The biogeographic legacy of an imperilled taxon provides a foundation for assessing lineage diversification, demography and conservation genetics

Abstract

Aim To test alternative biogeographic hypotheses related to the diversification of a montane mammal (Zapus hudsonius luteus) endemic to the American Southwest. Location South‐western United States. Methods We used statistical phylogeographic analyses of mitochondrial DNA (1512 bp; two genes) from 93 individuals from six geographic regions to test diversification hypotheses. Species distribution models of climate and fossil records were integrated to assess contemporary and historical distributions and barriers to gene flow. We calculated dates of divergence and examined historical demography using coalescent simulations. Results We documented monophyly of Z. h. luteus represented by 19 segregated haplotypes. Predicted current distribution generally coincided with known localities, while predicted paleodistributions suggested that this lineage was widespread throughout lower elevations of the American Southwest and on the Edwards Plateau (as documented by the fossil record). Population size did not change substantially during a westward shift in range that occurred in the last 100 k generations. Results supported fragmentation of a common ancestor during the Holocene as the most plausible explanation for genetic structure. Main conclusions Monophyletic Z. h. luteus reflects fragmentation of a common ancestor with recent (Holocene) upslope colonization of disjunct montane areas. We refute the hypotheses of in situ divergence or origins from a Colorado Piedmont ancestor. Instead, westward colonization from the Edwards Plateau during the Wisconsin followed by Holocene fragmentation, which serves as a generalized biogeographic hypothesis for species associated with mesic graminoid habitats in the American Southwest. Further exploration of these signatures using independent nuclear DNA is warranted. Key conservation implications are (1) Z. h. luteus is a monophyletic lineage on an independent evolutionary trajectory; (2) Z. h. luteus shared a recent common ancestor with Z. h. pallidus (not Z. h. preblei); (3) mtDNA does not reflect recent population declines; and (4) coalescent simulations and species distribution models reflect Holocene fragmentation.

Using biogeographical history to inform conservation: the case of Preble's meadow jumping mouse

“…(iv) Demographic Stability but Spatial Shift (Malaney et al . ). Finally, the Coastal, Southern Plains and the Southwestern lineage shifted from ancestral ranges, but experienced no significant demographic change.…”

“…) and anthropogenic fragmentation (Andren ) that may precipitate jumping mice declines (Frey & Malaney ; Malaney et al . ). Conversely, high‐latitude lineages of zapodids are the result of expanded ranges during the warming phase of the Holocene epoch (Lessa et al .…”

Phylogeography of the western jumping mouse (Zapus princeps) detects deep and persistent allopatry with expansion

“…Our h estimates (effective population size scaled to the neutral mutation rate) were calibrated to recent fossil dates using the equation h ¼ 4N E(f) l, assuming l ¼ 3.14 substitutions per million years as calculated by Malaney et al (2012) and scaled branch widths of h were used for the competitive hypotheses.…”

Timing of hibernation and reproduction in the endangered New Mexico meadow jumping mouse (Zapus hudsonius luteus)

“…Zapus h. luteus is a well-differentiated form that is endemic to the American Southwest, including portions of southern Colorado, New Mexico, and central and eastern Arizona (Hafner et al 1981, Frey 2012, Malaney et al 2012. Zapus h. luteus is a specialist of riparian habitats and hence its distribution includes both low elevation sites within desert biomes and high elevation sites within coniferous forest biomes Malaney 2009, Malaney et al 2012 Morrison 1988, Najera 1994.…”