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

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).

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“…The yellow bats of the genus Dasypterus were reciprocally monophyletic with respect to the (Lasiurus, Aeorestes) clade (Fig 4), in congruence with previously published phylogenies based on mtDNA, nuclear and Y-Chromosome genes [60,61]. It is worth noting that the sequence of the species Dasypterus xanthinus is annotated in Genbank (Accession Number AF369549) as Lasiurus xanthinus.…”

Observations on the Distribution and Status of Selected Nebraska Mammals

“…This species has been known under the scientific name of Lasiurus cinereus for many years, but recent molecular studies have shown that the relationships of members of the genus Lasiurus are best represented by dividing them into three genera-red (Lasiurus), hoary (Aeorestes), and yellow (Dasypterus) bats. Another result of these studies is treating A. cinereus as monotypic (Baird et al 2015(Baird et al , 2017, although debate on this taxonomic interpretation is ongoing (see Ziegler et al 2016, Novaes et al 2018.…”

Patagonian bats: new size limits, southernmost localities and updated distribution for Lasiurus villosissimus and Myotis dinellii (Chiroptera: Vespertilionidae)

“…The taxonomy of the tribe Lasiurini within Vespertilionidae is being reviewed, and molecular studies suggest a split in three different genera: Lasiurus [red bats, e.g. Lasiurus blossevillii (Lesson 1826 Baird et al 2015Baird et al , 2017. In the present work, however, we follow Ziegler et al (2016) and Novaes et al (2018b) and consider Aeorestes as a subgenus of Lasiurus.…”

“…In the present work, however, we follow Ziegler et al (2016) and Novaes et al (2018b) and consider Aeorestes as a subgenus of Lasiurus. Molecular evidence also provided support to treat the subspecies Lasiurus cinereus villosissimus as a full species (Baird et al 2015(Baird et al , 2017. So according to these studies, we considered Lasiurus villosissimus (É. Geoffroy St.-Hilaire 1806) as the hoary bat widely distributed in South America, in accordance with Teta et al (2018).…”