Allele surfing causes maladaptation in a Pacific salmon of conservation concern

Abstract

How various factors, including demography, recombination or genome duplication, may impact the efficacy of natural selection and the burden of deleterious mutations,is a central question in evolutionary biology and genetics. In this study, we show that key evolutionary processes, including variations in i) effective population size (Ne) ii) recombination rates and iii) chromosome inheritance, have influenced the genetic load and efficacy of selection in Coho salmon (Oncorhynchus kisutch), a widely distributed salmonid species on the west coast of North America. Using whole genome resequencing data from 14 populations at different migratory distances from their southern glacial refugium, we found evidence supporting gene surfing, wherein reduced Ne at the postglacial recolonization front, leads to a decrease in the efficacy of selection and a surf of deleterious alleles in the northernmost populations. Furthermore, our results indicate that recombination rates play a prime role in shaping the load along the genome. Additionally, we identified variation in polyploidy as a contributing factor to within-genome variation of the load. Overall, our results align remarkably well 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.

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?…”

“…Previous researchers have suggested that isolation-by-distance is an important factor influencing salmon genetics (Withler et al 2000;Rougemont et al 2020Rougemont et al , 2023. Others have suggested that different re-colonization events (e.g., from different glacial refugia) influence population structure in Fraser River salmon (Wood et al 1994;Small et al 1998;Teel et al 2000;Withler et al 2000).…”

Future climate warming threatens coral reef function on World Heritage reefs

“…The nearly neutral theory of evolution (Ohta, 1973) can provide clues for assessing the potential for selection of traits, like temperature tolerance at the range margins. For example, evidence in salmon suggests that selection is weaker at the range margins due to "surfing" of deleterious mutations, selection efficiency is lower (via greater number of nonadaptive substitutions and lower adaptive substitutions), and effective populations sizes are smaller (Rougemont et al, 2023). Multiple founder events-hallmarks of range margins-also have a similar effect (Rougemont et al, 2023).…”