A precarious future for distinctive peripheral populations of meadow voles (Microtus pennsylvanicus)

Abstract

Conservation efforts rely on robust taxonomic assessments that should be based on critical assessment of interspecific boundaries, infraspecific variation, and potentially distinctive peripheral populations. The meadow vole (Microtus pennsylvanicus) is widely distributed across North America, including 28 morphologically defined subspecies and numerous isolated populations. Because some subspecies are of high conservation concern, we examined geographic variation across the range of the species to test existing infraspecific taxonomy in terms of local and regional diversification. We sequenced mitochondrial DNA (mtDNA) from 20 subspecies of M. pennsylvanicus and contextualized infraspecific variation through comparison of pairwise genetic distances derived from an extended data set of 63 species of Microtus. We found strong support for at least three divergent clades within M. pennsylvanicus, with observed intraspecific clade divergence exceeding that between several pairwise comparisons of sister species within Microtus. Six nuclear genes were then sequenced to test the validity of mtDNA structure and to further evaluate the possibility of cryptic, species-level diversity using Bayes factor species delimitation (BFD) analyses. BFD consistently and decisively supported multiple species based on the multilocus approach. We propose that taxonomic revision of the meadow vole is required, with the eastern clade now identified as M. pennsylvanicus (Ord 1815), the western clade as M. drummondii (Audubon and Bachman 1853), and the coastal Florida clade as M. dukecampbelli (Woods, Post, and Kilpatrick 1982). We suggest that such an arrangement would more closely reflect evolutionary history and provide critical context for further examination of distinctive southern peripheral populations that harbor novel evolutionary legacies and adaptive potential.

Genomic resources for the North American water vole (Microtus richardsoni) and the montane vole (Microtus montanus)

“…The genus Microtus consists of 62 species of voles distributed throughout North America, Europe, and Asia [1]. Microtus is believed to have experienced rapid speciation and diversification, with all speciation events occurring within the past four million years [2, 3], and it has been suggested that some nominal species, such as M. pennsylvanicus , contain cryptic diversity [4]. Microtus has been an important model system across multiple biological disciplines, including studies of adaptation (e.g., [5]), infectious disease (e.g., [6]), parental care (e.g., [7]), and population dynamics (reviewed in [8]).…”

Island biogeography predicts skull gigantism and shape variation in meadow voles Microtus pennsylvanicus through ecological release and allometry

“…1). In the Atlantic region, we compared 11 island and mainland populations ranging 8.0 degrees latitude (38°05'24''–46°05'24''N), which fall into the eastern mitochondrial clade identified by Jackson and Cook (2020). In this sample, the island populations form two clusters: Fox and Islesboro Islands in the north off the coast of Maine, and Nantucket, Long Island and others clustering around the coasts of New York and Cape Cod to the south.…”

“…In this system, islands were connected to the mainland during the last glacial maximum (LGM), providing opportunity for potential widespread dispersal (Weddle and Choate 1983, Darvill et al 2018). So, current island occupants were likely marooned with rising sea levels rather than colonized islands via over‐water dispersal (Weddle and Choate 1983, Jackson and Cook 2020).…”

Climate relict vulnerable to extinction from multiple climate‐driven threats

“…Such shifts have already been observed within the range of voles, and are likely to continue if winters become increasingly mild (Osland et al, 2013(Osland et al, , 2020Stevens et al, 2006). Thus, despite the persistence of voles since the Pleistocene, novel climate-mediated factors may threaten this climate relict (Hotaling et al, 2010;Jackson & Cook, 2020).…”

“…The Florida saltmarsh vole (Microtus pennsylvanicus dukecampbelli; hereafter: "vole") is a climate relict from the Pleistocene epoch when the global climate was cooler (Woods et al, 1982). Though previously considered a subpopulation of the more widespread meadow vole (Microtus pennsylvanicus), more recent genetic analysis indicated that the population likely represents a distinct species (Jackson & Cook, 2020). Meadow voles appear to have been more widespread in Florida during the Pleistocene, but their southern range limit contracted poleward as the climate warmed during the Holocene (Jackson & Cook, 2020;Martin, 1968;Woods et al, 1982).…”