Range instability leads to cytonuclear discordance in a morphologically cryptic ground squirrel species complex

Abstract

The processes responsible for cytonuclear discordance frequently remain unclear. Here, we employed an exon capture dataset and demographic methods to test hypotheses generated by species distribution models to examine how contrasting histories of range stability vs. fluctuation have caused cytonuclear concordance and discordance in ground squirrel lineages from the Otospermophilus beecheyi species complex. Previous studies in O. beecheyi revealed three morphologically cryptic and highly divergent mitochondrial DNA lineages (named the Northern, Central, and Southern lineages based on geography) with only the Northern lineage exhibiting concordant divergence for nuclear genes. Here, we showed that these mtDNA lineages likely formed in allopatry during the Pleistocene, but responded differentially to climatic changes that occurred since the last interglacial (~120,000 years ago). We find that the Northern lineage maintained a stable range throughout this period, correlating with genetic distinctiveness among all genetic markers and low migration rates with the other lineages. In contrast, our results suggested that the Southern lineage expanded from Baja California Sur during the Late Pleistocene to overlap and potentially swamp a contracting Central lineage. High rates of intraspecific gene flow between Southern lineage individuals among expansion origin and expansion edge populations largely eroded Central ancestry from autosomal markers. However, male-biased dispersal in this system preserved signals of this past hybridization and introgression event in matrilineal-biased X-chromosome and mtDNA markers. Our results highlight the importance of range stability in maintaining the persistence of phylogeographic lineages, whereas unstable range dynamics can increase the tendency for lineages to merge upon secondary contact.

Are glacial refugia hotspots of speciation and cytonuclear discordances? Answers from the genomic phylogeography of Spanish common frogs

“…The origin of this ghost T6 mtDNA lineage is puzzling. Contrarily to Phuong et al (), here we did not find significant associations between patterns of cytonuclear discordances or genetic diversity and the variability of environmental conditions during the late‐Pleistocene, perhaps because the ranges remained broadly suitable for this species during the last glaciation (Figure and File ). Hence, we rather envisage two alternative scenarios: (a) mitochondrial capture from a now extinct nuclear T6 cluster; or (b) de novo emergence of the T6 mtDNA by drift and/or selection.…”

“…A major issue with over-reliance on mtDNA is the prevalence of cytonuclear discordances across taxa (Bonnet, Leblois, Rousset, & Crochet, 2017;Toews & Brelsford, 2012), which can lead to false evolutionary and taxonomic conclusions ("mirage of cryptic species", Hinojosa et al, 2019). Cytonuclear discordances may have selective causes (local adaptation of mtDNA genes, Pavlova et al, 2013;asymmetric hybridization, Chan & Levin, 2005), but they often result from neutral demographic processes, e.g., faster rate of molecular evolution and lower effective sizes of mitochondrial DNA (Rosenberg, 2003), sex-biased dispersal (e.g., Dai, Wang, & Lei, 2013), or mitochondrial introgression or fusion following secondary contacts (e.g., Garrick et al, 2019;Phuong, Bi, & Moritz, 2017). Theoretical (Currat, Ruedi, Petit, & Excoffier, 2008;Excoffier, Foll, & Petit, 2009) and empirical data (Cahill et al, 2013;Phuong et al, 2017) have shown that demographic expansions at range margins can promote asymmetric gene flow in the initial stages of the contact (from the local to the expanding taxa), traces of which are expected to persist longer in the mitochondrial than in the nuclear genome.…”

“…Cytonuclear discordances may have selective causes (local adaptation of mtDNA genes, Pavlova et al, 2013;asymmetric hybridization, Chan & Levin, 2005), but they often result from neutral demographic processes, e.g., faster rate of molecular evolution and lower effective sizes of mitochondrial DNA (Rosenberg, 2003), sex-biased dispersal (e.g., Dai, Wang, & Lei, 2013), or mitochondrial introgression or fusion following secondary contacts (e.g., Garrick et al, 2019;Phuong, Bi, & Moritz, 2017). Theoretical (Currat, Ruedi, Petit, & Excoffier, 2008;Excoffier, Foll, & Petit, 2009) and empirical data (Cahill et al, 2013;Phuong et al, 2017) have shown that demographic expansions at range margins can promote asymmetric gene flow in the initial stages of the contact (from the local to the expanding taxa), traces of which are expected to persist longer in the mitochondrial than in the nuclear genome. Consequently, it has been proposed that cytonuclear discordances may preferentially occur in regions subjected to climate instability (Phuong et al, 2017), where frequent range shifts offered recurrent opportunities for lineages to expand and admix.…”

“…Theoretical (Currat, Ruedi, Petit, & Excoffier, 2008;Excoffier, Foll, & Petit, 2009) and empirical data (Cahill et al, 2013;Phuong et al, 2017) have shown that demographic expansions at range margins can promote asymmetric gene flow in the initial stages of the contact (from the local to the expanding taxa), traces of which are expected to persist longer in the mitochondrial than in the nuclear genome. Consequently, it has been proposed that cytonuclear discordances may preferentially occur in regions subjected to climate instability (Phuong et al, 2017), where frequent range shifts offered recurrent opportunities for lineages to expand and admix.…”

Genotyping‐by‐sequencing and ecological niche modeling illuminate phylogeography, admixture, and Pleistocene range dynamics in quaking aspen (Populus tremuloides)

“…On the one hand, spatially explicit predictions of Pleistocene suitable areas for P. tremuloides and its intraspecific clusters from ENM hindcasting gave compelling indirect evidence for fully or partly stable niche suitability for clusters 1 and 2 to the southwest over LGM‐present (Figures 6 and Figure ). Greater range stability should increase the probability of phylogeographic lineage persistence, whereas genetic lineages are more likely to collapse following secondary contact or environmental stochasticity due to range instability (e.g., Phuong, Bi, & Moritz, 2017; Singhal & Moritz, 2013). Thus, the observation that a greater number of phylogeographic lineages (2 clusters; Figure 2) occurred over LGM to present in southwestern portions of the species range also supports stable‐edge dynamics.…”