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Research Article
Evolutionary relationships and population genetics of the Afrotropical leaf-nosed bats (Chiroptera, Hipposideridae)
expand article infoBruce D. Patterson, Paul W. Webala§, Tyrone H. Lavery|, Bernard R. Agwanda, Steven M. Goodman#, Julian C. Kerbis Peterhans¤, Terrence C. Demos
‡ Field Museum of Natural History, Chicago, United States of America
§ Maasai Mara University, Narok, Kenya
| The Australian National University, Canberra, Australia
¶ National Museums of Kenya, Nairobi, Kenya
# National Museums of Kenya, Antananarivo, Madagascar
¤ Roosevelt University, Chicago, United States of America
Open Access

Abstract

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.

Keywords

cryptic species, mtDNA, nuclear introns, Paleotropical, phylogeny, species delimitation, systematics

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: †Macronycteris besaoka (Madagascar), †Hipposideros amenhotepos (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: Hipposideros abae J. A. Allen,1917; †Hipposideros (Pseudorhinolophus) amenhotepos Gunnell, Winkler, Miller, Head, El-Barkooky, Gawad, Sanders & Gingerich, 2015; Phyllorhina angolensis Seabra, 1898; Hipposideros caffer var. aurantiaca De Beaux, 1924; Hipposideros beatus K. Andersen, 1906; †Hipposideros besaoka Samonds, 2007; Phyllorrhina bicornis Heuglin, 1861; Hipposideros braima Monard, 1939; Hipposideros caffer Sundevall, 1846; Phyllorhina caffra Peters, 1852; Hipposideros camerunensis Eisentraut, 1956; Hipposideros caffer centralis K. Andersen, 1906; Rhinolophus Commersonii É. Geoffroy, 1813; Hipposideros cryptovalorona Goodman, Schoeman, Rakotoarivelo & Willows-Munro, 2016; Hipposideros curtus G. M. Allen, 1921; Phyllorrhina cyclops Temminck, 1853; Phyllorrhina fuliginosa Temminck, 1853; Hipposideros gigas gambiensis K. Andersen, 1906; Rhinolophus gigas Wagner, 1845; Phyllorrhina gracilis Peters, 1852; Hipposideros caffer guineensis K. Andersen, 1906; Hipposideros jonesi Hayman, 1947; †Hipposideros kaumbului Wesselman, 1984; Hipposideros lamottei Brosset, 1985; Hipposideros langi J. A. Allen, 1917; Hipposideros marisae Aellen, 1954; Phyllorhina Commersoni, var. marungensis Noack, 1887; Hipposideros beatus maximus Verschuren, 1957; Phyllorrhina megalotis Heuglin, 1861; Rhinolophus micaceus de Winton, 1897; Hipposideros Commersoni mostellum Thomas, 1904; Hipposideros nanus J. A. Allen, 1917; Hipposideros gigas niangarae J. A. Allen, 1917; Hipposideros caffer niapu J. A. Allen, 1917; Phyllorrhina rubra Noack, 1893; Hipposideros sandersoni Sanderson, 1937; Hipposideros tephrus Cabrera, 1906; Phyllorhina Commersoni, var. thomensis Bocage, 1891; Hipposideros gigas viegasi Monard, 1939; Phyllorhina vittata 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 group calcaratus subgroup H. macrobullatus H. lankadiva
H. alongensis H. calcaratus c H. maggietaylorae H. lekaguli
H. armiger H. cervinus c H. nequam H. pelingensis
H. griffini a H. coxi c H. obscurus Larvatus group
H. pendelburyi a H. galeritus c H. orbiculus H. grandis
H. turpis ruber subgroup H. papua H. khasiana” a,g
Bicolor group H. abae d H. pygmaeus H. larvatus
ater subgroup H. beatus e Boeadii group H. madurae
H. ater b H. caffer e H. boeadii H. sorenseni
H. atrox a H. fuliginosus e Cyclops group f H. sumbae
H. bicolor b H. lamottei e H. corynophyllus Megalotis group
H. breviceps b H. ruber e H. edwardshilli H. megalotis
H. cineraceus b H. tephrus a,e H. muscinus Pratti group
H. coronatus b subgroup uncertain H. semoni H. lylei
H. dyacorum b H. cruminiferus H. stenotis H. pratti
H. einnaythu a,b H. curtus H. wollastoni H. scutinares
H. halophyllus b H. doriae Diadema group Speoris group
H. khaokhouayensis b H. durgadasi H. demissus H. jonesi h
H. nicobarulae a,b H. fulvus H. diadema H. marisae g
H. pomona b H. gentilis a H. dinops H. speoris
H. ridleyi b H. hypophyllus H. inexpectatus
H. rotalis b H. kunzi a H. inornatus

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 Hipposideros lamottei (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 Hipposideros caffer 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 Triaenops afer (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) Hipposideros caffer1–4; (4) Hipposideros caffer5–8; and (5) Hipposideros ruber1–4.

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 name Sequence Primer publication Substitution model
ACOX2-3-F 5’-CCTSGGCTCDGAGGAGCAGAT-3’ Salicini et al. 2011 K80+G / K81+G
ACOX2-3-R 5’-GGGCTGTGHAYCACAAACTCCT-3’
COPS7A-4-F 5’-TACAGCATYGGRCGRGACATCCA-3’ Salicini et al. 2011 HKY / K80
COPS7A-4-R 5’-TCACYTGCTCCTCRATGCCKGACA-3’
ROGDI-7-F 5’-CTGATGGAYGCYGTGATGCTGCA-3’ Salicini et al. 2011 K80+G / K81+G
ROGDI-7-R 5’-CACGGTGAGGCASAGCTTGTTGA-3’
STAT5B-16-F 5’--CTGCTCATCAACAAGCCCGA-3’ Matthee et al. 2001 GTR+G / K81+G
STAT5B-16-R 5’-GGCTTCAGGTTCCACAGGTTGC-3’
cyt-b-LGL-765-F 5’-GGCTTCAGGTTCCACAGGTTGC-3’ Trujillo et al. 2009 GTR+I+G
cyt-b -LGL-766-R 5’-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.

PS Effective pop. size Divergence depth Gamma distribution for prior
1 Large Deep θ = Γ [1, 10] and τ = Γ [1, 10]
2 Large Shallow θ = Γ [1, 10] and τ = Γ [2, 2000]
3 Small Shallow θ = Γ [2, 2000] and τ = Γ [2, 2000]
4 Small Deep θ = 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 Hipposideros caffer 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] Doryrhina camerunensis 0.003
[2] Doryrhina cf. camerunensis 0.055 na
[3] Doryrhina cyclops 1 0.057 0.048 0.008
[4] Doryrhina cyclops 2 0.055 0.041 0.030 0.006
[5] Hipposideros abae 0.176 0.173 0.168 0.166 0.033
[6] Hipposideros beatus 1 0.152 0.156 0.160 0.152 0.116 0.007
[7] Hipposideros beatus 2 0.146 0.149 0.151 0.147 0.117 0.044 0.006
[8] Hipposideros caffer 1 0.157 0.154 0.150 0.148 0.108 0.103 0.106 0.006
[9] Hipposideros caffer 2 0.153 0.150 0.150 0.147 0.106 0.096 0.108 0.045 0.01
[10] Hipposideros caffer 3 0.152 0.148 0.150 0.149 0.108 0.110 0.111 0.046 0.052 0.011
[11] Hipposideros caffer 4 0.162 0.159 0.160 0.154 0.106 0.105 0.114 0.077 0.078 0.079 0.018
[12] Hipposideros caffer 5 0.150 0.155 0.159 0.148 0.113 0.091 0.096 0.095 0.101 0.103 0.098 0.005
[13] Hipposideros caffer 6 0.155 0.156 0.164 0.153 0.112 0.093 0.102 0.090 0.097 0.099 0.094 0.028 0.011
[14] Hipposideros caffer 7 0.151 0.154 0.161 0.148 0.108 0.084 0.094 0.094 0.094 0.098 0.096 0.025 0.032 0.011
[15] Hipposideros caffer 8 0.154 0.155 0.160 0.152 0.111 0.090 0.092 0.092 0.095 0.102 0.093 0.033 0.039 0.029 0.021
[16] Hipposideros fuliginosus 0.155 0.149 0.154 0.142 0.101 0.095 0.096 0.078 0.084 0.087 0.094 0.088 0.086 0.080 0.085
[17] Hipposideros jonesi 0.153 0.143 0.154 0.147 0.160 0.145 0.138 0.135 0.140 0.140 0.139 0.134 0.134 0.137 0.139
[18] Hipposideros lamottei 0.171 0.173 0.174 0.163 0.106 0.097 0.118 0.094 0.086 0.095 0.097 0.057 0.059 0.052 0.060
[19] Hipposideros cf. lamottei 0.158 0.158 0.156 0.149 0.107 0.103 0.107 0.091 0.099 0.095 0.097 0.053 0.058 0.052 0.054
[20] Hipposideros marisae 0.177 0.180 0.178 0.172 0.159 0.153 0.153 0.144 0.148 0.140 0.152 0.148 0.144 0.154 0.159
[21] Hipposideros ruber 1 0.155 0.151 0.152 0.142 0.104 0.099 0.101 0.081 0.084 0.085 0.086 0.090 0.081 0.082 0.082
[22] Hipposideros ruber 2 0.155 0.155 0.156 0.142 0.103 0.097 0.102 0.081 0.082 0.089 0.089 0.086 0.078 0.083 0.081
[23] Hipposideros ruber 3 0.159 0.149 0.155 0.147 0.105 0.094 0.101 0.084 0.082 0.096 0.088 0.090 0.083 0.082 0.082
[24] Hipposideros ruber 4 0.153 0.147 0.151 0.141 0.100 0.094 0.097 0.073 0.073 0.085 0.082 0.083 0.077 0.078 0.078
[25] Hipposideros cf. ruber 0.164 0.161 0.161 0.153 0.099 0.094 0.100 0.086 0.084 0.095 0.093 0.081 0.080 0.080 0.083
[26] Macronycteris commersoni 0.157 0.156 0.155 0.145 0.164 0.159 0.154 0.164 0.169 0.168 0.171 0.166 0.170 0.167 0.162
[27] Macronycteris cryptovalorona 0.147 0.143 0.147 0.142 0.157 0.152 0.146 0.156 0.162 0.161 0.165 0.159 0.164 0.158 0.157
[28] Macronycteris gigas 0.151 0.149 0.154 0.144 0.164 0.163 0.158 0.162 0.168 0.165 0.170 0.165 0.171 0.164 0.165
[29] Macronycteris vittata 0.147 0.148 0.149 0.140 0.162 0.158 0.147 0.160 0.161 0.166 0.165 0.164 0.169 0.164 0.163
Table 4.

Continued.

[16] [17] [18] [19] [20] [21] [22] [23] [24] [25] [26] [27] [28] [29]
[16] Hipposideros fuliginosus 0.003
[17] Hipposideros jonesi 0.137 0.008
[18] Hipposideros lamottei 0.100 0.161 0.038
[19] Hipposideros cf. lamottei 0.091 0.142 0.054 0.006
[20] Hipposideros marisae 0.145 0.092 0.156 0.158 na
[21] Hipposideros ruber 1 0.082 0.144 0.093 0.087 0.152 0.013
[22] Hipposideros ruber 2 0.084 0.147 0.093 0.091 0.157 0.030 0.007
[23] Hipposideros ruber 3 0.082 0.142 0.085 0.088 0.158 0.052 0.057 0.022
[24] Hipposideros ruber 4 0.078 0.140 0.087 0.088 0.154 0.053 0.051 0.057 na
[25] Hipposideros cf. ruber 0.084 0.142 0.094 0.089 0.157 0.081 0.081 0.082 0.072 0.033
[26] Macronycteris commersoni 0.155 0.186 0.183 0.167 0.193 0.163 0.162 0.161 0.168 0.174 0.012
[27] Macronycteris cryptovalorona 0.149 0.176 0.170 0.163 0.185 0.161 0.161 0.158 0.160 0.162 0.028 0.003
[28] Macronycteris gigas 0.153 0.179 0.178 0.169 0.190 0.165 0.165 0.161 0.165 0.169 0.026 0.029 0.012
[29] Macronycteris vittata 0.150 0.181 0.180 0.168 0.192 0.158 0.159 0.158 0.159 0.164 0.026 0.029 0.027 0.006

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.

Figure 2. 

Continued.

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 A Doryrhina B Macronycteris.

Figure 4. 

Substitution network plots for Afrotropical hipposiderids A Hipposideros caffer clades 1–4 B Hipposideros caffer clades 5–8 C H. 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. halophyllus H. dyacorum, H. ridley, and H. durgadasi. This group is sister to all analyzed members of the ruber subgroup: the various clades allied with Hipposideros beatus, 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 Hipposideros caffer (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 Species PS1 PS2 PS3 PS4
Doryrhina camerunensis 0.30 0.76 0.95 0.51
D. cf. camerunensis 0.32 0.73 0.97 0.79
D. cyclops 2 0.23 0.68 0.95 0.51
Hipposideros beatus 2 1 1 1 1
H. caffer 1 0.99 0.99 0.99 0.99
H. caffer 2 0.99 1 1 1
H. caffer 3 0.99 0.99 0.99 0.99
H. caffer 5 0.14 0.18 0.11 0.08
H. caffer 6 0.56 0.61 0.85 0.82
H. caffer 7 0.14 0.18 0.11 0.08
H. caffer 8 0.99 0.99 0.99 0.99
H. ruber 1 0.99 0.99 0.99 0.99
H. ruber 2 1 0.99 1 0.99
H. ruber 4 0.99 0.99 0.99 0.99
Macronycteris commersoni 0.24 0.72 0.94 0.52
M. cryptovalorona 0.35 0.81 0.97 0.76
M. gigas 0.09 0.43 0.91 0.38
M. vittata 0.11 0.44 0.90 0.34

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 Hipposideros tephrus (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
A1 H. caffer caffer 4
A1a H. caffer caffer 4
A1b H. caffer caffer 4
A2 H. caffer H. caffer tephrus caffer 1
B H. ruber caffer 5
B1 H. ruber cf. lamottei
B2 H. ruber caffer 7
C1 H. ruber ruber 1, ruber 2
C1a H. cf. ruber ruber 1
C1b H. cf. ruber ruber 1
C2 H. ruber C2 H. cf. ruber ruber 3
ruber 4
D H. ruber H. cf. ruber cf. ruber
D1 H. cf. ruber cf. ruber
D2 H. cf. ruber cf. ruber
E1 H. cf. ruber cf. ruber
E2 H. cf. ruber cf. ruber
caffer 2
caffer 3
caffer 6
caffer 8
abae H. abae abae H. abae abae
beatus H. beatus beatus H. beatus beatus1, beatus 2
fuliginosus H. fuliginosus fuliginosus H. fuliginosus fuliginosus
lamottei H. lamottei lamottei H. lamottei lamottei

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. Macronycteris cryptovalorona 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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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.

Voucher cyt-b ACOX2 COPS ROGDI STAT5 ScientificName Country Latitude Longitude
KU316954 Asellia arabica Oman 17.100 54.080
KU316958 Asellia italosomalica Yemen 12.670 54.120
JF438999 Asellia tridens Libya 24.933 10.167
IEBR-T KU161572 Aselliscus dongbacana Vietnam 22.360 105.395
LC426460 Aselliscus stoliczkanus China
DQ888675 Aselliscus tricuspidatus Vanuatu -15.307 166.926
DM 8021 FJ457616 Cloeotis percivali Swaziland -25.817 31.283
DM 8026 FJ457615 Cloeotis percivali Swaziland -25.817 31.283
DQ888674 Coelops frithi Taiwan 21.948 120.780
FMNH 148981 redundant Doryrhina camerunensis Burundi -2.100 29.383
FMNH 148982 MT149719 MT149615 MT149513 MT149418 MT149317 Doryrhina camerunensis Burundi -2.850 29.400
NMK 187403 redundant MT149616 MT149514 MT149419 MT149318 Doryrhina camerunensis Kenya 0.344 34.857
NMK 187418 MT149720 Doryrhina camerunensis Kenya 0.344 34.857
FMNH 165159 MT149721 Doryrhina camerunensis Uganda 1.683 31.533
FMNH 165160 MT149722 Doryrhina camerunensis Uganda 1.683 31.533
FMNH 223198 MT149723 Doryrhina camerunensis Uganda 0.445 32.889
FMNH 223551 redundant MT149617 MT149515 MT149420 MT149319 Doryrhina camerunensis Uganda 0.445 32.889
FMNH 224066 MT149724 Doryrhina camerunensis Uganda 0.501 30.426
FMNH 224068 MT149725 Doryrhina camerunensis Uganda 0.501 30.426
FMNH 153929 MT149726 MT149618 MT149516 MT149421 MT149320 Doryrhina cf. camerunensis Tanzania -4.942 38.733
DM 12626 KF551833 Doryrhina cyclops1 Liberia 7.553 -8.492
IVB S261 EU934465 Doryrhina cyclops1 Senegal 12.883 -12.717
IVB S747 EU934466 Doryrhina cyclops1 Senegal 13.333 -13.217
FMNH 227409 MT149727 MT149619 MT149517 MT149422 MT149321 Doryrhina cyclops2 Central African Republic 13.033 16.410
FMNH 227410 MT149728 MT149620 MT149518 MT149423 MT149322 Doryrhina cyclops2 Central African Republic 3.033 16.410
FMNH 167772 MT149729 MT149621 MT149519 MT149424 MT149323 Doryrhina cyclops2 Gabon -2.283 10.497
FMNH 167773 MT149730 MT149622 MT149520 MT149425 MT149324 Doryrhina cyclops2 Gabon -2.283 10.497
NMP 91850 EU934446 Hipposideros abae Benin 7.783 2.267
NMP 91851 EU934447 Hipposideros abae Benin 7.783 2.267
IVB S822 EU934448 Hipposideros abae Senegal 12.350 -12.317
IEBR-T 90806.7 JN247006 Hipposideros alongensis Vietnam
YN07C123 JX849159 Hipposideros armiger China 23.600 102.002
UNIMAS 729 EF108140 redundant Hipposideros ater Malaysia 1.407 110.169
UNIMAS 1577 EF108139 redundant Hipposideros ater Malaysia 3.801 113.785
KU 164242 MT149731 MT149623 MT149521 MT149426 MT149325 Hipposideros ater Philippines 13.796 120.159
KU 164243 MT149732 MT149624 MT149522 MT149427 MT149326 Hipposideros ater Philippines 13.796 120.159
KU 164712 MT149733 MT149625 MT149523 MT149428 MT149327 Hipposideros ater Philippines 19.085 121.241
ROM 100579 FJ347975 Hipposideros beatus1 Ivory Coast 6.930 -7.217
DM 13241 KF551829 Hipposideros beatus1 Liberia 7.553 -8.492
DM 13242 KF551830 Hipposideros beatus1 Liberia 7.553 -8.492
FMNH 227406 MT149734 MT149613 MT149524 MT149429 MT149328 Hipposideros beatus2 Central African Republic 3.033 16.410
FMNH 149406 FJ347976 Hipposideros beatus2 Democratic Republic of Congo -1.417 28.583
FMNH 215440 MT149735 MT149626 MT149525 MT149430 MT149329 Hipposideros beatus2 Kenya 0.352 34.865
NMK 184861 MT149736 MT149627 MT149526 MT149431 MT149330 Hipposideros beatus2 Kenya 0.356 34.861
NMK 184864 redundant Hipposideros beatus2 Kenya 0.360 34.861
NMK 184870 MT149737 Hipposideros beatus2 Kenya 0.352 34.865
FMNH 192931 MT149738 Hipposideros beatus2 Tanzania -1.094 31.515
FMNH 192932 MT149739 Hipposideros beatus2 Tanzania -1.094 31.515
FMNH 192933 redundant MT149628 MT149527 MT149432 MT149331 Hipposideros beatus2 Tanzania -1.094 31.515
FMNH 164972 MT149740 Hipposideros beatus2 Uganda 1.733 31.467
FMNH 165157 redundant MT149629 MT149528 MT149433 MT149332 Hipposideros beatus2 Uganda 1.683 31.533
LSUMZ MT-4482 MT149741 MT149630 MT149529 MT149434 MT149333 Hipposideros bicolor Malaysia 1.970 103.500
LSUMZ MT-4489 MT149742 MT149631 MT149530 MT149334 Hipposideros bicolor Malaysia 1.970 103.500
FMNH 215441 redundant MT149632 MT149531 MT149435 MT149335 Hipposideros caffer1 Kenya -0.346 36.119
FMNH 215442 redundant Hipposideros caffer1 Kenya -0.346 36.119
FMNH 215443 redundant Hipposideros caffer1 Kenya -0.346 36.119
FMNH 215444 MT149743 Hipposideros caffer1 Kenya -0.346 36.119
FMNH 215445 redundant Hipposideros caffer1 Kenya -0.346 36.119
FMNH 215446 redundant Hipposideros caffer1 Kenya -0.346 36.119
FMNH 215447 redundant Hipposideros caffer1 Kenya -0.346 36.119
FMNH 216628 redundant Hipposideros caffer1 Kenya -0.346 36.119
FMNH 216629 redundant Hipposideros caffer1 Kenya -0.346 36.119
FMNH 216630 redundant Hipposideros caffer1 Kenya -0.346 36.119
FMNH 216631 redundant Hipposideros caffer1 Kenya -0.346 36.119
FMNH 216632 redundant Hipposideros caffer1 Kenya -0.346 36.119
FMNH 216645 redundant Hipposideros caffer1 Kenya -0.346 36.119
FMNH 216646 redundant Hipposideros caffer1 Kenya -0.346 36.119
FMNH 216647 redundant Hipposideros caffer1 Kenya -0.346 36.119
FMNH 216648 redundant MT149633 MT149532 MT149436 MT149336 Hipposideros caffer1 Kenya -0.346 36.119
FMNH 225346 redundant Hipposideros caffer1 Kenya -0.346 36.119
FMNH 225747 redundant Hipposideros caffer1 Kenya -0.564 36.254
FMNH 225748 redundant Hipposideros caffer1 Kenya -0.564 36.254
FMNH 225749 redundant Hipposideros caffer1 Kenya -0.564 36.254
FMNH 225750 redundant Hipposideros caffer1 Kenya -0.564 36.254
FMNH 225751 redundant Hipposideros caffer1 Kenya -0.564 36.254
NMK 184726 MT149744 Hipposideros caffer1 Kenya -0.564 36.254
NMK 184727 redundant Hipposideros caffer1 Kenya -0.564 36.254
NMK 184728 redundant Hipposideros caffer1 Kenya -0.564 36.254
NMK 184729 redundant Hipposideros caffer1 Kenya -0.564 36.254
NMK 184730 MT149745 Hipposideros caffer1 Kenya -0.564 36.254
NMK 184760 redundant Hipposideros caffer1 Kenya -0.430 36.174
NMK 184842 redundant Hipposideros caffer1 Kenya -0.539 36.294
NMK 184843 redundant Hipposideros caffer1 Kenya -0.539 36.294
NMK 187310 MT149718 Hipposideros caffer1 Kenya -0.539 36.294
NMK 187311 redundant Hipposideros caffer1 Kenya -0.539 36.294
NMK 187312 redundant Hipposideros caffer1 Kenya -0.539 36.294
NMK 187323 redundant Hipposideros caffer1 Kenya -0.346 36.119
NMK 187324 redundant Hipposideros caffer1 Kenya -0.346 36.119
NMK 187325 redundant MT149634 MT149533 MT149437 MT149337 Hipposideros caffer1 Kenya -0.346 36.119
NMK 187326 redundant Hipposideros caffer1 Kenya -0.346 36.119
EBD 23262 FJ347977 Hipposideros caffer1 Morocco 30.630 9.830
NMP EU934449 Hipposideros caffer1 Morocco 3.801 113.785
FMNH 223196 MT149746 MT149635 MT149534 MT149438 MT149338 Hipposideros caffer1 Uganda 0.445 32.889
FMNH 223197 MT149747 Hipposideros caffer1 Uganda 0.445 32.889
NMP EU934463 Hipposideros caffer1 Yemen 15.283 44.167
FMNH 220955 redundant MT149639 MT149538 MT149441 MT149342 Hipposideros caffer2 Kenya -2.203 37.714
FMNH 220956 redundant Hipposideros caffer2 Kenya -2.203 37.714
FMNH 220957 MT149753 Hipposideros caffer2 Kenya -2.203 37.714
FMNH 220958 redundant Hipposideros caffer2 Kenya -2.203 37.714
FMNH 225347 redundant MT149640 MT149539 MT149442 MT149343 Hipposideros caffer2 Kenya -1.547 35.306
FMNH 225348 redundant Hipposideros caffer2 Kenya -1.531 35.320
FMNH 225349 MT149754 Hipposideros caffer2 Kenya -1.531 35.320
FMNH 225350 MT149755 MT149641 MT149540 MT149443 Hipposideros caffer2 Kenya -1.531 35.320
FMNH 225351 MT149756 Hipposideros caffer2 Kenya -1.531 35.320
FMNH 225352 redundant Hipposideros caffer2 Kenya -1.531 35.320
NMK 184977 MT149749 Hipposideros caffer2 Kenya -0.117 34.541
NMK 184978 MT149750 MT149637 MT149536 MT149440 MT149340 Hipposideros caffer2 Kenya -0.117 34.541
NMK 184979 MT149751 Hipposideros caffer2 Kenya -0.117 34.541
NMK 184981 redundant Hipposideros caffer2 Kenya -0.117 34.541
NMK 184982 MT149752 MT149638 MT149537 MT149341 Hipposideros caffer2 Kenya -0.117 34.541
NMK 184999 MT149748 MT149636 MT149535 MT149439 MT149339 Hipposideros caffer2 Kenya -0.555 37.388
FMNH 215914 MT149768 Hipposideros caffer3 Kenya -3.706 38.776
FMNH 215915 redundant Hipposideros caffer3 Kenya -3.706 38.776
FMNH 215916 MT149769 Hipposideros caffer3 Kenya -3.706 38.776
FMNH 215917 redundant MT149646 MT149545 MT149448 MT149348 Hipposideros caffer3 Kenya -3.706 38.776
FMNH 215918 redundant Hipposideros caffer3 Kenya -3.706 38.776
FMNH 215921 redundant Hipposideros caffer3 Kenya -3.076 39.217
FMNH 215922 MT149770 Hipposideros caffer3 Kenya -3.076 39.217
FMNH 215923 MT149771 Hipposideros caffer3 Kenya -3.076 39.217
FMNH 215924 redundant Hipposideros caffer3 Kenya -3.076 39.217
FMNH 215925 MT149772 MT149647 MT149546 MT149449 MT149349 Hipposideros caffer3 Kenya -3.076 39.217
FMNH 220648 MT149766 Hipposideros caffer3 Kenya 0.170 38.194
FMNH 220669 MT149767 MT149645 MT149544 MT149447 MT149347 Hipposideros caffer3 Kenya 0.024 38.066
FMNH 234022 MT149757 Hipposideros caffer3 Kenya -1.019 38.326
FMNH 234023 MT149758 Hipposideros caffer3 Kenya -0.992 38.330
NMK 184226 MT149762 MT149644 MT149543 MT149446 MT149346 Hipposideros caffer3 Kenya 2.320 37.994
NMK 184238 MT149763 Hipposideros caffer3 Kenya 2.320 37.994
NMK 184284 MT149764 Hipposideros caffer3 Kenya 2.320 37.994
NMK 184287 MT149765 Hipposideros caffer3 Kenya 2.283 37.954
NMK 184425 MT149761 MT149643 MT149542 MT149445 MT149345 Hipposideros caffer3 Kenya 0.228 37.113
NMK 185050 redundant MT149642 MT149541 MT149444 MT149344 Hipposideros caffer3 Kenya -0.992 38.330
NMK 185051 redundant Hipposideros caffer3 Kenya -0.992 38.330
NMK 185052 MT149759 Hipposideros caffer3 Kenya -0.992 38.330
NMK 185053 redundant Hipposideros caffer3 Kenya -0.992 38.330
NMK 185054 MT149760 Hipposideros caffer3 Kenya -0.992 38.330
DM 8587 KF551805 Hipposideros caffer4 Mozambique -23.205 32.499
DM 8590 KF551810 Hipposideros caffer4 Mozambique -12.182 37.550
TM 48051 EU934451 Hipposideros caffer4 Mozambique -21.517 35.100
DM 11007 KF551806 redundant Hipposideros caffer4 South Africa -27.596 32.220
FJ347979 Hipposideros caffer4 South Africa -27.660 32.251
EU934452 Hipposideros caffer4 South Africa -23.999 31.645
DM 7920 EU934458 Hipposideros caffer4 Swaziland -26.870 31.463
FMNH 215941 redundant Hipposideros caffer5 Kenya -3.300 39.995
FMNH 220176 MT149780 Hipposideros caffer5 Kenya -4.590 39.331
FMNH 220177 MT149781 Hipposideros caffer5 Kenya -4.590 39.331
FMNH 220178 redundant Hipposideros caffer5 Kenya -4.590 39.331
FMNH 220179 MT149782 Hipposideros caffer5 Kenya -4.590 39.331
FMNH 220180 MT149783 Hipposideros caffer5 Kenya -4.590 39.331
FMNH 220182 MT149784 Hipposideros caffer5 Kenya -4.082 39.483
FMNH 220183 MT149785 Hipposideros caffer5 Kenya -4.082 39.483
FMNH 220184 MT149786 Hipposideros caffer5 Kenya -4.082 39.483
FMNH 220185 redundant Hipposideros caffer5 Kenya -4.082 39.483
FMNH 220186 redundant Hipposideros caffer5 Kenya -4.082 39.483
FMNH 220202 MT149773 Hipposideros caffer5 Kenya -3.300 39.995
FMNH 220203 redundant Hipposideros caffer5 Kenya -3.300 39.995
FMNH 220204 redundant MT149648 MT149547 MT149450 MT149350 Hipposideros caffer5 Kenya -3.300 39.995
FMNH 220205 redundant Hipposideros caffer5 Kenya -3.323 40.042
FMNH 220206 MT149774 Hipposideros caffer5 Kenya -3.323 40.042
FMNH 220207 redundant MT149649 MT149548 MT149451 MT149351 Hipposideros caffer5 Kenya -3.323 40.042
FMNH 220208 redundant MT149650 MT149549 MT149452 MT149352 Hipposideros caffer5 Kenya -3.323 40.042
FMNH 220209 MT149775 Hipposideros caffer5 Kenya -3.323 40.042
FMNH 233985 redundant Hipposideros caffer5 Kenya -3.335 40.031
NMK 187199 MT149776 Hipposideros caffer5 Kenya -3.323 40.042
NMK 187200 redundant Hipposideros caffer5 Kenya -3.323 40.042
NMK 187201 MT149777 Hipposideros caffer5 Kenya -3.323 40.042
NMK 187202 MT149778 Hipposideros caffer5 Kenya -3.323 40.042
NMK 187203 MT149779 Hipposideros caffer5 Kenya -3.323 40.042
CM 97957 FJ347980 Hipposideros caffer5 Kenya -4.250 39.383
FMNH 192789 MT149787 MT149651 MT149550 MT149453 MT149353 Hipposideros caffer5 Tanzania -4.902 39.688
FMNH 192855 redundant MT149652 MT149551 MT149454 MT149354 Hipposideros caffer5 Tanzania -4.902 39.688
FMNH 187385 redundant MT149653 MT149552 MT149455 MT149355 Hipposideros caffer6 Tanzania -8.003 39.762
FMNH 187386 MT149788 MT149654 MT149553 MT149456 Hipposideros caffer6 Tanzania -8.003 39.762
FMNH 187387 MT149789 Hipposideros caffer6 Tanzania -7.993 39.792
FMNH 187388 redundant Hipposideros caffer6 Tanzania -7.993 39.792
FMNH 187417 MT149790 Hipposideros caffer6 Tanzania -7.891 39.843
FMNH 187418 MT149791 Hipposideros caffer6 Tanzania -7.891 39.843
FMNH 187426 MT149792 Hipposideros caffer6 Tanzania -7.891 39.843
FMNH 187428 redundant Hipposideros caffer6 Tanzania -7.993 39.792
FMNH 198066 MT149793 MT149655 MT149554 MT149457 MT149356 Hipposideros caffer6 Tanzania -5.878 39.311
FMNH 198067 MT149794 Hipposideros caffer6 Tanzania -5.878 39.311
FMNH 198072 redundant MT149656 MT149555 MT149458 MT149357 Hipposideros caffer6 Tanzania -6.244 39.320
FMNH 198073 redundant Hipposideros caffer6 Tanzania -6.244 39.320
FMNH 198074 MT149795 MT149657 MT149556 MT149459 MT149358 Hipposideros caffer6 Tanzania -6.244 39.320
FMNH 198075 MT149796 Hipposideros caffer6 Tanzania -6.244 39.320
FMNH 198076 redundant Hipposideros caffer6 Tanzania -6.244 39.320
FMNH 198082 redundant Hipposideros caffer6 Tanzania -6.280 39.451
FMNH 198083 MT149797 Hipposideros caffer6 Tanzania -6.280 39.451
FMNH 198084 MT149798 Hipposideros caffer6 Tanzania -6.280 39.451
FMNH 198131 redundant Hipposideros caffer6 Tanzania -5.878 39.311
FMNH 198132 MT149799 Hipposideros caffer6 Tanzania -5.878 39.311
FMNH 198133 MT149800 Hipposideros caffer6 Tanzania -5.878 39.311
NMP EU934460 Hipposideros caffer6 Tanzania -5.998 39.187
NMP EU934477 Hipposideros caffer7 Malawi -16.033 35.500
DM 8528 KF551817 Hipposideros caffer7 Mozambique -13.401 34.870
DM 8550 KF551816 redundant Hipposideros caffer7 Mozambique -13.401 34.870
FMNH 155554 MT149801 MT149658 MT149557 MT149460 MT149359 Hipposideros caffer7 Tanzania -8.519 35.904
FMNH 192790 redundant MT149659 MT149558 MT149461 MT149360 Hipposideros caffer7 Tanzania -4.902 39.688
FMNH 192792 MT149802 Hipposideros caffer7 Tanzania -5.367 39.645
FMNH 192793 redundant Hipposideros caffer7 Tanzania -5.367 39.645
FMNH 192794 redundant Hipposideros caffer7 Tanzania -5.367 39.645
FMNH 192795 redundant Hipposideros caffer7 Tanzania -5.367 39.645
FMNH 192796 MT149803 Hipposideros caffer7 Tanzania -5.367 39.645
FMNH 192849 MT149804 MT149660 MT149559 MT149462 MT149361 Hipposideros caffer7 Tanzania -4.902 39.688
FMNH 187140 MT149805 MT149661 MT149560 MT149463 MT149362 Hipposideros caffer8 Tanzania -3.798 36.069
FMNH 219065 MT149806 MT149662 MT149561 MT149464 MT149363 Hipposideros caffer8 Tanzania -8.037 34.502
FMNH 219241 MT149807 Hipposideros caffer8 Tanzania -8.037 34.502
FMNH 219242 MT149808 Hipposideros caffer8 Tanzania -7.707 34.031
FMNH 232868 redundant Hipposideros caffer8 Uganda 2.240 31.688
FMNH 232869 MT149809 MT149663 MT149562 MT149465 MT149364 Hipposideros caffer8 Uganda 2.240 31.688
FMNH 232874 redundant MT149664 MT149563 MT149416 MT149365 Hipposideros caffer8 Uganda 2.240 31.688
FMNH 232875 MT149810 MT149665 MT149564 MT149366 Hipposideros caffer8 Uganda 2.240 31.688
LSUMZ MT-4480 redundant MT149666 MT149466 MT149367 Hipposideros cervinus Malaysia 1.970 103.500
LSUMZ MT-4481 MT149811 MT149667 MT149565 MT149467 MT149368 Hipposideros cervinus Malaysia 1.970 103.500
LSUMZ MT-4500 MT149812 MT149668 MT149566 MT149468 MT149369 Hipposideros cervinus Malaysia 1.970 103.500
UNIMAS 787 EF108144 Hipposideros cervinus Malaysia 3.316 113.125
UNIMAS 788 EF108146 Hipposideros cervinus Malaysia 3.316 113.125
LSUMZ MT-4495 MT149813 MT149669 MT149469 MT149370 Hipposideros cf. bicolor Malaysia 1.970 103.500
UNIMAS 1459 EF108142 Hipposideros cf. bicolor Malaysia 1.716 110.467
UNIMAS 1474 EF108143 Hipposideros cf. bicolor Malaysia 1.716 110.467
FMNH 235856 MT149814 MT149670 MT149567 MT149470 MT149371 Hipposideros cf. cervinus Solomon Islands -10.569 161.913
FMNH 235857 MT149815 MT149671 MT149568 MT149471 MT149372 Hipposideros cf. cervinus Solomon Islands -10.569 161.913
NMP 91848 EU934474 Hipposideros cf. lamottei Benin 7.783 2.267
NMP 91849 EU934475 Hipposideros cf. lamottei Benin 7.783 2.267
IVB S862 EU934453 Hipposideros cf. lamottei Senegal 12.350 -12.317
IVB PV56 HQ343266 Hipposideros cf. ruber Ghana 7.668 -1.962
DM 12598 KF551812 Hipposideros cf. ruber Liberia 7.553 -8.492
DM 12620 KF551811 Hipposideros cf. ruber Liberia 7.553 -8.492
IVB S119 EU934478 Hipposideros cf. ruber Senegal 13.050 -13.083
IVB S132 HQ343242 Hipposideros cf. ruber Senegal 14.071 -12.572
IVB S1374 EU934479 Hipposideros cf. ruber Senegal 13.250 -13.217
IVB S8 HQ343240 Hipposideros cf. ruber Senegal 12.884 -12.755
LSUMZ MT-4423 DQ054809 Hipposideros cineraceus Malaysia 3.717 102.167
FMNH 190042 JQ915701 Hipposideros coronatus Philippines 9.097 125.705
FMNH 202631 JQ915702 Hipposideros coronatus Philippines 9.764 124.266
KU 166444 MT149672 MT149472 MT149373 Hipposideros coronatus Philippines 11.813 125.278
EF108148 Hipposideros coxi Malaysia 1.378 110.120
EF108147 redundant Hipposideros coxi Malaysia 1.378 110.120
UNIMAS 1424 EF108149 Hipposideros diadema Malaysia 5.531 118.072
KU 164028 MT149816 MT149673 MT149569 MT149473 MT149374 Hipposideros diadema Philippines 19.331 121.439
KU 164029 MT149817 MT149674 MT149570 MT149474 MT149375 Hipposideros diadema Philippines 19.331 121.439
KU 164245 MT149818 MT149675 MT149571 MT149475 Hipposideros diadema Philippines 13.796 120.159
FJ460489 Hipposideros doriae Malaysia 1.117 110.217
NHMOU.CHI MP4.2016 KY176014 Hipposideros durgadasi India 23.317 78.414
UNIMAS 312 EF108150 Hipposideros dyacorum Malaysia 4.401 117.889
UNIMAS 556 EF108151 Hipposideros dyacorum Malaysia 3.316 113.125
EU934468 Hipposideros fuliginosus Guinea Bissau 11.117 -14.933
EU934467 Hipposideros fuliginosus Guinea Bissau 11.333 -13.900
JX849198 Hipposideros griffini Vietnam
CVVD AG 200700214 JN247005 Hipposideros halophyllus Thailand
NMP 91842 EU934471 Hipposideros jonesi Benin 7.783 2.267
IVB S804 EU934472 Hipposideros jonesi Senegal 12.350 -12.317
EU934473 Hipposideros jonesi Senegal 12.350 -12.317
EBD 23514 DQ054816 Hipposideros khaokhouayensis Laos 18.433 102.950
KF551824 Hipposideros lamottei Guinea 7.570 -8.471
KF551823 Hipposideros lamottei Guinea 7.570 -8.471
NHMOU.CHI MP15.2016 KY176015 Hipposideros lankadiva India 23.317 78.414
LSUMZ MT-4478 MT149819 MT149676 MT149572 MT149476 MT149376 Hipposideros larvatus Malaysia 1.970 103.500
LSUMZ MT-4479 redundant MT149677 MT149573 MT149377 Hipposideros larvatus Malaysia 1.970 103.500
LSUMZ MT-4488 MT149820 MT149678 MT149574 MT149477 MT149378 Hipposideros larvatus Malaysia 1.970 103.500
UNIMAS 1485 EF108152 redundant Hipposideros larvatus Malaysia 1.717 110.467
UNIMAS 1501 EF108153 Hipposideros larvatus Malaysia 1.717 110.467
FMNH 195507 JQ915904 Hipposideros lekaguli Philippines 16.314 121.394
KR908661 Hipposideros lylei China 25.603 99.752
DM 12607 KF551825 Hipposideros marisae Liberia 7.553 -8.492
FMNH 140601 JQ915906 Hipposideros obscurus Philippines 13.767 124.350
KU 165040 redundant MT149679 MT149575 MT149379 Hipposideros obscurus Philippines 11.434 122.079
KU 165041 MT149821 MT149680 MT149576 MT149478 MT149380 Hipposideros obscurus Philippines 11.434 122.079
KU 165226 MT149717 MT149577 MT149479 MT149381 Hipposideros obscurus Philippines 13.447 120.426
PSUZC MM2006.129 JN247029 Hipposideros pendelburyi Thailand 7.565 99.624
DQ054810 Hipposideros pomona Laos 18.250 104.517
EU434952 Hipposideros pratti China 27.729 115.734
FMNH 190070 JQ915992 Hipposideros pygmaeus Philippines 9.097 125.705
KU 164542 MT149822 MT149681 MT149578 MT149480 MT149382 Hipposideros pygmaeus Philippines 14.823 121.968
KU 164543 redundant MT149682 MT149579 MT149481 MT149383 Hipposideros pygmaeus Philippines 14.823 121.968
KU 164544 MT149716 MT149683 MT149580 MT149482 MT149384 Hipposideros pygmaeus Philippines 14.823 121.968
LSUMZ MT-4425 MT149715 MT149684 MT149581 MT149483 MT149385 Hipposideros ridleyi Malaysia 3.557 102.761
LSUMZ MT-4477 MT149823 MT149582 MT149484 MT149386 Hipposideros ridleyi Malaysia 3.557 102.761
SMF 83828 DQ054811 Hipposideros ridleyi Malaysia 3.717 102.167
DQ054813 Hipposideros rotalis Laos 18.250 104.517
FJ347996 Hipposideros ruber1 Cameroon 3.150 13.000
FJ347995 Hipposideros ruber1 Cameroon 4.451 11.571
FJ347993 Hipposideros ruber1 Cameroon 3.564 13.408
FJ347992 Hipposideros ruber1 Cameroon 3.564 13.408
FJ347989 Hipposideros ruber1 Cameroon 5.385 11.688
FMNH 195085 MT149824 MT149685 MT149583 MT149485 MT149387 Hipposideros ruber1 D. R. Congo -4.991 29.080
FMNH 215448 MT149826 Hipposideros ruber1 Kenya 1.036 34.753
FMNH 215449 MT149827 Hipposideros ruber1 Kenya 1.036 34.753
FMNH 215450 redundant Hipposideros ruber1 Kenya 1.036 34.753
FMNH 215451 redundant Hipposideros ruber1 Kenya 1.036 34.753
FMNH 215452 redundant Hipposideros ruber1 Kenya 1.036 34.753
FMNH 215453 redundant Hipposideros ruber1 Kenya 1.036 34.753
FMNH 215476 MT149828 Hipposideros ruber1 Kenya 1.036 34.753
FMNH 215477 redundant Hipposideros ruber1 Kenya 1.036 34.753
FMNH 215478 redundant Hipposideros ruber1 Kenya 1.036 34.753
NMK 184904 MT149825 MT149686 MT149584 MT149486 Hipposideros ruber1 Kenya 0.212 34.899
NMK 184905 redundant Hipposideros ruber1 Kenya 0.212 34.899
NMK 187407 redundant Hipposideros ruber1 Kenya 1.036 34.753
NMK 187408 MT149829 Hipposideros ruber1 Kenya 1.036 34.753
NMK 187409 MT149830 MT149687 MT149585 MT149487 MT149388 Hipposideros ruber1 Kenya 1.036 34.753
NMK 187410 redundant Hipposideros ruber1 Kenya 1.036 34.753
NMK 187412 MT149831 Hipposideros ruber1 Kenya 1.036 34.753
DM 12603 KF551819 Hipposideros ruber1 Liberia 7.553 -8.492
DM 13245 KF551815 Hipposideros ruber1 Liberia 7.553 -8.492
DM 13246 KF551820 Hipposideros ruber1 Liberia 7.553 -8.492
FMNH 225201 MT149832 MT149688 MT149586 MT149488 MT149389 Hipposideros ruber1 Rwanda -2.485 29.199
FMNH 225202 MT149833 Hipposideros ruber1 Rwanda -1.504 29.613
FMNH 225203 redundant Hipposideros ruber1 Rwanda -1.504 29.613
FMNH 225204 redundant Hipposideros ruber1 Rwanda -1.506 29.615
FMNH 225205 redundant Hipposideros ruber1 Rwanda -1.506 29.615
FMNH 225206 MT149834 Hipposideros ruber1 Rwanda -1.506 29.615
FMNH 225207 redundant Hipposideros ruber1 Rwanda -1.506 29.615
FMNH 225208 MT149835 MT149689 MT149587 MT149489 MT149390 Hipposideros ruber1 Rwanda -1.506 29.615
FMNH 225209 redundant Hipposideros ruber1 Rwanda -1.506 29.615
FMNH 192935 MT149836 MT149690 MT149588 MT149490 MT149391 Hipposideros ruber1 Tanzania -1.094 31.515
FMNH 137629 FJ347987 Hipposideros ruber1 Uganda 32.283 -0.005
FMNH 160358 MT149837 Hipposideros ruber1 Uganda -0.989 29.614
FMNH 160359 MT149838 MT149691 MT149589 MT149491 MT149392 Hipposideros ruber1 Uganda -0.989 29.614
FMNH 160361 MT149839 Hipposideros ruber1 Uganda -1.041 29.580
FMNH 161040 MT149840 Hipposideros ruber1 Uganda -0.245 29.819
FMNH 223866 redundant MT149692 MT149590 MT149492 MT149393 Hipposideros ruber1 Uganda -0.342 31.966
FMNH 223867 MT149841 Hipposideros ruber1 Uganda -0.342 31.966
FMNH 227415 MT149842 Hipposideros ruber2 Central African Republic 3.033 16.410
FMNH 227416 MT149843 Hipposideros ruber2 Central African Republic 3.033 16.410
FMNH 227417 MT149844 MT149693 MT149591 MT149394 Hipposideros ruber2 Central African Republic 3.033 16.410
FMNH 149408 FJ347986 MT149694 MT149592 MT149493 MT149395 Hipposideros ruber2 D. R. Congo -1.417 28.583
FMNH 149409 redundant Hipposideros ruber2 D. R. Congo -1.417 28.583
FMNH 149410 redundant MT149695 MT149593 MT149494 MT149396 Hipposideros ruber2 D. R. Congo -1.417 28.583
FMNH 149412 redundant Hipposideros ruber2 D. R. Congo -1.417 28.583
ROM 100546 FJ347978 Hipposideros ruber2 Ivory Coast 6.930 -7.217
FMNH 215479 redundant Hipposideros ruber2 Kenya 0.244 34.907
FMNH 215480 MT149845 Hipposideros ruber2 Kenya 0.244 34.907
FMNH 215481 MT149846 Hipposideros ruber2 Kenya 0.244 34.907
FMNH 215482 redundant MT149696 MT149594 MT149495 MT149397 Hipposideros ruber2 Kenya 0.244 34.907
FMNH 215483 redundant MT149697 MT149595 MT149496 MT149398 Hipposideros ruber2 Kenya 0.244 34.907
NMK 184878 MT149847 Hipposideros ruber2 Kenya 0.248 34.906
NMK 184880 MT149848 Hipposideros ruber2 Kenya 0.248 34.906
NMK 184882 MT149849 Hipposideros ruber2 Kenya 0.248 34.906
NMK 184883 MT149850 Hipposideros ruber2 Kenya 0.248 34.906
NMK 184884 MT149851 Hipposideros ruber2 Kenya 0.248 34.906
NMK 187383 redundant Hipposideros ruber2 Kenya 0.212 34.899
NMK 187384 MT149852 Hipposideros ruber2 Kenya 0.212 34.899
FMNH 165161 redundant Hipposideros ruber2 Uganda 1.733 31.467
FMNH 165162 MT149853 Hipposideros ruber2 Uganda 1.683 31.533
FMNH 165163 redundant MT149698 MT149596 MT149497 MT149399 Hipposideros ruber2 Uganda 1.683 31.533
FMNH 165164 MT149854 Hipposideros ruber2 Uganda 1.683 31.533
FMNH 165165 MT149855 Hipposideros ruber2 Uganda 1.683 31.533
FMNH 165166 redundant Hipposideros ruber2 Uganda 1.750 31.583
FMNH 165167 redundant MT149699 MT149597 MT149498 MT149400 Hipposideros ruber2 Uganda 1.733 31.467
FMNH 224069 redundant Hipposideros ruber2 Uganda 0.501 30.426
FMNH 224071 redundant Hipposideros ruber2 Uganda 0.501 30.426
FMNH 224074 MT149856 Hipposideros ruber2 Uganda 0.501 30.426
FMNH 224075 MT149857 Hipposideros ruber2 Uganda 0.501 30.426
FJ347994 Hipposideros ruber3 Cameroon 3.564 13.408
FJ347991 Hipposideros ruber3 Cameroon 2.941 9.911
FJ347990 Hipposideros ruber3 Cameroon 2.941 9.911
FJ347988 Hipposideros ruber3 Cameroon 4.913 9.241
EBD 18240 FJ347984 Hipposideros ruber3 Equatorial Guinea 1.889 9.793
EBD 18266 FJ347985 Hipposideros ruber3 Equatorial Guinea 1.889 9.793
EBD 18511 FJ347983 Hipposideros ruber3 Equatorial Guinea 3.747 8.750
EBD 18942 FJ347981 Hipposideros ruber3 Principe 1.615 7.404
EBD 18926 FJ347982 Hipposideros ruber3 São Tomé 0.219 6.727
FMNH 219477 MT149858 MT149700 MT149598 MT149499 MT149401 Hipposideros ruber4 D. R. Congo -5.290 14.871
FMNH 169707 KT583815 Macronycteris commersoni Madagascar -12.932 49.057
FMNH 175777 KT583822 Macronycteris commersoni Madagascar -16.380 45.345
FMNH 175966 KT583823 Macronycteris commersoni Madagascar -22.486 45.392
FMNH 175974 MT149859 Macronycteris commersoni Madagascar -22.317 45.293
FMNH 175975 MT149860 Macronycteris commersoni Madagascar -22.317 45.293
FMNH 176155 KT583824 MT149701 MT149599 MT149500 MT149402 Macronycteris commersoni Madagascar -22.778 43.523
FMNH 176158 MT149861 Macronycteris commersoni Madagascar -22.217 43.330
FMNH 176277 redundant Macronycteris commersoni Madagascar -12.942 49.055
FMNH 177302 KT583825 Macronycteris commersoni Madagascar -16.315 46.810
FMNH 178803 redundant Macronycteris commersoni Madagascar -12.712 49.474
FMNH 178806 KT583816 Macronycteris commersoni Madagascar -12.712 49.474
FMNH 178808 KT583817 redundant Macronycteris commersoni Madagascar -12.712 49.474
FMNH 178809 KT583818 Macronycteris commersoni Madagascar -12.712 49.474
FMNH 178810 KT583819 Macronycteris commersoni Madagascar -12.712 49.474
FMNH 178811 KT583820 Macronycteris commersoni Madagascar -12.712 49.474
FMNH 178812 KT583826 Macronycteris commersoni Madagascar -12.712 49.474
FMNH 178815 KT583821 redundant Macronycteris commersoni Madagascar -12.712 49.474
FMNH 179201 MT149862 Macronycteris commersoni Madagascar -17.280 49.420
FMNH 183934 KT583827 Macronycteris commersoni Madagascar -24.050 43.750
FMNH 183980 KT583813 redundant Macronycteris commersoni Madagascar -12.337 49.385
FMNH 184030 KT583812 Macronycteris commersoni Madagascar -14.966 47.308
FMNH 184170 KT583828 Macronycteris commersoni Madagascar -24.650 43.963
FMNH 184887 MT149863 Macronycteris commersoni Madagascar -15.904 46.598
FMNH 209236 MT149864 Macronycteris commersoni Madagascar -18.063 44.541
FMNH 217940 KT583831 redundant Macronycteris commersoni Madagascar -22.632 45.338
FMNH 221308 KT583829 Macronycteris commersoni Madagascar -12.932 49.057
FMNH 231862 MT149865 MT149702 MT149600 MT149501 MT149315 Macronycteris commersoni Madagascar -17.889 49.203
UADBA 32916 KT583830 Macronycteris commersoni Madagascar 15.538 46.886
UADBA 32987 KT583814 Macronycteris commersoni Madagascar -13.932 49.057
UADBA 32989 KR606333 Macronycteris commersoni Madagascar -12.917 49.143
FMNH 175970 MT149866 MT149703 MT149601 MT149502 MT149403 Macronycteris cryptovalorona Madagascar -22.317 45.293
FMNH 184173 MT149867 MT149704 MT149602 MT149503 MT149404 Macronycteris cryptovalorona Madagascar -24.650 43.963
AMNH 269871 KT583801 Macronycteris gigas Central African Republic
FMNH 219602 MT149868 MT149705 MT149603 MT149504 MT149405 Macronycteris gigas D. R. Congo 0.241 20.883
FMNH 219682 MT149869 MT149706 MT149604 MT149415 MT149406 Macronycteris gigas D. R. Congo 0.241 20.883
FMNH 220226 redundant MT149707 MT149605 MT149505 MT149407 Macronycteris gigas Kenya -4.647 39.380
FMNH 220227 redundant MT149708 MT149606 MT149506 MT149408 Macronycteris gigas Kenya -4.647 39.380
FMNH 220239 MT149870 Macronycteris gigas Kenya -4.215 39.451
DM 12602 KF551826 Macronycteris gigas Liberia 7.553 -8.492
IVB S1032 EU934469 Macronycteris gigas Senegal 12.350 -13.217
IVB S1044 EU934470 Macronycteris gigas Senegal 12.350 -13.217
AMNH 269879 KT583802 Macronycteris vittata Central African Republic 3.500 16.000
FMNH 215942 MT149871 MT149709 MT149607 MT149507 MT149409 Macronycteris vittata Kenya -3.300 39.995
FMNH 215943 redundant Macronycteris vittata Kenya -3.300 39.995
FMNH 215944 redundant Macronycteris vittata Kenya -3.300 39.995
FMNH 215945 redundant Macronycteris vittata Kenya -3.300 39.995
FMNH 215946 MT149872 Macronycteris vittata Kenya -3.287 39.982
FMNH 215947 redundant Macronycteris vittata Kenya -3.287 39.982
FMNH 215948 MT149873 Macronycteris vittata Kenya -3.287 39.982
FMNH 215949 redundant Macronycteris vittata Kenya -3.287 39.982
FMNH 215950 MT149874 Macronycteris vittata Kenya -3.287 39.982
FMNH 215951 MT149875 Macronycteris vittata Kenya -3.282 39.971
FMNH 215952 MT149876 Macronycteris vittata Kenya -3.282 39.971
FMNH 215953 redundant MT149710 MT149608 MT149410 Macronycteris vittata Kenya -3.282 39.971
FMNH 215954 MT149877 Macronycteris vittata Kenya -3.282 39.971
FMNH 215955 redundant Macronycteris vittata Kenya -3.282 39.971
FMNH 215959 MT149878 Macronycteris vittata Kenya -3.309 40.018
FMNH 215960 MT149879 Macronycteris vittata Kenya -3.309 40.018
FMNH 215961 MT149880 Macronycteris vittata Kenya -3.309 40.018
FMNH 215962 MT149881 Macronycteris vittata Kenya -3.309 40.018
FMNH 215963 MT149882 Macronycteris vittata Kenya -3.309 40.018
FMNH 215967 MT149883 Macronycteris vittata Kenya -3.303 39.999
FMNH 215968 redundant Macronycteris vittata Kenya -3.305 39.937
FMNH 215969 redundant Macronycteris vittata Kenya -3.305 39.937
FMNH 220224 redundant Macronycteris vittata Kenya -4.647 39.378
FMNH 220225 MT149885 Macronycteris vittata Kenya -4.647 39.380
FMNH 220228 MT149886 Macronycteris vittata Kenya -4.647 39.380
FMNH 220229 MT149887 MT149711 MT149609 MT149508 MT149411 Macronycteris vittata Kenya -4.647 39.380
FMNH 220231 MT149888 Macronycteris vittata Kenya -4.614 39.354
FMNH 220232 MT149889 Macronycteris vittata Kenya -4.614 39.354
FMNH 220233 MT149890 Macronycteris vittata Kenya -4.614 39.354
FMNH 220234 redundant Macronycteris vittata Kenya -4.614 39.354
FMNH 220235 MT149891 MT149712 MT149610 MT149509 MT149412 Macronycteris vittata Kenya -4.614 39.354
FMNH 220236 redundant Macronycteris vittata Kenya -4.614 39.354
FMNH 220237 redundant Macronycteris vittata Kenya -4.614 39.354
FMNH 220238 redundant Macronycteris vittata Kenya -4.614 39.354
FMNH 220240 redundant Macronycteris vittata Kenya -3.300 39.995
NMK 187219 redundant Macronycteris vittata Kenya -3.335 40.031
NMK 187220 MT149884 Macronycteris vittata Kenya -3.335 40.031
NMK 187221 redundant Macronycteris vittata Kenya -3.335 40.031
NMK 187222 redundant Macronycteris vittata Kenya -3.335 40.031
DM 8645 KF551828 redundant Macronycteris vittata Mozambique -18.565 32.220
DM 11510 KF551827 Macronycteris vittata Mozambique -18.978 34.176
FMNH 192800 redundant MT149713 MT149611 MT149510 MT149413 Macronycteris vittata Tanzania -4.902 39.688
FMNH 192801 MT149892 Macronycteris vittata Tanzania -4.902 39.688
FMNH 192857 redundant MT149714 MT149612 MT149511 MT149414 Macronycteris vittata Tanzania -4.902 39.688
FMNH 192858 redundant Macronycteris vittata Tanzania -4.902 39.688
FMNH 192859 MT149893 Macronycteris vittata Tanzania -4.902 39.688
FMNH 192860 KT583807 Macronycteris vittata Tanzania -4.902 39.688
FMNH 192865 KT583808 redundant Macronycteris vittata Tanzania -4.902 39.688
FMNH 192866 KT583809 Macronycteris vittata Tanzania -4.902 39.688
FMNH 220268 MT149614 MT149512 MT149417 MT149316 Triaenops afer Kenya -4.590 39.331

Supplementary materials

Supplementary material 1 

Figure S1. Geographic distribution of voucher specimens used in this analysis

Bruce D. Patterson, Paul W. Webala, Tyrone H. Lavery, Bernard R. Agwanda, Steven M. Goodman, Julian C. Kerbis Peterhans, Terrence C. Demos

Data type: occurrence

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Download file (819.08 kb)
Supplementary material 2 

Figure S2. Phylogeny of Hipposideridae based on maximum likelihood analysis of cyt-b based on 452 individuals

Bruce D. Patterson, Paul W. Webala, Tyrone H. Lavery, Bernard R. Agwanda, Steven M. Goodman, Julian C. Kerbis Peterhans, Terrence C. Demos

Data type: phylogenetic tree

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Download file (27.34 kb)
Supplementary material 3 

Figure S3. Phylogeny of Hipposideridae based on Bayesian inference analysis of cyt-b based on 452 individuals

Bruce D. Patterson, Paul W. Webala, Tyrone H. Lavery, Bernard R. Agwanda, Steven M. Goodman, Julian C. Kerbis Peterhans, Terrence C. Demos

Data type: phylogenetic tree

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Download file (26.25 kb)