From genotype to phenotype: Genetic redundancy and the maintenance of an adaptive polymorphism in the context of high gene flow

TY - JOUR

T1 - From genotype to phenotype

T2 - Genetic redundancy and the maintenance of an adaptive polymorphism in the context of high gene flow

AU - Bataillon, Thomas

AU - Gauthier, Perrine

AU - Villesen, Palle

AU - Santoni, Sylvain

AU - Thompson, John D.

AU - Ehlers, Bodil K.

PY - 2022/4

Y1 - 2022/4

N2 - A central question in evolution is how several adaptive phenotypes are maintained within a species. Theory predicts that the genetic determination of a trait, and in particular the amounts of redundancy in the mapping of genotypes to phenotypes, mediates evolutionary outcomes of phenotypic selection. In Mediterranean wild thyme, numerous discrete chemical phenotypes (chemotypes) occur in close geographic proximity. Chemotypes are defined by the predominant monoterpene produced by individual plants in their essential oil. In this study, we analyze the ecological genetics of six chemotypes nested within two well-established chemical families (hereafter ecotypes). Ecotypes, and chemotypes within ecotypes, are spatially segregated, and their distributions track local differences in the abiotic environment. By combining population genomic, phenotypic, and environmental data from 700 individuals, we show how the genetics of ecotype determination mediates this evolutionary response. Variation in three terpene-synthase loci explains variation in ecotype identity, with one single locus accounting for as much as 78% of this variation. Phenotypic selection combined with low segregating genotypic redundancy of ecotypes leaves a clear footprint at the genomic level: alleles associated with ecotype identity track environmental variation despite extensive gene flow. Different chemotypes within each ecotype differentially track environmental variation. Their identity is determined by multiple loci and displays a wider range of genotypic redundancy that dilutes phenotypic selection on their characteristic alleles. Our study thus provides a novel illustration of how genetic redundancy of a phenotype modulates the ability of selection to maintain adaptive differentiation. Identifying the precise genetics of the chemical polymorphism in thyme is the next crucial step for our understanding of the origin and maintenance of a polymorphism that is present in many aromatic plants.

AB - A central question in evolution is how several adaptive phenotypes are maintained within a species. Theory predicts that the genetic determination of a trait, and in particular the amounts of redundancy in the mapping of genotypes to phenotypes, mediates evolutionary outcomes of phenotypic selection. In Mediterranean wild thyme, numerous discrete chemical phenotypes (chemotypes) occur in close geographic proximity. Chemotypes are defined by the predominant monoterpene produced by individual plants in their essential oil. In this study, we analyze the ecological genetics of six chemotypes nested within two well-established chemical families (hereafter ecotypes). Ecotypes, and chemotypes within ecotypes, are spatially segregated, and their distributions track local differences in the abiotic environment. By combining population genomic, phenotypic, and environmental data from 700 individuals, we show how the genetics of ecotype determination mediates this evolutionary response. Variation in three terpene-synthase loci explains variation in ecotype identity, with one single locus accounting for as much as 78% of this variation. Phenotypic selection combined with low segregating genotypic redundancy of ecotypes leaves a clear footprint at the genomic level: alleles associated with ecotype identity track environmental variation despite extensive gene flow. Different chemotypes within each ecotype differentially track environmental variation. Their identity is determined by multiple loci and displays a wider range of genotypic redundancy that dilutes phenotypic selection on their characteristic alleles. Our study thus provides a novel illustration of how genetic redundancy of a phenotype modulates the ability of selection to maintain adaptive differentiation. Identifying the precise genetics of the chemical polymorphism in thyme is the next crucial step for our understanding of the origin and maintenance of a polymorphism that is present in many aromatic plants.

KW - Ecologically important trait

KW - local adaptation

KW - population genomics

UR - http://www.scopus.com/inward/record.url?scp=85125097692&partnerID=8YFLogxK

U2 - 10.1002/evl3.277

DO - 10.1002/evl3.277

M3 - Letter

C2 - 35386834

AN - SCOPUS:85125097692

SN - 2056-3744

VL - 6

SP - 189

EP - 202

JO - Evolution Letters

JF - Evolution Letters

IS - 2

ER -