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Bat Systematics in the Light of Unconstrained Analyses of a Comprehensive Molecular Supermatrix

Abstract

Bats (Chiroptera) represent the largest diversification of extant mammals after rodents. Here we report the results of a large-scale phylogeny of bats based on unconstrained searches for a data matrix of 804 non-chimeric, taxonomically updated bat terminals (796 species represented by a single terminal plus three species represented by ≥2 genetically distinct subspecies), able to preliminary test the systematics of most groups simultaneously. We used nine nuclear and mitochondrial DNA sequence markers fragmentary represented for ingroups (c. 90% and 64% of extant diversity at genus and species level, respectively) and 20 diverse placental outgroups. Maximum Likelihood and Parsimony analyses applied to the concatenated dataset yielded a highly resolved, variously supported phylogeny that recovered the majority of currently recognized clades at all levels of the chiropteran tree. Calibration points based on 44 key fossils allowed the Bayesian dating of bat origins at c. 4 my after the K-Pg boundary, and the determination of stem and crown ages of intraordinal clades. As expected, bats appeared nested in Laurasiatheria and split into Yinpterochiroptera and Yangochiroptera. More remarkable, all polytypic, currently recognized families were monophyletic, including Miniopteridae, Cistugidae, and Rhinonycteridae, as well as most polytypic genera with few expected exceptions (e.g., Hipposideros). The controversial Myzopodidae appeared in a novel position as sister of Emballonuroidea―a result with interesting biogeographic implications. Most recently recognized subfamilies, genera, and species groups were supported or only minor adjustments to the current taxonomy would be required, except Molossidae, which should be revised thoroughly. In light of our analysis, current bat systematics is strongly supported at all levels; the emergent perception of a strong biogeographic imprint on many recovered bat clades is emphasized.

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Acknowledgements

We thank the support from Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina, grant PICT 2008–1798 to NPG, and grants PICT 1930_2011 and PIP 0260 to SAC.

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Correspondence to Norberto P. Giannini.

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Fig S1.

Pteropodidae. A: Cynopterinae; B: Cynopterini; C: Balionycterini; D: Scotonycterini; E: Rousettinae; F: Eonycterini; G: Rousettini; H: Stenonycterini; I: Myonycterini; J: Epomophorini; K: Macroglossinae; L: Harpyionycterinae; M: Eidolinae; N: Nyctimeninae; O: Pteropodinae (JPEG 3447 kb)

High resolution image (TIFF 5864 kb)

Fig S2.

Rhinolophoidea. A: African Hipposideros species; B: Asian Hipposideros species; C: Afro-Paleartic Rhinolophus clade; D: Indomalayan Rhinolophus clade (JPEG 3767 kb)

High resolution image (TIFF 6448 kb)

Fig S3.

Yangochiroptera. A: Asian Nycteris clade; B: African Nycteris clade; C: Taphozoinae; D: Emballonurinae; E: Emballonurini; F: Diclidurini; G: Afro-Malagasy emballonurini genera; H: Indo-Pacific emballonurini genus; I: Chaerephon/Mops group; J: Otomops group; K: New World Molossidae group; L: Oriental-Australasian Miniopterus clade; M: Ethiopian Miniopterus clade; N: Indian Ocean Miniopterus clade (JPEG 4114 kb)

High resolution image (TIFF 6878 kb)

Fig S4.

Relationships within Phyllostomidae. The subfamilies are indicated in bold (JPEG 4357 kb)

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Fig S5.

Relationships within Vespertilionidae (part 1: Kerivoulinae, Murininae, Myotinae). A: New World Myotis clade; B: Paleartic lineage “brandtii”; C: Neartic clade; D: Neotropical clade; E: Old World Myotis clade; F: Ethiopian clade; G: Euroasian clade (JPEG 3654 kb)

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Fig S6.

Relationships within Vespertilionidae (part 2: Vespertilioninae). The tribes are indicated in bold (JPEG 3972 kb)

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Fig S7.

Pteropodidae. A: Cynopterinae; B: Cynopterini; C: Balionycterini; D: Scotonycterini; E: Rousettinae; F: Eonycterini; G: Rousettini; H: Stenonycterini; I: Myonycterini; J: Epomophorini; K: Macroglossinae; L: Harpyionycterinae; M: Eidolinae; N: Nyctimeninae; O: “Pteropodinae” (JPEG 3509 kb)

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Fig S8.

Rhinolophoidea. A: African Hipposideros species; B: Asian Hipposideros species; C: Afro-Paleartic Rhinolophus clade (JPEG 3578 kb)

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Fig S9.

Yangochiroptera. A: Asian Nycteris clade; B: African Nycteris clade; C: Taphozoinae; D: Emballonurinae; E: Emballonurini; F: Diclidurini; G: Afro-Malagasy emballonurini genera; H: Indo-Pacific emballonurini genus; I: New World Molossidae group; J: Otomops group; K: Oriental-Australasian Miniopterus clade; L: Ethiopian Miniopterus clade; M: Indian Ocean Miniopterus clade (JPEG 3901 kb)

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Fig S10.

Relationships within Phyllostomidae. The subfamilies are indicated in bold (JPEG 3877 kb)

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Fig S11.

Relationships within Vespertilionidae (part 1: Kerivoulinae, Murininae, Myotinae). A: New World Myotis clade; B: Paleartic lineage “brandtii”; C: Neartic clade; D: Neotropical clade; E: Old World Myotis clade; F: Ethiopian clade; G: Euroasian clade; H: Oriental clade (JPEG 3563 kb)

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Fig S12.

Relationships within Vespertilionidae (part 2: Vespertilioninae). The tribes are indicated in bold (JPEG 4337 kb)

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Fig S13.

Outgroups (JPEG 608 kb)

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Fig S14.

Yinpterochiroptera (JPEG 2716 kb)

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Fig S15.

Yangochiroptera (in part): Noctilionoidea + Emballonuroidea (JPEG 2677 kb)

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Fig S16.

Yangochiroptera (in part): Vespertilionoidea (JPEG 3078 kb)

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Fig S17.

Complete molecular dating obtained from a Bayesian analysis (PDF 72 kb)

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Amador, L.I., Moyers Arévalo, R.L., Almeida, F.C. et al. Bat Systematics in the Light of Unconstrained Analyses of a Comprehensive Molecular Supermatrix. J Mammal Evol 25, 37–70 (2018). https://doi.org/10.1007/s10914-016-9363-8

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  • DOI: https://doi.org/10.1007/s10914-016-9363-8

Keywords

  • Chiroptera
  • Phylogeny
  • Molecular dating
  • Maximum likelihood
  • Parsimony