The Genetic Consequences of Spatially Varying Selection in the Panmictic American Eel (Anguilla rostrata)

Abstract

Our understanding of the genetic basis of local adaptation has recently benefited from the increased power to identify functional variants associated with environmental variables at the genome scale. However, it often remains challenging to determine whether locally adaptive alleles are actively maintained at intermediate frequencies by spatially varying selection. Here, we evaluate the extent to which this particular type of balancing selection explains the retention of adaptive genetic variation in the extreme situation of perfect panmixia, using the American eel (Anguilla rostrata) as a model. We first conducted a genome scan between two samples from opposite ends of a latitudinal environmental gradient using 454 sequencing of individually tagged cDNA libraries. Candidate SNPs were then genotyped in 992 individuals from 16 sampling sites at different life stages of the same cohort (including larvae from the Sargasso Sea, glass eels, and 1-year-old individuals) as well as in glass eels of the following cohort. Evidence for spatially varying selection was found at 13 loci showing correlations between allele frequencies and environmental variables across the entire species range. Simulations under a multiple-niche Levene's model using estimated relative fitness values among genotypes rarely predicted a stable polymorphic equilibrium at these loci. Our results suggest that some genetic-by-environment interactions detected in our study arise during the progress toward fixation of a globally advantageous allele with spatially variable effects on fitness.

Mechanisms of Thermal Tolerance in Reef-Building Corals across a Fine-Grained Environmental Mosaic: Lessons from Ofu, American Samoa

“…Simulation studies show that even alleles that are not maintained at intermediate frequencies by balancing selection can contribute to local adaptation; under some circumstances this could lead to persistence of locally adapted populations with a shifting set of genomic variants underlying adaptive differentiation between populations (Yeaman, 2015). The existence of significant F ST outliers which do not appear to be at stable equilibrium among eel populations that show a Levenetype system may provide evidence for the importance of nonequilibrium processes in local adaptation involving polygenic traits (Gagnaire et al, 2012).…”

Population Genomics of Marine Fishes: Next-Generation Prospects and Challenges

“…Gagnaire et al (2012) scanned for signatures of single-generation selection in American eel (A. rostrata) using a panel of 100 SNPs. They found evidence for spatially varying selection at 13 loci showing correlations between allele frequencies and environmental variables across the entire species range.…”

The influence of genotype on habitat selection of fish and the analysis of population structure

“…Similarly, a weak genetic differentiation between samples of eels collected in different rivers was observed in AFLP and SNP analyses (Gagnaire et al, 2009(Gagnaire et al, , 2012. However, the authors of these articles note that the differentiation was probably caused by selection at loci linked to some of the sequences studied.…”