Evidence for Admixture and Rapid Evolution During Glacial Climate Change in an Alpine Specialist

Abstract

The pace of current climate change is expected to be problematic for alpine flora and fauna, as their adaptive capacity may be limited by small population size. Yet, despite substantial genetic drift following post-glacial recolonization of alpine habitats, alpine species are notable for their success surviving in highly heterogeneous environments. Population genomic analyses demonstrating how alpine species have adapted to novel environments with limited genetic diversity remain rare, yet are important in understanding the potential for species to respond to contemporary climate change. In this study, we explored the evolutionary history of alpine ground beetles in the Nebria ingens complex, including the demographic and adaptive changes that followed the last glacier retreat. We first tested alternative models of evolutionary divergence in the species complex. Using millions of genome-wide SNP markers from hundreds of beetles, we found evidence that the N. ingens complex has been formed by past admixture of lineages responding to glacial cycles. Recolonization of alpine sites involved a distributional range shift to higher elevation, which was accompanied by a reduction in suitable habitat and the emergence of complex spatial genetic structure. We tested several possible genetic pathways involved in adaptation to heterogeneous local environments using genome scan and genotype-environment association approaches. From the identified genes, we found enriched functions associated with abiotic stress responses, with strong evidence for adaptation to hypoxia-related pathways. The results demonstrate that despite rapid demographic change, alpine beetles in the N. ingens complex underwent rapid physiological evolution.

Keywords: adaptation; climate change; demography; population genomics; spatially explicit; speciation.

Fig. 1.

The two competing demographic models (isolation and admixture models). τ₁ denotes the divergence time of the three lineages, τ₂ represents the time of admixture thus only applies to admixture model, and m_c-s is the gene contribution of intermediate lineage (Selden) from N. riversi (Conness). The model comparison using approximate Bayesian computation shows the intermediate lineage (Selden) in the N. ingens complex formed as a consequence of nearly equal admixture between N. ingens (Army) and N. riversi (Conness). The population tree on the top with the 3D map of the Sierra Nevada in California was adapted from Weng et al. 2021a; the 3D map was drawn using the R package rasterVis v 0.51.5 (Lamigueiro et al. 2023) with the digital elevation model from the WorldClim database (Fick and Hijmans 2017).