Conflicting Evolutionary Histories of the Mitochondrial and Nuclear Genomes in New World Myotis Bats

Abstract

The rapid diversification of Myotis bats into more than 100 species is one of the most extensive mammalian radiations available for study. Efforts to understand relationships within Myotis have primarily utilized mitochondrial markers and trees inferred from nuclear markers lacked resolution. Our current understanding of relationships within Myotis is therefore biased towards a set of phylogenetic markers that may not reflect the history of the nuclear genome. To resolve this, we sequenced the full mitochondrial genomes of 37 representative Myotis, primarily from the New World, in conjunction with targeted sequencing of 3648 ultraconserved elements (UCEs). We inferred the phylogeny and explored the effects of concatenation and summary phylogenetic methods, as well as combinations of markers based on informativeness or levels of missing data, on our results. Of the 294 phylogenies generated from the nuclear UCE data, all are significantly different from phylogenies inferred using mitochondrial genomes. Even within the nuclear data, quartet frequencies indicate that around half of all UCE loci conflict with the estimated species tree. Several factors can drive such conflict, including incomplete lineage sorting, introgressive hybridization, or even phylogenetic error. Despite the degree of discordance between nuclear UCE loci and the mitochondrial genome and among UCE loci themselves, the most common nuclear topology is recovered in one quarter of all analyses with strong nodal support. Based on these results, we re-examine the evolutionary history of Myotis to better understand the phenomena driving their unique nuclear, mitochondrial, and biogeographic histories.

Population genetics revealMyotis keenii(Keen’s myotis) andMyotis evotis(long-eared myotis) to be a single species

“…This pattern may reflect the complex landscape forms that facilitate and limit gene flow such as high elevation mountains and low-lying river valleys. Platt et al (2018) shows complete discordance between mtDNA (single locus) and nuclear-derived (thousands of loci) species trees. These results provide cautionary examples of the risks of using any single marker to study relationships (Platt et al 2018), particularly if that single marker only records the gene flow mediated by one sex (e.g.…”

“…Stemming from the suggestion by Carstens and Dewey (2010) gene-flow' models of phylogeny, concluding gene flow occurred among these taxa during divergence prior to the Pleistocene. Until Platt et al (2018) and Morales et al (2017), phylogenies of Myotis were based on mtDNA (Dewey 2006) or combinations of mtDNA and nuclear sequences (Stadelmann et al 2007;Carstens and Dewey 2010), in which mtDNA may have swamped potentially conflicting signals from nuclear markers (Platt et al 2018). Platt et al's (2018) separate analyses of mitochondrial versus nuclear sequences revealed consistently conflicting gene trees between these markers, concluding that bifurcating phylogenies based on a single gene (ie.…”

“…Examination of M. evotis and M. keenii based solely on nuclear DNA includesPlatt et al (2018) and this study. The former included nuclear sequencing of one individual per species (1 M. evotis from Mexico and 1 M. keenii from Alaska).…”

Bat Biology, Genomes, and the Bat1K Project: To Generate Chromosome-Level Genomes for All Living Bat Species

“…This is particularly true for bats, for which many species are likely to have undergone rapid radiation, diversification, and potentially hybridization and/or incomplete lineage sorting (135)(136)(137)(138). In particular, genome-level data sets should at best be able to account for the phylogenetic noise inherent in analyses of single genes or at worst at least clearly indicate the degree of noise that they impart (139).…”

Porous barriers? Assessment of gene flow within and among sympatric long‐eared bat species

“…Yet, in the speciose order of Chiroptera, accounting for 20% of all mammal species (Burgin, Colella, Kahn, & Upham, 2018), cases of hybridization appear to be rare. For instance, the family Vespertilionidae contains about 500 species but only includes very few well-documented cases of interspecific hybrids (Afonso, Goydadin, Giraudoux, & Farny, 2017;Berthier, Excoffier, & Ruedi, 2006;Centeno-Cuadros et al, 2017), whereas cases of historical events of gene introgression exemplified by cytonuclear discrepancies are more common (Artyushin, Bannikova, Lebedev, & Kruskop, 2009;Baird, Hillis, Patton, & Bickham, 2008;Kuo et al, 2015;Morales & Carstens, 2018;Morales, Jackson, Dewey, O'meara, & Carstens, 2017;Platt et al, 2017;Trujillo, Patton, Schlitter, & Bickham, 2009;Vallo, Benda, Červený, & Koubek, 2013). However, it is possible that contemporary interspecific hybridization is underestimated, since most of the taxonomic studies conducted on bats usually rely only on mitochondrial genes for species-level recognition (Baker & Bradley, 2006;Clare, Lim, Engstrom, Eger, & Hebert, 2007;Francis et al, 2010).…”