Westward range expansion from middle latitudes explains the Mississippi River discontinuity in a forest herb of eastern North America

Abstract

It is often expected that temperate plants have expanded their geographical ranges northward from primarily southern refugia. Evidence for this hypothesis is mixed in eastern North American species, and there is increasing support for colonization from middle latitudes. We studied genome‐wide patterns of variation in RADseq loci to test hypotheses concerning range expansion in a North American forest herb (Campanula americana). First, spatial patterns of genetic differentiation were determined. Then phylogenetic relationships and divergence times were estimated. Spatial signatures of genetic drift were also studied to identify the directionality of recent range expansion and its geographical origins. Finally, spatially explicit scenarios for the spread of plants across the landscape were compared, using variation in the population mutation parameter and Tajima's D. We found strong longitudinal subdivision, with populations clustering into groups west and east of the Mississippi River. While the southeastern region was probably part of a diverse Pleistocene refugium, there is little evidence that range expansion involved founders from these southern locales. Instead, declines in genetic diversity and the loss of rare alleles support a westward colonization wave from a middle latitude refugium near the southern Appalachian Mountains, with subsequent expansion from a Pleistocene staging ground in the Mississippi River Valley (0.51–1.27 million years ago). These analyses implicate stepping stone colonization from middle latitudes as an important mechanism of species range expansion in eastern North America. This study further demonstrates the utility of population genetics as a tool to infer the routes travelled by organisms during geographical range expansion.

Hybrid breakdown is elevated near the historical cores of a species' range

“…The resulting dataset contained 2605 RAD loci with an average of 2.5 SNPs per RAD locus. Genotypic data were then used to count the number of nucleotide differences within populations using Watterson's and Tajima's estimators of θ [32]. Pairwise F ST among populations was estimated using analysis of variance implemented in the StAMPP R package [42,43].…”

“…Genetic structure among populations in the Western clade and standing levels of within-population genetic diversity reflect a complex evolutionary history involving Pleistocene range expansion. Spatial signatures of genetic drift including declines in genetic diversity and the loss of rare alleles support westward colonization from a mid-latitude refugium near the southern Appalachian Mountains [31,32]. Within this westward expansion, a staging ground in the Mississippi River Valley was the source of subsequent colonization west of the Mississippi River, resulting in a genetic discontinuity among populations that largely coincides with the Mississippi River (figure 1; [32,33]).…”

“…Another signature of genetic structure in the Western clade indicates ancient genetic subdivision between most populations and those at the southern range margin, where suitable Pleistocene habitats for C. americana were concentrated near the Gulf Coast [33]. Indeed, populations nearest the Gulf Coast are the earliest diverging lineages relative to all other populations in the Western clade [32,33] suggesting this genetic subdivision was preserved as the leading edge of the species' range expansion advanced in a primarily western direction.…”

“…In C. americana , a recent range expansion has geographically structured patterns of genetic diversity and differentiation [31] (figure 1). Populations farther from a mid-latitude glacial refugium maintain fewer nucleotide polymorphisms (figure 1 b ; [32]), and contemporary populations at extreme latitudes are the most genetically differentiated (figure 1 c ). Phylogenomic studies and habitat suitability models also implicate the southern Gulf Coast as an important refugial region for C. americana [32,33].…”

“…Populations farther from a mid-latitude glacial refugium maintain fewer nucleotide polymorphisms (figure 1 b ; [32]), and contemporary populations at extreme latitudes are the most genetically differentiated (figure 1 c ). Phylogenomic studies and habitat suitability models also implicate the southern Gulf Coast as an important refugial region for C. americana [32,33]. We address the following questions: (i) does variability in F 2 hybrid breakdown covary with distance from regions of glacial refugia?…”