Four Lineages in Peromyscus leucopus
In all analyses, the most divergent lineage was the Southwest lineage, a
group found in Mexico, New Mexico, Texas, and southern Oklahoma.
Multiple lines of evidence support divergence of the Southwest lineage,
namely the highest estimated divergence time in BEAST
(~25kya) and Fst values among all between lineage
comparisons. Furthermore, the Southwest lineage roughly correspond to
the previously defined western chromosomal race as identified in Baker
et al. (1983). Baker et al. (1983) found that the chromosomal races meet
at an ecotone transition between the Great Plains and eastern temperate
forests (Strangl 1986) in Oklahoma, Kansas, and northern Texas. Our
analysis extends the contact zone beyond Oklahoma to include eastern
Texas and New Mexico, boundaries largely coincident with habitat
transitions between grassland/desert and forests. A similar pattern of
divergence is observed in the more cosmopolitan Peromyscus
maniculatus where habitat is thought to reinforce divergence between
putative species and lineages (Kalvik et al. 2012). Indeed, most
lineages associated with forest and grassland habitats were once
allopatric during the Pleistocene (Kalvik et al. 2012). Contact zones
also occurred at habitat transitions, much like the breaks between the
Southwest lineage and the remaining groups.
We believe the contact zone between the Southwest and the other lineages
identified here exists in the southern Great Plains as observed in
Strangl et al. (1986) where eastern deciduous forests transition into
grassland habitats (i.e., eastern Oklahoma, Kansas, and Texas). This
habitat transition acts as a contact zone between eastern and western
lineages in both birds (Rising 1983) and mammals that were isolated
during the Pleistocene (Reding et al. 2012, Kierepka et al. 2023), but
levels of differentiation vary greatly across taxa. While our analysis
presents evidence for fairly strong differentiation of southwesternP. leucopus , further study is needed to clarify this
relationship. Mitochondrial DNA does not provide the full picture of
evolutionary history due to its maternal inheritance and differing
evolutionary rates. Reclassification has occurred in otherPeromyscus species including P. maniculatus , which was
separated into six species based on numerous genetic, ecological, and
morphological studies (e.g., Dragoo et al. 2006, Kalvik et al. 2012,
Greenbaum et al. 2019). The Southwest lineage could be a cryptic species
as observed in the P. maniculatus species group (P.
maniculatus and. P. sonoriensis ), but nuclear DNA should confirm
differentiation and patterns of hybridization within the contact zone.
Unlike the Southwest lineage, the East and Midwest lineages are
primarily found in forested habitats. Splits between these lineages were
aged at ~20,000 years ago during the Last Glacial Maximum
(LGM) and received strong support in the haplotype network, PCoA, and
Fst analyses. We acknowledge these estimates may be underestimations
based on previous estimates (e.g. Moscarella et al. 2019, Prado et al.
2019). However, our TMRCA remained in the Pleistocene, which supports
previous findings of two Pleistocene lineages separated by the Great
Lakes and the St. Lawrence River (Rowe et al. 2006, Fiset et al. 2015,
Baumgartner and Hoffman 2019, Moscarella et al. 2019, Prado et al.
2022). Beyond the Great Lakes and northeastern United States/Canada,
East has the largest geographic distribution of P. leucopus’ lineages, extending along the entire eastern coast and Appalachians into
western Tennessee, Alabama, and Louisiana. We also recorded East
individuals in Wisconsin and Illinois whereas the Midwest lineage was
largely confined to northern Midwest states including Minnesota,
Illinois, the Upper Peninsula of Michigan, Wisconsin, Nebraska, and
North Dakota. These areas largely correspond with the different
hypothesized colonization routes taken following the LGM in the East and
Midwest lineages and large water barriers that existed prior to the LGM
(Rowe et al. 2006, Fiset et al. 2015, Moscarella et al. 2019, Prado et
al. 2022). With the greater coverage of the reduced dataset, we found
that East and Midwest co-occur in Indiana and Illinois along with the
Central lineage. All three lineages crossed the Mississippi River, so we
did not find evidence for it as a barrier.
While Southwest, East, and Midwest were highly supported in every
analysis, the Central lineage is the least distinct. Central did not
receive high support in the BEAST analysis, had the youngest divergence
time, and was in the middle of the haplotype network and PCoA. Fst
metrics were also smallest in Central comparisons. Interestingly,
Central was placed sister to East in the phylogenetic tree, but was the
least differentiated from Southwest in the PCoA and haplotype network.
Rowe et al. (2006)’s dataset placed Central sister to the Midwest
lineage, but also did not receive high support in the phylogeny. Fst
values were the smallest between Central and Southwest, which appears to
support that Central is more closely related to Southwest. Central also
does not occur east of Indiana and primarily occurs in Missouri, east
Texas, Louisiana, Illinois, Indiana, and northern New Mexico. All these
areas are largely forested, which may indicate habitat-based
differentiation between Southwest and Central or a separate refugium
like the Ozarks. The hypothesized refugium for the Midwest lineage
occurred in Illinois (Rowe et al. 2006), so another isolated refugium
within a southern area is most likely for Central. We cannot discount
that these results could be due to low sample sizes of Central or
homoplasy. Much of our eastern Central individuals were from Genbank,
and therefore, only had control region sequences, a marker more
susceptible to homoplasy than slower evolving regions. This lineage was
also detected in Herrera (2021), which used cytochrome b, so homoplasy
in two markers is unlikely for the Central lineage. Consequently, more
data is needed to elucidate the evolutionary relationship of Central to
the other lineages.