Allele surfing causes maladaptation in a Pacific salmon of conservation concern

Abstract

The Anthropocene threatens worldwide biodiversity, with a potential to induce species decline and range contraction. In this context, it is important to quantify species adaptive potential and how demographic changes may impact selection efficacy and the burden of deleterious mutations in different populations. Here we show that key evolutionary processes, including variation in effective population size through postglacial change in demography and recombination rates have affected the efficacy of selection and impacted the load in Coho salmon (Oncorhynchus kisutch), a widely distributed salmonid species on the west coast of North America. Using whole genome resequencing (30x coverage) data from populations at different latitudinal distances from their southern glacial refugium, we found support for postglacial gene surfing, with reduced Ne at the range recolonization front, thus inducing both a reduction of the adaptive potential and a surf of deleterious alleles in populations evolving at low Ne. This inference was robust to various proxy of the load, namely ratios of non-synonymous to synonymous diversity, the number of missense and loss of function mutations. In addition, comparing residual tetrasomic and re-diploidizing regions of the salmon genome, we found support for a prime role of recombination rates in shaping the within-genome variation of the load. Overall, our empirical results are remarkably consistent with expectations under the nearly neutral theory of molecular evolution. We discuss the fundamental and applied implications of these findings for evolutionary and conservation genomics.

Too big to purge: persistence of deleterious mutations in island populations of the European barn owl (Tyto alba)

“…This pattern was, however, not observed for all types of deleterious mutations, which suggests that selection has been as efficient at removing deleterious alleles for all these categories. Overall, the depletion of minor alleles in recolonized populations goes against what has been reported in the literature (Peischl et al, 2013;Henn et al, 2016;Rougemont et al, 2023). However, this could be explained because the continental populations were recolonized long ago and are not at the extremities of range expansion anymore.…”

“…Like most recolonization events in other species, the recolonization of Europe by the barn owl probably occurred with bottlenecks at the front of the colonization side, followed by population expansion (Ursenbacher et al, 2015;McDevitt et al, 2022). This scenario has been shown to lead to an increased number in deleterious mutations per individual and a reduction in selection efficiency due to the smaller effective population size both with simulated data (Peischl et al, 2013) and with empirical data such as out-of-Africa human expansion (Henn et al, 2016;McCoy and Akey, 2016) and salmons postglacial recolonization (Rougemont et al, 2023).…”

The genetic consequences of range expansion and its influence on diploidization in polyploids

“…More specifically, outside of an unlikely model of additive dominance, the masking advantage provided by whole genome duplication when mutations are partially or fully recessive results in an accumulation of deleterious mutations that in turn leads to a protracted drop in the fitness of polyploids with tetrasomic inheritance during expansion relative to their diploid counterparts. Indeed, recent evidence in Coho salmon ( Oncorhynchus kisutch ) showed residual tetraploid regions of their genome that had not yet re-diploidized harbored a greater mutational load than the diploidized regions (Rougemont et al 2023)…”

“…More specifically, outside of an unlikely model of additive dominance, the masking advantage provided by whole genome duplication when mutations are partially or fully recessive results in an accumulation of deleterious mutations that in turn leads to a protracted drop in the fitness of polyploids with tetrasomic inheritance during expansion relative to their diploid counterparts. Indeed, recent evidence in Coho salmon (Oncorhynchus kisutch) showed residual tetraploid regions of their genome that had not yet re-diploidized harbored a greater mutational load than the diploidized regions (Rougemont et al 2023) Abundant evidence has demonstrated a link between polyploidy and previously glaciated areas (Brochmann et al 2004;Paun et al 2006;Novikova et al 2018;Sutherland and Galloway 2018;Rice et al 2019;David 2022;Booker et al 2023). While support for this observation has many adaptive explanations-such as fixed heterozygosity (Stebbins 1985;Brochmann et al 2004), increased adaptability of gene regulatory networks (Freeling and Thomas 2006;Hegarty and Hiscock 2007;Fusco et al 2010;Yao et al 2019;Ebadi et al 2023), or the relaxed constraint on gene duplicates enabling more rapid adaptation (Lynch and Conery 2000;Lynch and Force 2000;Gout and Lynch 2015)-these arguments too rely on some level of subgenomic differentiation, and therefore disomy, to maintain their validity.…”

Revealing the evolutionary history and contemporary population structure of Pacific salmon in the Fraser River through genome resequencing

“…Understanding why we observe these genetic groups is important (e.g., (Nadeau et al 2016;Rougemont et al 2023)). Are they a technical artifact from trying to cluster genomes influenced by isolation-by-distance?…”