A highly pleiotropic amino acid polymorphism in theDrosophilainsulin receptor contributes to life-history adaptation

Abstract

Finding the specific nucleotides that underlie adaptive variation is a major goal in evolutionary biology, but polygenic traits pose a challenge because the complex genotype–phenotype relationship can obscure the effects of individual alleles. However, natural selection working in large wild populations can shift allele frequencies and indicate functional regions of the genome. Previously, we showed that the two most common alleles of a complex amino acid insertion–deletion polymorphism in the Drosophila insulin receptor show independent, parallel clines in frequency across the North American and Australian continents. Here, we report that the cline is stable over at least a five-year period and that the polymorphism also demonstrates temporal shifts in allele frequency concurrent with seasonal change. We tested the alleles for effects on levels of insulin signaling, fecundity, development time, body size, stress tolerance, and life span. We find that the alleles are associated with predictable differences in these traits, consistent with patterns of Drosophila life-history variation across geography that likely reflect adaptation to the heterogeneous climatic environment. These results implicate insulin signaling as a major mediator of life-history adaptation in Drosophila, and suggest that life-history trade-offs can be explained by extensive pleiotropy at a single locus.

An inversion supergene in Drosophila underpins latitudinal clines in survival traits

“…Paaby & Schmidt, ): genotypes that confer stress resistance and survival at the expense of reduced fecundity might be favoured at high latitudes, where seasonal stressors such as cold and food shortage impose strong selection on somatic maintenance, whereas at low latitude, selection might favour alternative genotypes that confer fast development and high fecundity at the expense of reduced stress resistance and survival. In support of this adaptive scenario, we observed that high‐latitude flies from Maine lived longer and were more resistant to starvation and cold stress than low‐latitude flies from Florida, consistent with previous observations along the North American cline (Schmidt et al., , , b; Schmidt & Paaby, ; Paaby et al., ; Mathur & Schmidt, ).…”

“…This suggests a pattern of climatic adaptation whereby harsh winters and seasonal stress at high latitudes favour stress resistance and overwintering ability (dormancy), along with correlated (e.g. pleiotropic) responses in terms of larger body size, increased lifespan and reduced fecundity (Schmidt & Paaby, ; Paaby & Schmidt, ; Flatt et al., ; Paaby et al., ). Yet, whether clinal inversion polymorphisms such as In(3R)P contribute to this pattern of phenotypic climatic adaptation is largely unclear (De Jong & Bochdanovits, ; Hoffmann et al., ; Rako et al., ; Hoffmann & Weeks, ; Hoffmann & Rieseberg, ; Kapun et al., , b).…”

“…Schmidt et al., , , b; Schmidt & Paaby, ; Paaby et al., ; Mathur & Schmidt, ). In agreement with previous phenotypic results, we find that high‐latitude flies from Maine lived longer and are more stress resistant than low‐latitude flies from Florida, consistent with the idea that selection at high latitude favours genotypes and phenotypes that confer improved survival and somatic maintenance (Paaby & Schmidt, ; Flatt et al., ; Paaby et al., ). Interestingly, we observe that the clines in these traits are partly driven by the clinal frequency gradient in In(3R)P : on average flies carrying the In(3R)P inversion from Florida live shorter and are less stress resistant than flies from Florida or Maine which possess the uninverted chromosomal segment.…”

Broad geographic sampling reveals predictable, pervasive, and strong seasonal adaptation inDrosophila

“…If we treat cpo as the true seasonal locus, this result implies that we lack power to discover many many causal genes involved in seasonal adaptation. There was no excess of seasonal SNPs surrounding the insulin receptor (InR), wherein seasonally variable indels and SNPs had been previously reported (Paaby et al 2014).…”

How to get the most bang for your buck: the evolution and physiology of nutrition-dependent resource allocation strategies

“…Studies in flies and beetles have likewise suggested the IIS as a major pathway involved in resource distribution. An exonic indel polymorphism in the insulin-like receptor (lnR) gene was identified as a functional direct candidate target of natural selection in wild D. melanogaster [72,73]. In rhinoceros beetles, horn size is highly sensitive to nutrition and to perturbations in the IIS than are other body structures [74].…”