A clinal polymorphism in the insulin signaling transcription factorfoxocontributes to life-history adaptation inDrosophila

Abstract

A fundamental aim of adaptation genomics is to identify polymorphisms that underpin variation in fitness traits. In Drosophila melanogaster, latitudinal life-history clines exist on multiple continents and make an excellent system for dissecting the genetics of adaptation. We have previously identified numerous clinal single-nucleotide polymorphism in insulin/insulin-like growth factor signaling (IIS), a pathway known from mutant studies to affect life history. However, the effects of natural variants in this pathway remain poorly understood. Here we investigate how two clinal alternative alleles at foxo, a transcriptional effector of IIS, affect fitness components (viability, size, starvation resistance, fat content). We assessed this polymorphism from the North American cline by reconstituting outbred populations, fixed for either the low-or high-latitude allele, from inbred DGRP lines. Because diet and temperature modulate IIS, we phenotyped alleles across two temperatures (18°C, 25°C) and two diets differing in sugar source and content. Consistent with clinal expectations, the high-latitude allele conferred larger body size and reduced wing loading. Alleles also differed in starvation resistance and expression of insulin-like receptor, a transcriptional target of FOXO. Allelic reaction norms were mostly parallel, with few GxE interactions. Together, our results suggest that variation in IIS makes a major contribution to clinal life-history adaptation. K E Y W O R D S : Adaptation, cline, insulin signaling, life history, plasticity, pleiotropy.

Digest: A clinal polymorphism and life‐history adaptations in Drosophila *

“…Consistent with predictions, the low latitude flies showed a 12% greater quantity of InR transcript than the high latitude flies. Durmaz et al (2019) conclude that these clinal foxo variants have pleiotropic effects on fitness-related traits that are consistent with trade-offs and contribute to observed life history clines of North American D. melanogaster. Together with similar results on a polymorphism in InR (Paaby et al 2010(Paaby et al , 2014, the results of Durmaz et al (2019) suggest that natural variation in IIS makes an important contribution to clinal adaptation in Drosophila.…”

“…Studying such natural polymorphisms allow evolutionary geneticists to address key questions such as: "Which genetic mechanisms underlie variation in fitness-related traits?," "What are the * This article corresponds to Durmaz, E., S. Rajpurohit phenotypic effects of natural life-history variants?," and "Do evolutionary changes in life-history traits occur independently, or via the same pathways and genes?" Durmaz et al (2019) identified a natural variant of the foxo gene in D. melanogaster that exhibits a strong allele frequency cline along the North American east coast. This variant consists of two alternative alleles, one of which is common at low latitude (Florida) and the other at high latitude (Maine), with the alleles differing at two nucleotide positions.…”

Distinct genomic signals of lifespan and life history evolution in response to postponed reproduction and larval diet inDrosophila

“…Similar to ours, these studies found only weak support for an involvement of loci in the IIS/TOR or other major longevity pathways in the evolution of longevity (Table S5). This is an interesting observation given that functional variation in canonical "aging" genes in natural populations has been observed to contribute to life history adaptation along latitudinal clines, for example the Drosophila Insulin receptor (InR) (Paaby et al 2010;Paaby et al 2014), transcription factor foxo (Durmaz et al 2019), and methusaleh (Paaby and Schmidt 2008). However, the selection pressures to which these alleles respond in clinal populations may be different from selection for postponed reproduction or adaptation to larval diet such as in our experiment.…”

Allelic polymorphism at foxo contributes to local adaptation in Drosophila melanogaster

“…These sites were observed to be in perfect linkage disequilibrium ( r 2 =1) in the DGRP, such that they covary and are not independent. Further details regarding these polymorphic sites and the landscape of linkage disequilibrium at foxo are provided in our previous publication (Durmaz et al, 2019).…”