Phylogeography of a widespread small carnivore, the western spotted skunk (Spilogale gracilis) reveals temporally variable signatures of isolation across western North America.

Adam W Ferguson,Molly M Mcdonough,Gema I Guerra,Robert C Dowler,Margaret Rheude,Loren K Ammerman,Jerry W Dragoo

doi:10.1002/ece3.2931

Abstract

We analyzed phylogeographic patterns in the western spotted skunk, Spilogale gracilis Merriam, 1890 (Carnivora: Mephitidae) in relation to historical events associated with Pre‐Pleistocene Divergence (PPD) and Quaternary climate change (QCC) using mitochondrial DNA from 97 individuals distributed across Western North America. Divergence times were generated using BEAST to estimate when isolation in putative refugia occurred. Patterns and timing of demographic expansion was performed using Bayesian skyline plot. Putative climatic refugia resulting from Quaternary climate change were identified using paleoecological niche modeling and divergence dates compared to major vicariant events associated with Pre‐Pleistocene conditions. We recovered three major mitochondrial clades corresponding to western North America (California, Baja, and across the Great Basin), east‐central North America (Texas, central Mexico, New Mexico), and southwestern Arizona/northwestern Mexico. Time to most recent common ancestor for S. gracilis occurred ~1.36 Ma. Divergence times for each major clade occurred between 0.25 and 0.12 Ma, with signature of population expansion occurring 0.15 and 0.10 Ma. Ecological niche models identified three potential climatic refugia during the Last Interglacial, (1) west coast of California and Oregon, (2) northwestern Mexico, and (3) southern Texas/northeastern Mexico as well as two refugia during the Last Glacial Maximum, (1) western USA and (2) southern Texas/northeastern Mexico. This study supports PPD in shaping species‐level diversity compared to QCC‐driven changes at the intraspecific level for Spilogale, similar to the patterns reported for other small mammals (e.g., rodents and bats). Phylogeographic patterns also appear to have been shaped by both habitat and river vicariance, especially across the desert southwest. Further, continuing climate change during the Holocene coupled with anthropogenic modifications during the Anthropocene appears to be removing both of these barriers to current dispersal of western spotted skunks.

Highlights

Recent phylogeographic studies of a diverse array of North American plants and animals have resulted in identification of broadscale patterns of genetic variation attributable to both Pre-Pleistocene Divergence (PPD) resulting from vicariance and Quaternary climate change (QCC) associated with expansion and contraction of glaciers during the Pleistocene-Holocene (Hewitt, 2004)
This broad ecological niche combined with the estimated age and distribution of this lineage across a well-studied but complex biogeographic region makes this species well-suited for analyses of the relative influence of PPD and QCC in shaping phylogeographic patterns of small carnivores across western North America
Using mitochondrial DNA and ecological niche modeling, we explored patterns of genetic variation and divergence time estimates for S. gracilis and other Spilogale species in relation to well- characterized events associated with PPD as well as fluctuating climates attributable to QCC across western North America

Summary

| INTRODUCTION

Recent phylogeographic studies of a diverse array of North American plants and animals have resulted in identification of broadscale patterns of genetic variation attributable to both Pre-Pleistocene Divergence (PPD) resulting from vicariance and Quaternary climate change (QCC) associated with expansion and contraction of glaciers during the Pleistocene-Holocene (Hewitt, 2004). Recent work on wide-ranging species whose distributions encompass all or parts of these three regions have begun to emerge, including work on both large [e.g., mule deer Odocoileus hemionus (Latch et al, 2014), bighorn sheep Ovis canadensis (Buchalski et al, 2016); black bear Ursus americanus (Puckett, Etter, Johnson, & Eggert, 2015)] and small [e.g., Antelope squirrels of the genus Ammospermophilus (Mantooth, Hafner, Bryson, & Riddle, 2013); harvest mouse Reithrodontomys megalotis (Nava-García et al, 2016)] mammals These shed light on how wide-ranging, vertebrate taxa with broad ecological niches respond to biogeographic events associated with different historical signatures. The catholic choice of habitat maintained by S. gracilis makes it well-suited for examining patterns of genetic subdivision associated with QCC This broad ecological niche combined with the estimated age and distribution of this lineage across a well-studied but complex biogeographic region makes this species well-suited for analyses of the relative influence of PPD and QCC in shaping phylogeographic patterns of small carnivores across western North America. We predict that S. gracilis will show phylogeographic patterns intermediate to those of larger, more mobile species and smaller, less mobile species, with species-level divergence occurring around well-defined phylogeographic breaks associated with PPD followed by population-level divergence associated with QCC

| MATERIALS AND METHODS

| DISCUSSION

| CONCLUSIONS

Findings

CONFLICT OF INTEREST