Nuclear and mtDNA phylogenetic analyses clarify the evolutionary history of two species of native Hawaiian bats and the taxonomy of Lasiurini (Mammalia: Chiroptera).

Amy B Baird,Mark D Engstrom,Burton K Lim,John C Patton,Ashlyn C Holbert,John W Bickham,Michael A Mares,Maritza G Huerta,Janet K Braun,William J Etges

doi:10.1371/journal.pone.0186085

Amy B Baird, Mark D Engstrom + Show 8 more

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https://doi.org/10.1371/journal.pone.0186085

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Abstract

Previous studies on genetics of hoary bats produced differing conclusions on the timing of their colonization of the Hawaiian Islands and whether or not North American (Aeorestes cinereus) and Hawaiian (A. semotus) hoary bats are distinct species. One study, using mtDNA COI and nuclear Rag2 and CMA1, concluded that hoary bats colonized the Hawaiian Islands no more than 10,000 years ago based on indications of population expansion at that time using Extended Bayesian Skyline Plots. The other study, using 3 mtDNA and 1 Y-chromosome locus, concluded that the Hawaiian Islands were colonized about 1 million years ago. To address the marked inconsistencies between those studies, we examined DNA sequences from 4 mitochondrial and 2 nuclear loci in lasiurine bats to investigate the timing of colonization of the Hawaiian Islands by hoary bats, test the hypothesis that Hawaiian and North American hoary bats belong to different species, and further investigate the generic level taxonomy within the tribe. Phylogenetic analysis and dating of the nodes of mtDNA haplotypes and of nuclear CMA1 alleles show that A. semotus invaded the Hawaiian Islands approximately 1.35 Ma and that multiple arrivals of A. cinereus occurred much more recently. Extended Bayesian Skyline plots show population expansion at about 20,000 years ago in the Hawaiian Islands, which we conclude does not represent the timing of colonization of the Hawaiian Islands given the high degree of genetic differentiation among A. cinereus and A. semotus (4.2% divergence at mtDNA Cytb) and the high degree of genetic diversity within A. semotus. Rather, population expansion 20,000 years ago could have resulted from colonization of additional islands, expansion after a bottleneck, or other factors. New genetic data also support the recognition of A. semotus and A. cinereus as distinct species, a finding consistent with previous morphological and behavioral studies. The phylogenetic analysis of CMA1 alleles shows the presence of 2 clades that are primarily associated with A. semotus mtDNA haplotypes, and are unique to the Hawaiian Islands. There is evidence for low levels of hybridization between A. semotus and A. cinereus on the Hawaiian Islands, but it is not extensive (<15% of individuals are of hybrid origin), and clearly each species is able to maintain its own genetic distinctiveness. Both mtDNA and nuclear DNA sequences show deep divergence between the 3 groups (genera) of lasiurine bats that correspond to the previously recognized morphological differences between them. We show that the Tribe Lasiurini contains the genera Aeorestes (hoary bats), Lasiurus (red bats), and Dasypterus (yellow bats).

Highlights

Hoary bats (Lasiurini: Aeorestes) are unique among land mammals, in that they include the only extant mammal species native to the Hawaiian Islands
Aeorestes cinereus occurs in North America and the Hawaiian Islands, A. semotus is restricted to the Hawaiian Islands, A. villosissimus is found in South America, and the more distantly related A. egregius occurs in Panama and northern South America, and previously was considered to be related to red bats based on morphology
An insertion of 222–228 base pairs was present in some yellow bat species in CMA1. It was present in D. ega (North and South American forms), D. insularis, and D. intermedius but not D. xanthinus

Summary

Introduction

Hoary bats (Lasiurini: Aeorestes) are unique among land mammals, in that they include the only extant mammal species native to the Hawaiian Islands. Russell et al [2] sequenced mitochondrial COI, and nuclear Rag and CMA1 (which they referred to as CHY; here we use the NCBI accepted abbreviation of CMA1 for the chymase gene) They utilized extended Bayesian skyline plots (EBSP) to understand historical population size changes in hoary bats and used them to estimate the time of colonization of Hawaii by lasiurines. Baird et al [1] sequenced mitochondrial Cytb, ND1, ND2, and the Y-chromosomal DBY locus to conduct a molecular systematic revision of Lasiurini They implemented maximum likelihood and Bayesian analyses of each gene separately, as well as ÃBEAST species tree analysis of combined data. Outgroups included Eptesicus nilssoni, Myotis formosus, M. lucifugus, M. velifer and/or Tadarida brasiliensis

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