Do putatively deleterious alleles increase in frequency along the edge of a range expansion?

Background/Question/Methods

Range expansions have become increasingly common due to anthropogenic changes, including the introduction of novel species to new geographic areas and the shifting of species’ ranges due to climate change. The ecological consequences of range expansions have long been studied, but the extent of the evolutionary consequences of range expansions has only begun to be appreciated recently. For example, recent work has shown the evolution of increased dispersal in expansions of both microcosm and field populations. Critically, studies have also shown an increased role for genetic drift in expanding populations due to small effective population sizes and repeated founder events characteristic of an expanding range edge. Theoretical models have shown that this increased role for genetic drift can lead to the accumulation of deleterious alleles in individuals at an expansion edge, however these predictions have yet to be empirically validated. Here, we leverage whole-genome sequencing data from a previous range expansion experiment to evaluate whether expanding populations do, in fact, accumulate deleterious alleles that correlate with reductions in fitness. This experiment had replicate red flour beetle (Tribolium castaneum) populations expand for 8 generations through a benign, homogenous environment ensuring genetic changes were due to spatial dynamics.

Results/Conclusions

We performed pooled DNA extractions from three populations in each replicate: (1) the founding population, (2) the edge population from the last generation of expansion, and (3) the core population from the last generation of expansion. Using these population groups, we quantified changes in allele frequencies across the genome over 8 generations of range expansion. We further compared the patterns of those changes in edge vs. core populations to quantify the impact of spatial evolution. Finally, we used Genomic Evolutionary Rate Profiling (GERP) to identify putatively deleterious alleles by finding highly conserved portions of the genome across evolutionary history. Our results show that allele frequency changes were much higher at the edge (P < 0.005) and were associated with a reduction in fitness (R2 = 0.2, P < 0.005). We also showed that alleles at loci with high GERP scores (i.e., highly conserved regions) had a 15% higher change in frequency in edge populations compared to the core (P < .05). These findings support the theoretical predictions that edge populations could accumulate deleterious alleles and suggest that increased genetic drift at the edge of expanding populations can have important consequences for the outcomes of range expansions.