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A time-calibrated species-level phylogeny of bats (Chiroptera, Mammalia)

Ingi Agnarsson*,Carlos M Zambrana-Torrelio*,Nadia Paola Flores-Saldana*,Laura J May-Collado*
*University of Puerto Rico, Puerto Rico;EcoHealth Alliance andAsociación para la Biología de la Conservación - Bolivia

Accepted 2011 Feb 2.

This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.

PMCID: PMC3038382  PMID:21327164

Abstract

Despite their obvious utility, detailed species-level phylogenies are lacking for many groups, including several major mammalian lineages such as bats. Here we provide a cytochrome b genealogy of over 50% of bat species (648 terminal taxa). Based on prior analyzes of related mammal groups, cytb emerges as a particularly reliable phylogenetic marker, and given that our results are broadly congruent with prior knowledge, the phylogeny should be a useful tool for comparative analyzes. Nevertheless, we stress that a single-gene analysis of such a large and old group cannot be interpreted as more than a crude estimate of the bat species tree. Analysis of the full dataset supports the traditional division of bats into macro- and microchiroptera, but not the recently proposed division into Yinpterochiroptera and Yangochiroptera. However, our results only weakly reject the former and strongly support the latter group, and furthermore, a time calibrated analysis of a pruned dataset where most included taxa have the entire 1140bp cytb sequence finds monophyletic Yinpterochiroptera. Most bat families and many higher level groups are supported, however, relationships among families are in general weakly supported, as are many of the deeper nodes of the tree. The exceptions are in most cases apparently due to the misplacement of species with little available data, while in a few cases the results suggest putative problems with current classification, such as the non-monophyly of Mormoopidae. We provide this phylogenetic hypothesis, and an analysis of divergence times, as tools for evolutionary and ecological studies that will be useful until more inclusive studies using multiple loci become available.

Introduction

Phylogenies form the backbone of evolutionary biology and represent tools that underlie a broad spectrum of evolutionary and ecological studies[1][2]. Phylogenetic work on any given group often first focuses on the ‘big picture’, that is the placement of, and relationship among, major groups, long before species level phylogenies become available. One simple reason for this focus is that general interest questions, such as where and how the major divisions of life fit together, can be answered through sampling relatively few taxa, in a relatively cost and time effective manner. Yet, more detailed species-level phylogenies, often lagging far behind, are the most useful tools for evolutionary and ecological analyses. The above is certainly true for mammalian phylogenetics, where higher level phylogenetics are intensely studied, with the few detailed species level studies for major groups lagging far behind (see e.g.[3][4][5][6]).

The ultimate goal of phylogenetics must be detailed species level phylogenies of all of life, based on many data. However, achieving this goal will take much time and effort. In the meantime, species level phylogenies may be rapidly reconstructed with already available data using several approaches. One is the construction of phylogenetic supertrees where available trees and taxonomies are united into a summary cladogram[7]. Another is the creation of supermatrices based on available character data. Both approaches make available useful research tools, which may have different strengths.

The bats (Chiroptera) are one such group where many phylogenetic studies have focused either on understanding higher-level bat relationships (e.g.[8][9]) or species-level relationships within specific groups (e.g.[10][11][12]). Available phylogenies have then been summarized in a supertree[13]. Here, we provide cytochrome b gene tree for over 50% of bat species (648 total taxa). Cytb not only is the most widely available marker for most mammals, but also has been shown to be a particularly reliable phylogenetic marker (e.g.[14]). Thus according with prior analyses of other mammal groups[3][4][5][6], the cytb gene tree can be expected to at least roughly approximate the species-level phylogeny of Chiroptera.  We provide this phylogeny simply as an alternative tool to super-tree phylogenies, until more detailed studies become available.

 Methods

            Cytochrome b sequences were downloaded from GenBank for 648 bats, including nearly 550 named species, and the remaining terminal taxa being subspecies or unidentified/undescribed species. As outgroups we selected 10 species representing other Pegasoferae[15]: Cetartidoactyla, Perissodactyla, Carnivora, Pholidota (pangolins), and Erinaceomorpha as the primary outgroup. Because many of the taxa have incomplete Cytb sequences, and missing data can cause problems in phylogenetic reconstruction (e.g.[16]), we also created a ‘pruned’ dataset where taxa with less than 30% of the full sequence were removed (‘pruned’ matrix), and another set where only 2 representatives of each family were retained (‘time’ matrix). The latter was used for analysis of divergence times. The sequences were aligned in Mesquite[17], a trivial task given that it is a protein-coding gene with no implied gaps. The appropriate model for the Bayesian analysis was selected with jModeltest[18] using the AIC criterion[19]. The best model was GTR+Γ+I[20][21]. Bayesian analysis was performed using MrBayes V3.1.2[22] with settings as in[3][4] with separate model estimation for first, second, and third codon positions. The MCMC was run with one cold and three heated chains for 30,000,000 generations, sampling trees every 1,000 generations. The first 15,000,000 were then discarded as burnin, after which stationarity was reached. The data matrix and trees are available from the first author and data and trees will be submitted to Treebase (http://www.treebase.org). Genbank accession numbers are listed in Table 1 (see Appendices).


            The ‘time’ matrix was used to estimate divergence times using relaxed clock methods in BEAST 1.6.1.[23][24]. For Emballonuridae we additionally retained twoTaphozous species as these did not group with the other Emballonuridae in the full analysis. The analysis was calibrated using normally distributed priors reflecting: (1) the minimal age of 37 my for the split between Rhinolophidae and Hipposiderids based on the estimated age of the oldest rhinolophid and hipposiderid fossils[25][26]; (2) the estimated age of Carnivora (split of cat plus dog) of 54 my (the age of Carnivora as estimated by[27]); the estimated age of Chiroptera as a normally distributed prior with mean of 54 my, also based on[27]; and (4) the minimal age of Emballonuridae of 48 my based on the oldest fossils that are with some certainty placed within that family[28]. Prior to the divergence time analysisErinaceus (Erinaceomorpha) andTalpa (Eulipotyphla) were set as primary outgroups by enforcing the monophyly of the remaining taxa, and the monophyly of Rhinolopidae plus Hipposideridae was furthermore enforced. The resulting age estimates were then compared to the above mentioned fossil data in addition to the age of other known fossil bats[28].

Results and Discussion

Phylogenetics

The analysis of the full dataset supports the monophyly of bats, and the major division of Chiroptera into Megachiroptera (Pteropodidae) and Microchiroptera with Yangochiroptera contained within the latter group (Figures 1-2). 


Figure 1. Relationships among bat families according with the analysis of all data. Numbers are posterior probabilities, above branches from the full analysis, below branches support from the pruned analysis.

graphic file with name figure1final.jpg

Figure 2. Relationship among bat species with major clade names. Numbers are posterior probabilities. The results are detailed in Figure 4, see Appendices.

graphic file with name figure2final.jpg

The analysis of the ‘time’ matrix, however, supports the now rather generally accepted split into Yinpterochiroptera and Yangochiroptera (see below) (e.g.[29][30][31][32][33][34]).

    The Macrochiroptera, or fruitbats (Pteropodidae), are in the main analysis sister to the remaining bats (Figures 2, 4a). Within Pteropodidae most genera are monophyletic, with the exception ofRousettus angolensis (synonymLissonycterisangolensis) nests withMyonycteris. Overall, these results are similar to results of previous studies on macrochiroptera phylogenetics (e.g.[10]). 


The Microchiroptera is divided in two major clades, one is the Yangochiroptera including the families Emballonuridae, Furipteridae, Miniopteridae, Molossidae, Mormoopidae, Mystacinidae, Myzopodidae, Natalidae Noctilionidae, Phyllostomidae, Thyropteridae, and Vespertilionidae. The other major group, which we refer to as a modified “Rhinolophoidea” (Figures 1-2, 4), contains the remaining microbat families Craseonycteridae, Hipposideridae, Megadermatidae, Rhinolophidae, and Rhinopomatidae. Hipposideridae and Rhinolophidae are sister families as supported by previous studies (e.g.,[13][31][34]).  Only Hipposideridae here contains more than a single genus, and within that familyHipposiderus is paraphyletic, containing several small genera.

 Overall most microchiropteran superfamilies are not supported as monophyletic, except Rhinopomatoidea (Figure 2). A modified Rhinolophoidea that contains Rhinopomatoidea is also supported, and the superfamily Vespertilionioidea is monophyletic except for containing a couple of apparently misplaced species (Figures 2, 4b). The relationships among the families, however, in general are poorly supported and differ among analyses (see Figures 1, 3-4). Taxonomic families are generally recovered either as strictly monophyletic, or approximately, as paraphyletic groups due to one or a couple of ‘misplaced’ taxa.  In the full analysis, families that are strictly supported (i.e. monophyletic, or in the case of families represented by single species, not nesting within another family) are: Craseonycteridae, Furipteridae, Hipposideridae, Megadermatidae, Miniopteridae, Molossidae, Mystacinidae, Myzopodidae, Natalidae, Noctilionidae, Rhinolophidae, Rhinopomatidae, and Thyropteridae. Not monophyletic families are  Phyllostomidae due to the placement of onePlatalina species nesting within Vestpertilionidae,  Emballonuridae is rendered polyphyletic by the placement of the genusTaphozous (2 species) and one species ofEmballonura outside it. Vespertilionidae is paraphyletic in that within it are placed the above mentionedPlatalina andEmballonura. Finally Mormoopidae forms two clades that are not sister, one including the genusMormoops, the other the genusPteronotus.  These ‘minor’ deviations from family monophyly in most cases probably do not represent refutation of family clades; rather this seems to be mostly an issue of missing data. For example, when species with less than 30% of the sequence are removed, all families are recovered monophyletic, with two exceptions that may be taxonomically informative :(1) The genusTaphozous still groups outside Emballonuridae which contradicts previous studies (e.g.,[32][34][35]) and (2) the Mormoopidae family still forms two separate clades, which agrees with Kennedy et al[36] (for contrasting topologies see e.g.,[13][31]).

Finally, several genera of the family Phyllostomidae are not monophyletic, includingMimon,Mycronycteris,Rousettus,Vampyressa, andArtibeus. Within MolossidaeTadarida,Mops,Chaerephon are not monophyletic. Within Natalidae,Chilonatalus is non-monophyletic, and within Vespertilionidae, the large generaPipistrellus andMyotis are not monophyletic.

Many taxa in the full analysis only have available a partial Cytb sequence, and notably clade support is low for many of the deeper clades of the phylogeny. Low support is unsurprising given missing data, and the use of only a single locus for both very many taxa and old divergences. Further, any given gene tree can be expected to differ from the species tree due to various processes including incomplete lineage sorting, introgression, and others. Thus, future effort should focus on resolving the species-level phylogeny of bats with a multi-locus approach. Nevertheless, the phylogeny, especially when the taxa with the highest % missing data are removed, is broadly congruent with prior knowledge, and should thus be a useful tool.  


Divergence times

The analysis of divergence times (Figure 3) generally agrees with prior studies[27][35][37], though the estimated ages are rather lower in general than those estimated by Jones et al.[38]. 


Figure 3. A calibrated phylogeny of bat families. Numbers are in million years, and gray bars are 95% confidence intervals


graphic file with name figure3.jpg

In part this may relate to the different suggested relationships among bat families across these studies, though the error margins of many nodes estimated are rather wide and nearly always include age estimates found by prior studies. The results also in most cases are consistent with the available bat fossil record[28]. The age of crown bats, i.e. the split between Yinpterochiroptera and Yangochiroptera is estimated at 58.9 my, a value lying in between the estimates of Cao et al.[27], and Jones et al.[38] and Arnason et al.[37]. Other dates that were included as priors, as expected, also are consistent with the fossil record. The split between Hipposideridae and Rhinolophidae is estimated at 36.9 my, consistent with the oldest known Hipposideridae fossil dated at close to 40 my. Similarly the age of Molossidae estimated at 36.1 my is close to the oldest Molossidae fossil at near 40 my[28]. The split between Emballonuridae and its sister lineage is estimated at 49 my, right around the age of the oldest emballonurid fossil. Most other dates are also consistent with the fossil record. The genusTaphozoushas a fossil record going up to 20.4 my, a date in between the estimated split between crownTaphozous (18.1 my) and the split betweenTaphozous and other Emballonuridae (44.2 my). The oldest Mystacinidae fossil dates from around 20 my[28] and the estimated split here between Mystacinidae and its sister lineage is 24.3 my. The oldest Phyllostomidae fossil dates from around 16 my[28], a date in between the split between crownPhyllostoma (14.4 my) and the split between Phyllostomidae and its sister lineage (28.5 my). In a few cases the estimates are younger than possible given current understanding the fossil record, e.g. the age of Megadermatidae at 23.6 my while the oldest fossil is at least 37 my. However, 95% confidence interval of this node estimate reaches over 40 my. The age of Natalidae, estimated at around 43 my, is younger than the oldest fossil thought to belong to that family, at over 50 my. Similarly one putative Vespertilionidae genus,Stehlinia, has a fossil record older (up to 48 my) than the estimated age of the family at 36.1 my. These mismatches may reflect simply erroneous age estimates, or could possibly indicate that some fossil bats are taxonomically misplaced. In most other cases the estimated ages are older than the oldest available fossils, which may reflect the incompleteness of the fossil record.

In sum, we provide acytochrome b genealogy for Chiroptera, which we expect to crudely approximate the bat species tree. Until more detailed species-level phylogenies become available, this offers an alternative phylogenetic tool to super-tree phylogenies, for comparative evolutionary, ecological analyzes, and phylogenetic conservation assessment.

Acknowledgments

Thanks to PLoS Currents: Tree of Life board of reviewers, the editor, and two anonymous reviewers for comments that improved this manuscript.

Funding information


This research was funded, in part, by the University of Puerto Rico.

Competing interests
The authors have declared that no competing interests exist.

Appendices

Figure 4.Results from Fig. 2 in standard tree format.

Figure 4a. Results from Figure 2, Pteropodidae. Numbers are posterior probabilities

graphic file with name figure4a1.jpg

Figure 4b. Results from Figure 2, Megadermatidae, Craseonycteridae, Rhinopomatidae, Hipposideridae, and Rhinolophidae. Numbers are posterior probabilities.

graphic file with name figure4b1.jpg

Figure 4c. Results from Figure 2, Miniopteridae, Noctilionidae, Mormoopidae, Mystacinidae, Thyropteridae, Furipteridae, and Phyllostomidae in part. Numbers are posterior probabilities

graphic file with name figure4c1.jpg

Figure 4d. Results from Figure 2, Phyllostomidae, in part. Numbers are posterior probabilities

graphic file with name figure4d.jpg

Figure 4e. Results from Figure 2, Molossidae,Emballonuridae, Myzopodidae, Natalidae, and Vespertilionidae in part. Numbers are posterior probabilities

graphic file with name figure4e.jpg

Figure 4f. Results from Figure 2, Vespertilionidae in part. Numbers are posterior probabilities

graphic file with name figure4f1.jpg

Figure 4g. Results from Figure 2, Vespertilionidae in part. Numbers are posterior probabilities

graphic file with name figure4g1.jpg

Table 1.

Species included and Genbank accession numbers

GenusSpeciessub sp or voucherAccession Number
Acerodon jubatusEU330962
Aethalops alectoAY629006
Ametrida centurio AY604446
Anoura caudiferL19506
Anoura geoffroyiFJ155495
AntrozousdubiaquercusEF222381
AntrozouspallidusEF222382
Ardops nichollsiAY572337
Ariteus flavescensAY604436
ArtibeusamplusEU160947
ArtibeusanderseniU66509
ArtibeusaztecusU66510
Artibeuscf.jamaicensisDQ985486
Artibeuscf.obscurusDQ903818 
ArtibeuscinereusEU805599
ArtibeusconcolorU66519
ArtibeusfimbriatusU66498
ArtibeusfraterculusU66499
ArtibeusfuliginosusL19505 
ArtibeusglaucuswatsoniFJ179259
ArtibeusglaucusU66512
ArtibeusglaucusbogotensisEU805596
ArtibeusglaucusgnomusEU805594
ArtibeushartiiEU160972
ArtibeushirsutusU66500
ArtibeusinopinatusU66501
ArtibeusintermediusFJ179231
ArtibeusjamaicensisaequatorialisDQ869450
ArtibeusjamaicensisjamaicensisDQ869518
ArtibeusjamaicensisparvipesDQ869474
ArtibeusjamaicensispaulusDQ869456
ArtibeusjamaicensisrichardsoniDQ869454
ArtibeusjamaicensistrinitatisDQ003028
ArtibeusjamaicensistriomylusAY382782
ArtibeusjamaicensisyucatanicusDQ869484
ArtibeuslituratusEU160813
ArtibeusobscurusU66507
ArtibeusphaeotisFJ376727
ArtibeusplanirostrisfallaxDQ869426
ArtibeusplanirostrisgrenadensisDQ869439
ArtibeusplanirostrisherculesDQ869421
ArtibeusplanirostrisplanirostrisDQ869396
ArtibeusplanirostristrinitatisDQ869433
ArtibeusschwartziDQ869531
Artibeussp.FURBDQ985497 
ArtibeustoltecusU66515
AselliatridensFJ457617
AselliscusstoliczkanusEU434954
AselliscustricuspidatusDQ888679
BalantiopterysinfuscaEF584151
BalantiopterysioEF584153
BalantiopterysplicataEF584154
Balionycteris maculata AF044636
BarbastellabarbastellusEU360700
BarbastellabeijingensisEF534762
BarbastellaleucomelasEF534766
Brachyphylla cavernarumAY572383
Brachyphylla nanaEU521680
Brachyphylla pumilaEU521678
Carollia benkeithiDQ177282
Carollia brevicaudaFJ154120
Carollia castaneaDQ888289
Carollia sowelliAF511973
Carollia subrufaAF187024
Centronycteris centralisEF584155
Centronycteris maximilianiEF584157
Centurio senexgreenhalliAY604445
Centurio  senexAY604444
ChaerephonansorgeiAY377967
ChaerephonchapiniAY591329
ChaerephonjobensisAY591331
ChaerephonleucogasterEU716041
ChaerephonnigeriaeAY591330
ChaerephonpumilaAY614756
ChalinolobustuberculatusNC_002626 
ChilonatalusmicropusAY621026
ChilonatalustumidifronsAY621028
Chiroderma improvisumL28938
Chiroderma  doriaeAY169958
Chiroderma  salviniL28939
Chiroderma  trinitatumDQ312413
Chiroderma  villosumFJ154121
Chironax melanocephalusAY629005
Chrotopterus auritusFJ155481
CloeotispercivaliFJ457616
CoelopsfrithiiEU434955
CormurabrevirostrisEF584159
CraseonycteristhonglongyaiEF035012
CynomopsparanusAY675219
Cynopterusbrachyotis EF201644
Cynopterushorsfieldii EF201643
CynopterussphinxDQ445703
CyttaropsalecoEF584162
Dermanura bogotensisFJ376714
Dermanura ravaFJ179252
Dermanura rosenbergiFJ179254
Dermanura  incomitataFJ376718
Desmalopexleucopterus EU330965
DesmalopexmicroleucopterusEU330976
Desmodus rotundusFJ155477
Diaemus youngiFJ155475
Diclidurus albusEF584163
Diclidurus ingensEF584164
Diclidurus isabellusEF584166
Diclidurus scutatusEF584167
Diphylla ecaudataFJ155476
DobsoniainermisDQ445704
DobsoniaminorDQ445705
DobsoniamoluccensisAF144064
Dyacopterus spadiceusEF105531
Ectophylla albaDQ312404
Emballonura alectoAY426101
Emballonura atrataDQ178261
Emballonura beccarriiEF584222
Emballonura monticolaEF584223
Emballonura raffrayanaEF584224
Emballonura semicaudataEF635553
Emballonura seriiEF635544
Emballonura tiavatoDQ178285
Eonycteris spelaea AB062476
Epomophorus wahlbergiDQ445706
Epomops franqueti DQ445707
EptesicusandersoniandersoniEU786850
EptesicusandersonipallescensEU786841
EptesicusbottaeanatolicusEU786812
EptesicusbottaehingstoniEU786819
EptesicusbottaeinnesiEU786815
EptesicusbottaeogveniEU786876
EptesicusbottaetaftanimontisEU786814
EptesicusdiminutusEU786864
EptesicusfuscusEU786866
EptesicushottentotusEU786823
EptesicusisabellinusboscaiEU786838
EptesicusisabellinusisabellinusEU786831
EptesicusnasutusEU786840
EptesicusnilssoniAF376836
EptesicusregulusAY007531
EptesicusserotinusmirzaEU786861
EptesicusserotinusturcomanusEU786875
Erophylla bombifronsAY620438
Erophylla sezekorniAY620439
EumopsglaucinusfloridanusEU350026
EumopsperotisEU349991
Eumopssp.MMM-2008EU349999
EumopsunderwoodiEU349989
FuripterushorrensAY621004
Glossophaga commissarisiAF382886
Glossophaga leachiAF382878
Glossophaga longirostrisAF382875
Glossophaga morenoiAF382882
Glossophaga soricinaFJ392516
Glyphonycteris  daviesiAY380747
Glyphonycteris  sylvestrisAY380746
Haplonycteris fischeriAY817881
HarpiocephalusmordaxAJ841971
Harpyionycteris whiteheadiDQ445708
HipposiderosabaeEU934448
HipposiderosarmigerEU434946
HipposiderosaterDQ054807
HipposiderosbeatusFJ347976
HipposiderosbicolorDQ054808
HipposideroscafferFJ347980
HipposideroscalcaratusDQ054806
HipposideroscervinusDQ054805
HipposideroscineraceusDQ054809
HipposideroscoxiEF108148
HipposideroscyclopsEU934466
HipposiderosdiademaDQ219421
HipposiderosdyacorumEF108151
HipposiderosfuliginosusEU934468
HipposiderosgigasEU934470
HipposiderosjonesiEU934473
HipposideroskhaokhouayensisDQ054816
HipposideroslarvatusEU434949
HipposiderospomonaEU434950
HipposiderosprattiEU434952
HipposiderosridleyiDQ054812
HipposiderosrotalisDQ054814
HipposiderosruberFJ347996
Hipposiderossp.1KS-2008EU434948
HipposiderosspeorisDQ680823
HypsugocardonaeDQ318883
HypsugosaviiDQ120866
Hypsugosp.C1EU360677
Hypsugosp.C2EU360678
Hypsugosp.C4EU360679
IaioDQ302094
IdionycterisphyllotisIINMTCYTB
Kerivoulacf.papillosaAJ841970
LaephotiswintoniAJ841964
LasionycterisnoctivagansLSNMTCYTBZ
LasiuruscinereusDQ421825
LasiurusegaDQ421826
LasiurusxanthinusAF369549
Leptonycteris curasoaeAF382889
Lionycteris spurrelliAF423100
Lonchophylla chocoanaAF423092
Lonchophylla handleyiAF423094
Lonchophylla mordaxAF423095
Lonchophylla robustaAF423091
Lonchophylla thomasiAF423086
Lonchorhina  auritaFJ155494
Lophostoma silvicolaFJ155493
Lophostoma  brasilienseFJ155486
Lophostoma  evotisFJ155491
Lophostoma  schulziFJ155485
Macroglossus minimusAY926645
Macroglossus sobrinusFJ226494
Macrophyllum macrophyllumFJ155484
Macrotus  californicusAY380744
Macrotus  waterhousiiAY380745
MegadermalyraDQ888678
MegadermaspasmaAY057942
Megaerops ecaudatusEF201645
Megaerops niphanaeAF044647
Megaerops wetmoreiEF105537
MegaloglossuswoermanniDQ445710
Melonycteris fardoulisifardoulisiAY847251
Melonycteris fardoulisimaccoyi AY847254
Melonycteris fardoulisimengermani AY847241
Melonycteris fardoulisischouteni AY847236
Melonycteris melanopsAF044645
Melonycteris woodfordiwoodfordi AY847234
Mesophylla macconnelliFJ154122
Micronycteris brachyotisAY380748
Micronycteris brossetiAY380771
Micronycteris cf.schmidtorumDQ077407
Micronycteris giovanniaeAY380750
Micronycteris hirsutaDQ077415
Micronycteris homeziAY380754
Micronycteris matsesDQ077419
Micronycteris megalotisDQ077429
Micronycteris microtisAY380756
Micronycteris minutaDQ077405
Micronycteris schmidtorumDQ077442                 
Micronycteris sp.TK136752DQ077420
Micronycteris  niceforiAY380749
Micropteropus pusillusAF044648
Mimon crenulatumFJ155478
Mimon  bennettiiDQ903832 
MiniopterusafricanusEF363524
MiniopterusaustralisAY614735
MiniopterusfraterculusAJ841975
MiniopterusfuliginosusAB085735
MiniopterusgleniFJ383146
MiniopterusgriveaudiFJ232802
MiniopterusgriveaudigriveaudiFJ383143
MiniopterusinflatusAY614737
MiniopterusmacrocnemeAY614734
MiniopterusmagnaterEF517308
MiniopterusmajoriDQ899776
MiniopterusmanaviFJ383130
MiniopterusminorFJ232805
MiniopterusnatalensisAY614744
MiniopterusnewtoniiEF363521
MiniopteruspetersoniEU091258
MiniopteruspusillusDQ837650
MiniopterusschreibersiiEF530348
MiniopterusschreibersiibassaniiAY614733
MiniopterusschreibersiiblepotisAF217444
MiniopterusschreibersiioceanensisAF130123
MiniopterusschreibersiiorianaeAY614732
MiniopterusschreibersiipallidusAY614736
Miniopterussp.BBRA-2009bFJ383134
Miniopterussp.Comoros clade 2FJ232800
Miniopterussp.FMNH 167450FJ383132
Miniopterussp.FMNH 172602FJ383133
Miniopterussp.sororculusDQ899771
MolossusmolossusL19724
Monophyllus plethodonAF382887
Monophyllus redmaniAF382888
MopscondylurusEF474030
MopsleucostigmaEF474029
MopsmidasEF474049
MormoopsblainvilliiAY604462
MormoopsmegalophyllaAF330808
MormopteruskalinowskiiL19725
MosianigrescensEF635558
Murinacf.cyclotisAJ841974
MurinaleucogasterAB085733
Murinasp.GGJ-2006DQ435071
Murinasp.hn1151EF570883
Myonycteris brachycephalaAF044644
Myonycteris relictaAF044649
Myonycteris torquataAF044650
MyotisadversusAB106587
MyotisalbescensAF376839
MyotisalcathoeAJ841955
MyotisaltariumFJ215677
MyotisannectansAJ841956
MyotisatacamensisAM261882
MyotisaurascensAY665161
MyotisauriculusAM261884
MyotisaustroripariAM261885
MyotisbechsteiniiAF376843
MyotisblythiiDQ120906
MyotisblythiiancillaAM284170
MyotisblythiiblythiiAF376840
MyotisblythiiomariDQ288853
MyotisblythiioxygnathusAF376841
MyotisblythiipunicusAF376842
MyotisbocageiAJ504408
MyotisbombinusEF555240
MyotisbombinusamurensisAM284169
MyotisbrandtiiAM261886
MyotiscalifornicusAM261887
MyotiscapacciniiAF376845
Myotiscf.nipalensiskukunorensisAY699845
Myotiscf.pequiniusAM284173
Myotiscf.punicusAF246252
MyotischiloensisAM261888
MyotischinensisAB106588
MyotisciliolabrumAM261889
MyotisdasycnemeAF376846
MyotisdaubentoniAY665137
MyotisdaubentoninathalinaeAF376862
MyotisdaubentonidaubentoniiEU153105
MyotisdavidiiAB106591
MyotisdominicensisAF376848
MyotiselegansAM261891
MyotisemarginatusAF376849
MyotisescaleraiFJ460363
MyotisevotisAJ841949
MyotisfimbriatusEF555226
MyotisformosusAJ841950
MyotisformosusflavusEU434932
MyotisformosuswataseiEU434933
MyotisfraterAB106593
MyotisgoudotiAJ504451
MyotisgracilisAB243029
MyotisgrisescensAM261892
MyotishajastanicusAY665138
MyotishasseltiiAF376850
MyotishorsfieldiiAF376851
MyotisikonnikoviAB106602
MyotiskeaysiAF376852
MyotiskeeniiAM262329
MyotislanigerEF555229
MyotislatirostrisAM262330
MyotisleibiiAM262331
MyotislesueuriAY485687
MyotislevisAF376853
MyotislongipesFJ215678
MyotislucifugusAF376854
MyotislucifugusalascensisDQ503483
MyotislucifuguscarissimaAF294512
MyotislucifuguslucifugusDQ503488
MyotislucifugusrelictusDQ503558
MyotismacrodactylusEF555238
MyotismacropusAJ841959
MyotismacrotarsusAJ841960
MyotismartiniquensisAM262332
MyotismontivagusAM262333
MyotismuricolaAY665144
MyotismuricolabrowniAF376859
MyotismyotisAM261883
MyotismyotismyotisAF246246
MyotismystacinusAY665167
MyotisnattereriAB106606
MyotisnattereriescaleraeEU360649
MyotisnattereritschuliensisAM284171
MyotisnigricansAF376864
MyotisnipalensisAY699844
MyotisoxyotusAF376865
MyotispequiniusAM284172
MyotispetaxEF555236
MyotispruinosusAB106607
MyotispunicusEU360640
MyotisrickettiAJ504452
MyotisripariusAF376866
MyotisruberAF376867
MyotisschaubiAF376868
MyotisscottiAJ841958
MyotisseabraiAJ841962
MyotisseptentrionalisAM262335
MyotissicariusAJ841951
MyotissiligorensisFJ215679
MyotissimusAM262336
MyotissodalisAM262337
Myotissp.1 ZZ-2009FJ215680
Myotissp.2 ZZ-2009FJ215681
Myotissp.AM_M15111AY007527
Myotissp.C1EU360644
Myotissp.C2EU360645
Myotissp.C3EU360646
Myotissp.C4EU360647
Myotissp.C5EU360648
Myotissp.KK0005AB106609
Myotissp.PH-2006DQ337479
Myotissp.XT-2007EF555233
MyotisthysanodesAF376869
MyotistricolorAJ841952
MyotisveliferAF376870
MyotisvivesiAJ504406
MyotisvolansAF376871
MyotiswelwitschiiAF376874
MyotisyanbarensisAB106610
MyotisyumanensisAF376875
MystacinatuberculataAY960981
MyzopodaauritaEF432190
MyzopodaschliemanniEF432213
NatalusjamaicensisAY621023
NatalusmajorAY621021
NatalussaturatusAY621014
NatalusstramineusAY621019
NatalustumidirostrisAY621008
NeoromiciabrunneusEU786868
NeoromiciacapensisAJ841966
NeoromiciasomalicusEU786869
NoctilioalbiventrisAF330806
NyctalusazoreumDQ887590
NyctaluslasiopterusDQ120871
NyctalusleisleriAF376832
NyctalusnoctulaAJ841967
NyctalusplancyiDQ435073
NycterisleporinusAF330802
NycticeiushumeralisL19727
NyctielluslepidusAY621007
Nyctimene albiventerDQ314264
Nyctimene cephalotesDQ314268
Nyctimene majorAF044652
Nyctimene robinsoni AF144066
Nyctimene vizcaccia DQ445711
NyctinomopsaurispinosusL19728
NyctinomopslaticaudatusL19729
Otomopscf.formosusEF504252
OtomopsmadagascariensisEF216381
OtomopsmartiensseniEF216441
OtomopswroughtoniEF504251
Otopteropus cartilagonodusAY974770
Penthetor lucasiEF105542
PeropteryxkappleriEF584169
Peropteryxleucoptera EF584175
PeropteryxmacrotisEF584180
PeropteryxspvoucherROM104396EF584170
PeropteryxspvoucherRSV2330EF584171
PeropteryxtrinitatisEF584182
Phylloderma stenopsFJ155480
Phyllonycteris aphyllaAF187033
Phyllops  falcatusDQ211651
Phyllostomus  hastatusFJ155479
PipistrellusabramusAJ504448
Pipistrelluscf.javanicusAJ504447
PipistrellushesperidusAJ841968
PipistrellushesperusDQ421823
PipistrelluskuhliAJ504444
PipistrellusmaderensisAJ426632
PipistrellusnathusiiAJ504446
PipistrelluspipistrellusAJ504443
PipistrelluspygmaeusDQ120856
PipistrelluspygmaeusxmediterraneusAJ504442
Pipistrellussp.Be_2136_8AY426091
Pipistrellussp.Be_2137_9AY426092
Pipistrellussp.Be_2142_10AY426089
Pipistrellussp.Be_2145AY316334
Pipistrellussp.Be_2151_13AY426090
Pipistrellussp.Be_2152AY316332
Pipistrellussp.CO1EU420890
Pipistrellussp.CO2EU420891
Pipistrellussp.CO3EU420892
Pipistrellussp.PH-2007EF370417
Pipistrellussp.Be_2129AY316333
PipistrellussubflavusAJ504449
Platalina genovensiumAF423101
Platyrrhinus albericoiFJ154124
Platyrrhinus helleriFJ154141
Platyrrhinus helleriincarumFJ154146
Platyrrhinus masuFJ154164
Platyrrhinus matapalensisFJ154168
Platyrrhinus  aurariusFJ154127
Platyrrhinus  brachycephalusFJ154132
Platyrrhinus  dorsalisFJ154139
Platyrrhinus  lineatusFJ154160
Platyrrhinus  recifinusFJ154176
Platyrrhinus  vittatusFJ154178
PlecotusauritusEF570882
PlecotusaustriacusEU360707
PlecotusbalensisAF513798
Plecotuscf.kolombatoviciAF513783
PlecotuschristiiEU743801
PlecotuskolombatoviciAF513785
PlecotusmacrobullarisAF513805
PlecotusmexicanusAY776038
PlecotusrafinesquiiAY776084
Plecotussp.JJJ-2003AF513791
PlecotusteneriffaeEU360704
PromopscentralisL19732
Ptenochirus jagoriAB046325
Ptenochirus minorAY974702
Pteralopex acrodontaFJ561376
PteronotusdavyiAF338672
PteronotusgymnonotusAF338675
PteronotusmacleayiiAY604461
PteronotusparnelliiAY604456
PteronotuspersonatusAF338680
PteronotuspusillusAY604455
PteronotusquadridensAY604460
PteronotusrubiginosusAY604457
PteropusrufusAB085732
Pteropus aldabrensisFJ561394
Pteropus alectoAF144065                 
Pteropus conspicillatusFJ561380
Pteropus giganteusFJ561381
Pteropus hypomelanus FJ561383
Pteropus livingstonii FJ561384
Pteropus lylei EF584229
Pteropus nigerFJ561385
Pteropus poliocephalusFJ561387
Pteropus pumilusFJ561390
Pteropus rodricensisFJ561392
Pteropus scapulatusFJ561377
Pteropus seychellensisseychellensisFJ561399
Pteropus seychellensiscomoroensisFJ561398
Pteropus speciosusAB062474
Pteropus tonganusAF044656
Pteropus vampyrusFJ561401
Pteropus voeltzkowiFJ561405
Pygoderma bilabiatumAY604438
RhinolophusacumiatusEF108155
RhinolophusaffinisEU434934
RhinolophusblasiiEU436669
RhinolophusblythiDQ865344
RhinolophusborneensisEF108162
RhinolophusclivosusEU436674
RhinolophuscornutusDQ297594
RhinolophuscreaghiEF108164
RhinolophusdarlingiEU436675
RhinolophuseloquensEU436677
RhinolophuseurvaleEU436671
RhinolophusferrumequinumEU436673
RhinolophusformosaeNC_011304  
RhinolophusfumigatusEU436678
RhinolophushildebrandtiEU436676
RhinolophushipposiderosEU360631
RhinolophuslanderiFJ457612
RhinolophuslepidusAF451338
RhinolophusluctusEF544422
RhinolophusmacrotisEU434957
RhinolophusmarshalliEU434938
RhinolophusmehelyiEU436672
RhinolophusmonocerusEF555788
RhinolophuspearsoniiEU434940
RhinolophusperditusAY141039
RhinolophusphilippinensisEF108169
RhinolophuspumilusNC_005434
RhinolophuspusillusEF217392
RhinolophusrexEU075216
RhinolophussedulusEF108174
RhinolophussimulatorEU436670
RhinolophussinicusEU434941
Rhinolophussp.1KS-2008EU434937
Rhinolophussp.2KS-2008EU434942
RhinolophussthenoEF108175
RhinolophusthomasiEU434943
RhinolophustrifoliatusEF108177
RhinolophusxinanzhongguoensisEU750753
Rhinophylla alethinaAF187028
Rhinophylla fischeraeAF187032
Rhinophylla pumilioAF187031
RhinopomahardwickeiAY056462
RhinopomamicrophyllumAM931063
RhinopomamuscatellumDQ337500
RhogeessaaeneusEF222359
RhogeessagenowaysiEF222326
RhogeessagracilisEF222412
RhogeessaioEF222392
RhogeessamiraEF222336
RhogeessaparvulaEF222355
RhogeessatumidaEF222367
RhogeessavelillaEF222341
RhynchonycterisnasoEF584192
RousettusaegyptiacusEU624124
RousettusaegyptiacusaegyptiacusAF044658
RousettusaegyptiacusprincepsAF044659
RousettusamplexicaudatusAB046329
RousettusangolensisAF044643
RousettuslanosusAF044661
RousettusleschenaultiiFJ549331
RousettusmadagascariensisAF044663
RousettusspinalatusEF105523
SaccopterixbilineataEF584202
SaccopterixcanescensEF584206
SaccopterixgymnuraEF584208
SaccopterixlepturaEF584216
ScotomanesornatusDQ435069
ScotophilusborbonicusDQ459067
ScotophilusdinganiiEU750999
ScotophilusheathiiEU750946
ScotophiluskuhliiEU750931
ScotophilusleucogasterEU750940
ScotophilusmarovazaEU750943
ScotophilusnigritaEU750955
ScotophilusnuxEU750939
ScotophilusrobustusEU750948
ScotophilustandrefanaEU750941
Scotophilusviridis EU750991
Scotophilusviridis nigritellusEU750976
Sphaeronycteris toxophyllumAY604452 
Stenoderma rufumAY604431
SturniraluisiserotinusAF435170 
SturniraluisithomasiAF435250 
SturniraluisivulcanensisAF435251 
Sturnira aratathomasiAF435252 
Sturnira bidensAF435201 
Sturnira bogotensisAF435248 
Sturnira erythromosFJ154179
Sturnira ludoviciAF435235
Sturnira luisiangeliAF435158 
Sturnira luisipaulsoniAF435162 
Sturnira luisizygomaticusAF435159 
Sturnira magnaAF435180 
Sturnira mordaxAF435212 
Sturnira nanaAF435253 
Sturnira oporaphilumAF435210 
Sturnira sp.CAI-2003AAF435203 
Sturnira sp.CAI-2003BAF435204 
Sturnira  liliumAF187035
Sturnira  tildaeAF435185 
Syconycteris sp.AF044665
TadaridabrasiliensisL19734
TadaridafulminansEU760911
TadaridateniotisEU360721
TaphozouslongimanesEF584219
TaphozousmelanopogonEF584221
ThyropteratricolorAY621005
TomopeasravusL19735
Tonatia  bidensFJ155490
Tonatia  saurophilaFJ155488
Trachops cirrhosusFJ155483
TriaenopsaferEU798750
TriaenopsauritusDQ005794
TriaenopsfurculusDQ005845
TriaenopspersicusEU798758
TriaenopsrufusDQ005771
Triaenopssp.PPV-2008EU798756
TylonycterispachypusEF517315
Uroderma  bilobatumAY169955
Uroderma  magnirostrumFJ154180
Vampyressa bidensAY157055
Vampyressa melissaFJ154185
Vampyressa pusillaDQ312428
Vampyressa thyoneDQ312431
Vampyressa  brockiDQ312421
Vampyressa  nymphaeaDQ312418
Vampyrodes caraccioliFJ154184
Vampyrum spectrumFJ155482
VespertiliomurinusAB287359
VespertiliosinensisAB287362

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