAS 312EF108150HipposiderosdyacorumMalaysia4.401117.889
UNIMAS 556EF108151HipposiderosdyacorumMalaysia3.316113.125
EU934468HipposiderosfuliginosusGuinea Bissau11.117-14.933
EU934467HipposiderosfuliginosusGuinea Bissau11.333-13.900
JX849198HipposiderosgriffiniVietnam
CVVD AG200700214JN247005HipposideroshalophyllusThailand
NMP 91842EU934471HipposiderosjonesiBenin7.7832.267
IVB S804EU934472HipposiderosjonesiSenegal12.350-12.317
EU934473HipposiderosjonesiSenegal12.350-12.317
EBD 23514DQ054816HipposideroskhaokhouayensisLaos18.433102.950
KF551824HipposideroslamotteiGuinea7.570-8.471
KF551823HipposideroslamotteiGuinea7.570-8.471
NHMOU.CHI MP15.2016KY176015HipposideroslankadivaIndia23.31778.414
LSUMZ MT-4478MT149819MT149676MT149572MT149476MT149376HipposideroslarvatusMalaysia1.970103.500
LSUMZ MT-4479redundantMT149677MT149573MT149377HipposideroslarvatusMalaysia1.970103.500
LSUMZ MT-4488MT149820MT149678MT149574MT149477MT149378HipposideroslarvatusMalaysia1.970103.500
UNIMAS 1485EF108152 redundantHipposideroslarvatusMalaysia1.717110.467
UNIMAS 1501EF108153HipposideroslarvatusMalaysia1.717110.467
FMNH 195507JQ915904HipposideroslekaguliPhilippines16.314121.394
KR908661HipposideroslyleiChina25.60399.752
DM 12607KF551825HipposiderosmarisaeLiberia7.553-8.492
FMNH 140601JQ915906HipposiderosobscurusPhilippines13.767124.350
KU 165040redundantMT149679MT149575MT149379HipposiderosobscurusPhilippines11.434122.079
KU 165041MT149821MT149680MT149576MT149478MT149380HipposiderosobscurusPhilippines11.434122.079
KU 165226MT149717MT149577MT149479MT149381HipposiderosobscurusPhilippines13.447120.426
PSUZC MM2006.129JN247029HipposiderospendelburyiThailand7.56599.624
DQ054810HipposiderospomonaLaos18.250104.517
EU434952HipposiderosprattiChina27.729115.734
FMNH 190070JQ915992HipposiderospygmaeusPhilippines9.097125.705
KU 164542MT149822MT149681MT149578MT149480MT149382HipposiderospygmaeusPhilippines14.823121.968
KU 164543redundantMT149682MT149579MT149481MT149383HipposiderospygmaeusPhilippines14.823121.968
KU 164544MT149716MT149683MT149580MT149482MT149384HipposiderospygmaeusPhilippines14.823121.968
LSUMZ MT-4425MT149715MT149684MT149581MT149483MT149385HipposiderosridleyiMalaysia3.557102.761
LSUMZ MT-4477MT149823MT149582MT149484MT149386HipposiderosridleyiMalaysia3.557102.761
SMF 83828DQ054811HipposiderosridleyiMalaysia3.717102.167
DQ054813HipposiderosrotalisLaos18.250104.517
FJ347996Hipposideros ruber1Cameroon3.15013.000
FJ347995Hipposideros ruber1Cameroon4.45111.571
FJ347993Hipposideros ruber1Cameroon3.56413.408
FJ347992Hipposideros ruber1Cameroon3.56413.408
FJ347989Hipposideros ruber1Cameroon5.38511.688
FMNH 195085MT149824MT149685MT149583MT149485MT149387Hipposideros ruber1D. R. Congo-4.99129.080
FMNH 215448MT149826Hipposideros ruber1Kenya1.03634.753
FMNH 215449MT149827Hipposideros ruber1Kenya1.03634.753
FMNH 215450redundantHipposideros ruber1Kenya1.03634.753
FMNH 215451redundantHipposideros ruber1Kenya1.03634.753
FMNH 215452redundantHipposideros ruber1Kenya1.03634.753
FMNH 215453redundantHipposideros ruber1Kenya1.03634.753
FMNH 215476MT149828Hipposideros ruber1Kenya1.03634.753
FMNH 215477redundantHipposideros ruber1Kenya1.03634.753
FMNH 215478redundantHipposideros ruber1Kenya1.03634.753
NMK 184904MT149825MT149686MT149584MT149486Hipposideros ruber1Kenya0.21234.899
NMK 184905redundantHipposideros ruber1Kenya0.21234.899
NMK 187407redundantHipposideros ruber1Kenya1.03634.753
NMK 187408MT149829Hipposideros ruber1Kenya1.03634.753
NMK 187409MT149830MT149687MT149585MT149487MT149388Hipposideros ruber1Kenya1.03634.753
NMK 187410redundantHipposideros ruber1Kenya1.03634.753
NMK 187412MT149831Hipposideros ruber1Kenya1.03634.753
DM 12603KF551819Hipposideros ruber1Liberia7.553-8.492
DM 13245KF551815Hipposideros ruber1Liberia7.553-8.492
DM 13246KF551820Hipposideros ruber1Liberia7.553-8.492
FMNH 225201MT149832MT149688MT149586MT149488MT149389Hipposideros ruber1Rwanda-2.48529.199
FMNH 225202MT149833Hipposideros ruber1Rwanda-1.50429.613
FMNH 225203redundantHipposideros ruber1Rwanda-1.50429.613
FMNH 225204redundantHipposideros ruber1Rwanda-1.50629.615
FMNH 225205redundantHipposideros ruber1Rwanda-1.50629.615
FMNH 225206MT149834Hipposideros ruber1Rwanda-1.50629.615
FMNH 225207redundantHipposideros ruber1Rwanda-1.50629.615
FMNH 225208MT149835MT149689MT149587MT149489MT149390Hipposideros ruber1Rwanda-1.50629.615
FMNH 225209redundantHipposideros ruber1Rwanda-1.50629.615
FMNH 192935MT149836MT149690MT149588MT149490MT149391Hipposideros ruber1Tanzania-1.09431.515
FMNH 137629FJ347987Hipposideros ruber1Uganda32.283-0.005
FMNH 160358MT149837Hipposideros ruber1Uganda-0.98929.614
FMNH 160359MT149838MT149691MT149589MT149491MT149392Hipposideros ruber1Uganda-0.98929.614
FMNH 160361MT149839Hipposideros ruber1Uganda-1.04129.580
FMNH 161040MT149840Hipposideros ruber1Uganda-0.24529.819
FMNH 223866redundantMT149692MT149590MT149492MT149393Hipposideros ruber1Uganda-0.34231.966
FMNH 223867MT149841Hipposideros ruber1Uganda-0.34231.966
FMNH 227415MT149842Hipposideros ruber2Central African Republic3.03316.410
FMNH 227416MT149843Hipposideros ruber2Central African Republic3.03316.410
FMNH 227417MT149844MT149693MT149591MT149394Hipposideros ruber2Central African Republic3.03316.410
FMNH 149408FJ347986MT149694MT149592MT149493MT149395Hipposideros ruber2D. R. Congo-1.41728.583
FMNH 149409redundantHipposideros ruber2D. R. Congo-1.41728.583
FMNH 149410redundantMT149695MT149593MT149494MT149396Hipposideros ruber2D. R. Congo-1.41728.583
FMNH 149412redundantHipposideros ruber2D. R. Congo-1.41728.583
ROM 100546FJ347978Hipposideros ruber2Ivory Coast6.930-7.217
FMNH 215479redundantHipposideros ruber2Kenya0.24434.907
FMNH 215480MT149845Hipposideros ruber2Kenya0.24434.907
FMNH 215481MT149846Hipposideros ruber2Kenya0.24434.907
FMNH 215482redundantMT149696MT149594MT149495MT149397Hipposideros ruber2Kenya0.24434.907
FMNH 215483redundantMT149697MT149595MT149496MT149398Hipposideros ruber2Kenya0.24434.907
NMK 184878MT149847Hipposideros ruber2Kenya0.24834.906
NMK 184880MT149848Hipposideros ruber2Kenya0.24834.906
NMK 184882MT149849Hipposideros ruber2Kenya0.24834.906
NMK 184883MT149850Hipposideros ruber2Kenya0.24834.906
NMK 184884MT149851Hipposideros ruber2Kenya0.24834.906
NMK 187383redundantHipposideros ruber2Kenya0.21234.899
NMK 187384MT149852Hipposideros ruber2Kenya0.21234.899
FMNH 165161redundantHipposideros ruber2Uganda1.73331.467
FMNH 165162MT149853Hipposideros ruber2Uganda1.68331.533
FMNH 165163redundantMT149698MT149596MT149497MT149399Hipposideros ruber2Uganda1.68331.533
FMNH 165164MT149854Hipposideros ruber2Uganda1.68331.533
FMNH 165165MT149855Hipposideros ruber2Uganda1.68331.533
FMNH 165166redundantHipposideros ruber2Uganda1.75031.583
FMNH 165167redundantMT149699MT149597MT149498MT149400Hipposideros ruber2Uganda1.73331.467
FMNH 224069redundantHipposideros ruber2Uganda0.50130.426
FMNH 224071redundantHipposideros ruber2Uganda0.50130.426
FMNH 224074MT149856Hipposideros ruber2Uganda0.50130.426
FMNH 224075MT149857Hipposideros ruber2Uganda0.50130.426
FJ347994Hipposideros ruber3Cameroon3.56413.408
FJ347991Hipposideros ruber3Cameroon2.9419.911
FJ347990Hipposideros ruber3Cameroon2.9419.911
FJ347988Hipposideros ruber3Cameroon4.9139.241
EBD 18240FJ347984Hipposideros ruber3Equatorial Guinea1.8899.793
EBD 18266FJ347985Hipposideros ruber3Equatorial Guinea1.8899.793
EBD 18511FJ347983Hipposideros ruber3Equatorial Guinea3.7478.750
EBD 18942FJ347981Hipposideros ruber3Principe1.6157.404
EBD 18926FJ347982Hipposideros ruber3São Tomé0.2196.727
FMNH 219477MT149858MT149700MT149598MT149499MT149401Hipposideros ruber4D. R. Congo-5.29014.871
FMNH 169707KT583815MacronycteriscommersoniMadagascar-12.93249.057
FMNH 175777KT583822MacronycteriscommersoniMadagascar-16.38045.345
FMNH 175966KT583823MacronycteriscommersoniMadagascar-22.48645.392
FMNH 175974MT149859MacronycteriscommersoniMadagascar-22.31745.293
FMNH 175975MT149860MacronycteriscommersoniMadagascar-22.31745.293
FMNH 176155KT583824MT149701MT149599MT149500MT149402MacronycteriscommersoniMadagascar-22.77843.523
FMNH 176158MT149861MacronycteriscommersoniMadagascar-22.21743.330
FMNH 176277redundantMacronycteriscommersoniMadagascar-12.94249.055
FMNH 177302KT583825MacronycteriscommersoniMadagascar-16.31546.810
FMNH 178803redundantMacronycteriscommersoniMadagascar-12.71249.474
FMNH 178806KT583816MacronycteriscommersoniMadagascar-12.71249.474
FMNH 178808KT583817 redundantMacronycteriscommersoniMadagascar-12.71249.474
FMNH 178809KT583818MacronycteriscommersoniMadagascar-12.71249.474
FMNH 178810KT583819MacronycteriscommersoniMadagascar-12.71249.474
FMNH 178811KT583820MacronycteriscommersoniMadagascar-12.71249.474
FMNH 178812KT583826MacronycteriscommersoniMadagascar-12.71249.474
FMNH 178815KT583821 redundantMacronycteriscommersoniMadagascar-12.71249.474
FMNH 179201MT149862MacronycteriscommersoniMadagascar-17.28049.420
FMNH 183934KT583827MacronycteriscommersoniMadagascar-24.05043.750
FMNH 183980KT583813 redundantMacronycteriscommersoniMadagascar-12.33749.385
FMNH 184030KT583812MacronycteriscommersoniMadagascar-14.96647.308
FMNH 184170KT583828MacronycteriscommersoniMadagascar-24.65043.963
FMNH 184887MT149863MacronycteriscommersoniMadagascar-15.90446.598
FMNH 209236MT149864MacronycteriscommersoniMadagascar-18.06344.541
FMNH 217940KT583831 redundantMacronycteriscommersoniMadagascar-22.63245.338
FMNH 221308KT583829MacronycteriscommersoniMadagascar-12.93249.057
FMNH 231862MT149865MT149702MT149600MT149501MT149315MacronycteriscommersoniMadagascar-17.88949.203
UADBA 32916KT583830MacronycteriscommersoniMadagascar15.53846.886
UADBA 32987KT583814MacronycteriscommersoniMadagascar-13.93249.057
UADBA 32989KR606333MacronycteriscommersoniMadagascar-12.91749.143
FMNH 175970MT149866MT149703MT149601MT149502MT149403MacronycteriscryptovaloronaMadagascar-22.31745.293
FMNH 184173MT149867MT149704MT149602MT149503MT149404MacronycteriscryptovaloronaMadagascar-24.65043.963
AMNH 269871KT583801MacronycterisgigasCentral African Republic
FMNH 219602MT149868MT149705MT149603MT149504MT149405MacronycterisgigasD. R. Congo0.24120.883
FMNH 219682MT149869MT149706MT149604MT149415MT149406MacronycterisgigasD. R. Congo0.24120.883
FMNH 220226redundantMT149707MT149605MT149505MT149407MacronycterisgigasKenya-4.64739.380
FMNH 220227redundantMT149708MT149606MT149506MT149408MacronycterisgigasKenya-4.64739.380
FMNH 220239MT149870MacronycterisgigasKenya-4.21539.451
DM 12602KF551826MacronycterisgigasLiberia7.553-8.492
IVB S1032EU934469MacronycterisgigasSenegal12.350-13.217
IVB S1044EU934470MacronycterisgigasSenegal12.350-13.217
AMNH 269879KT583802MacronycterisvittataCentral African Republic3.50016.000
FMNH 215942MT149871MT149709MT149607MT149507MT149409MacronycterisvittataKenya-3.30039.995
FMNH 215943redundantMacronycterisvittataKenya-3.30039.995
FMNH 215944redundantMacronycterisvittataKenya-3.30039.995
FMNH 215945redundantMacronycterisvittataKenya-3.30039.995
FMNH 215946MT149872MacronycterisvittataKenya-3.28739.982
FMNH 215947redundantMacronycterisvittataKenya-3.28739.982
FMNH 215948MT149873MacronycterisvittataKenya-3.28739.982
FMNH 215949redundantMacronycterisvittataKenya-3.28739.982
FMNH 215950MT149874MacronycterisvittataKenya-3.28739.982
FMNH 215951MT149875MacronycterisvittataKenya-3.28239.971
FMNH 215952MT149876MacronycterisvittataKenya-3.28239.971
FMNH 215953redundantMT149710MT149608MT149410MacronycterisvittataKenya-3.28239.971
FMNH 215954MT149877MacronycterisvittataKenya-3.28239.971
FMNH 215955redundantMacronycterisvittataKenya-3.28239.971
FMNH 215959MT149878MacronycterisvittataKenya-3.30940.018
FMNH 215960MT149879MacronycterisvittataKenya-3.30940.018
FMNH 215961MT149880MacronycterisvittataKenya-3.30940.018
FMNH 215962MT149881MacronycterisvittataKenya-3.30940.018
FMNH 215963MT149882MacronycterisvittataKenya-3.30940.018
FMNH 215967MT149883MacronycterisvittataKenya-3.30339.999
FMNH 215968redundantMacronycterisvittataKenya-3.30539.937
FMNH 215969redundantMacronycterisvittataKenya-3.30539.937
FMNH 220224redundantMacronycterisvittataKenya-4.64739.378
FMNH 220225MT149885MacronycterisvittataKenya-4.64739.380
FMNH 220228MT149886MacronycterisvittataKenya-4.64739.380
FMNH 220229MT149887MT149711MT149609MT149508MT149411MacronycterisvittataKenya-4.64739.380
FMNH 220231MT149888MacronycterisvittataKenya-4.61439.354
FMNH 220232MT149889MacronycterisvittataKenya-4.61439.354
FMNH 220233MT149890MacronycterisvittataKenya-4.61439.354
FMNH 220234redundantMacronycterisvittataKenya-4.61439.354
FMNH 220235MT149891MT149712MT149610MT149509MT149412MacronycterisvittataKenya-4.61439.354
FMNH 220236redundantMacronycterisvittataKenya-4.61439.354
FMNH 220237redundantMacronycterisvittataKenya-4.61439.354
FMNH 220238redundantMacronycterisvittataKenya-4.61439.354
FMNH 220240redundantMacronycterisvittataKenya-3.30039.995
NMK 187219redundantMacronycterisvittataKenya-3.33540.031
NMK 187220MT149884MacronycterisvittataKenya-3.33540.031
NMK 187221redundantMacronycterisvittataKenya-3.33540.031
NMK 187222redundantMacronycterisvittataKenya-3.33540.031
DM 8645KF551828 redundantMacronycterisvittataMozambique-18.56532.220
DM 11510KF551827MacronycterisvittataMozambique-18.97834.176
FMNH 192800redundantMT149713MT149611MT149510MT149413MacronycterisvittataTanzania-4.90239.688
FMNH 192801MT149892MacronycterisvittataTanzania-4.90239.688
FMNH 192857redundantMT149714MT149612MT149511MT149414MacronycterisvittataTanzania-4.90239.688
FMNH 192858redundantMacronycterisvittataTanzania-4.90239.688
FMNH 192859MT149893MacronycterisvittataTanzania-4.90239.688
FMNH 192860KT583807MacronycterisvittataTanzania-4.90239.688
FMNH 192865KT583808 redundantMacronycterisvittataTanzania-4.90239.688
FMNH 192866KT583809MacronycterisvittataTanzania-4.90239.688
FMNH 220268MT149614MT149512MT149417MT149316TriaenopsaferKenya-4.59039.331
https://www.researchpad.co/tools/openurl?pubtype=article&doi=10.3897/zookeys.929.50240&title=Evolutionary relationships and population genetics of the Afrotropical leaf-nosed bats (, )&author=Bruce D. Patterson,Paul W. Webala,Tyrone H. Lavery,Bernard R. Agwanda,Steven M. Goodman,Julian C. Kerbis Peterhans,Terrence C. Demos,&keyword=cryptic species,mtDNA,nuclear introns,Paleotropical,phylogeny,species delimitation,systematics,&subject=Research Article,Animalia,Chiroptera,Chordata,Hipposideridae,Mammalia,Placentalia,Theria,Vertebrata,Biogeography,Cenozoic,Neogene,Africa,Asia,Australasia,Central Africa,East Africa,Southern Africa,West Africa,