The impact of environmental fluctuations, sexual dimorphism, dominance reversal and plasticity on the pigmentation-related genetic and phenotypic variation in D. melanogaster populations - A modelling study
Résumé
In this article, we consider a phenotypic trait which is variable only in females and depends both on the individual's allelic state at a given locus and on environmental conditions at birth. Whatever their genotype and environment, males express the same phenotype. The key example of such traits that we study here is the pigmentation of the posterior abdomen in Drosophila melanogaster, which, in females, is influenced by the genotype of the individual and by the environmental temperature during development (and is approximately constant in males). In the absence of sexual dimorphism and with selection acting on a trait, it has been shown that periodically fluctuating environments can maintain genetic variation at the underlying locus. Here, we introduce a more complex model integrating several important features that can also influence the genetic and phenotypic composition of the population, in order to partially disentangle their effects on the maintenance of variation at the genetic and phenotypic levels. In this model, selection acts on the trait, the population is sexually dimorphic, individuals are diploid, the trait considered is plastic and dominance reversal renders the contribution of the genotype to the phenotype dependent on the environment (i.e., an individual heterozygous at the locus of interest tends to have a trait value which is favourable in the environment in which it was born). Because drosophila populations experience massive seasonal fluctuations in size due to variations in resource availability and environmental conditions, we model a spatially structured population with a local regulation of population sizes and whose demography exhibits boom and bust dynamics.
Using simulations of a rather caricatural model of thermal adaptation based on abdominal pigmentation in D. melogaster that constitute our case study, we find that, in periodically fluctuating environments, the combination of plasticity, dominance reversal and sexual dimorphism leads to oscillations of the mean female phenotype but not of allele frequencies, which tend to stabilise around some random value away from 0 and 1 (that is, genetic variability within the population is conserved). Plasticity and dominance reversal allow gradual but fast phenotypic adaptation in the female population, which is all the more efficient as the period of environment oscillations is long. However, the absence of sexual dimorphism leads to higher extinction probabilities, as not enough individuals exhibit the best adapted phenotype during the periods when surviving tough environmental conditions is crucial. Conversely, sexual dimorphism without plasticity and dominance reversal leads to phenotypic variability but no oscillations of the female population mean phenotype. The male population thus serves as a reserve of individuals with optimal phenotypes to survive harsh conditions and restart the population when better times are coming; because male phenotypes are independent of their genotypes, this reserve also shelters alleles associated with less adapted phenotypes, thereby helping to maintain genetic variability in the whole population.
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