Genetic basis of thermal plasticity variation inDrosophila melanogasterbody size

Abstract

12Body size is a quantitative trait that is closely associated to fitness and under the 13 control of both genetic and environmental factors. While developmental plasticity for 14 this and other traits is heritable and under selection, little is known about the genetic 15 basis for variation in plasticity that can provide the raw material for its evolution. We 16 quantified genetic variation for body size plasticity in Drosophila melanogaster by 17 measuring thorax and abdomen length of females reared at two temperatures from a 18 panel representing naturally segregating alleles, the Drosophila Genetic Reference 19 Panel (DGRP). We found variation between genotypes for the levels and direction of 20 thermal plasticity in size of both body parts. We then used a Genome-Wide Association 21 Study (GWAS) approach to unravel the genetic basis of inter-genotype variation in 22 body size plasticity, and used different approaches to validate selected QTLs and to 23 explore potential pleiotropic effects. We found mostly "private QTLs", with little overlap 24 between the candidate loci underlying variation in plasticity for thorax versus abdomen 25 size, for different properties of the plastic response, and for size versus size plasticity. 26We also found that the putative functions of plasticity QTLs were diverse and that 27 alleles for higher plasticity were found at lower frequencies in the target population. 28Importantly, a number of our plasticity QTLs have been targets of selection in other 29 populations. Our data sheds light onto the genetic basis of inter-genotype variation in 30 size plasticity that is necessary for its evolution. 31 Significance Statement 32The environmental conditions under which development takes place can affect 33 developmental outcomes and lead to the production of phenotypes adjusted to the 34 environment adults will live in. This developmental plasticity, which can help organisms 35 cope with environmental heterogeneity, is heritable and under selection. Plasticity can 36 itself evolve, a process that will be partly dependent on the available genetic variation 37 for this trait. Using a wild-derived D. melanogaster panel, we identified DNA sequence 38 variants associated to variation in thermal plasticity for body size. We found that these 39 variants correspond to a diverse set of gene functions. Furthermore, their effects differ 40 between body parts and properties of the thermal response, which can, therefore, 41 evolve independently. Our results shed new light onto a number of key questions about 42 the long discussed genes for plasticity.43 44 45 size, body proportions natural variation for many adaptive traits in D. melanogaster and other species (6, 43-mapping panels (46, 47) allowed the dissection of the genetic architecture of various 83 quantitative traits in D. melanogaster (48-50), including body size (51). However, with 84 a few recent exceptions (52-55), the genetic basis of phenotypic variation has been 85 investigated under a single environmental condition, precluding asse...

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

“…[] and Lafuente et al. [] for examples using this method). For each allele, we used two independent sets of DGRP lines (sets A and B for HL; sets C and D for LL; each set consisting of 20 distinct lines) and two replicate population cages per set, giving a total of eight population cages (Fig.…”

Sex and tissue‐specific evolution of developmental plasticity in Drosophila melanogaster

“…Our dataset includes 20 wild lines from two distinct populations. Developmental plasticity is genetically regulated (Debat et al., 2009; Lafuente et al., 2018; Stanley et al., 2017), and the differences in nutritional plasticity observed in our study may be due to the genetic variants found in the ME and PC populations compared to the three strains that were analyzed previously.…”

“…Next, we tested whether wing and femur size had different plasticity responses to temperature and nutrition by comparing the percent change in size and the slope of the reaction norm, which is commonly used for studying within species plasticity response to limited number of environmental parameters (Gianoli & González‐Teuber, 2005; Gutteling et al., 2007; Lafuente et al., 2018; Ungerer et al., 2003).…”

“…We calculated norms of reaction for both wing and femur lengths for each of the sex, temperature, and nutrition variables, holding constant the other two nonfocal variables. Following previous work on plasticity (Gianoli & González‐Teuber, 2005; Gutteling et al., 2007; Lafuente et al., 2018; Ungerer et al., 2003), we calculated the slope of the reaction norm using a linear model in R of the form Model = log (Measurement) ~ Variable, where variable is sex, temperature, or nutrition and measurement is either wing length or femur length for each genotype. The slope estimates the amount of phenotypic difference observed for each genotype under two different treatments, for example, low versus high temperature, while keeping the other variables constant, in this example, sex and nutritional status.…”

“…Developmental plasticity allows for the same genotype to give rise to different phenotypes when juveniles are exposed to varying environmental conditions (Bradshaw, 1965; Stearns, 1989). Plasticity is genetically regulated (Lafuente et al., 2018; Scheiner et al., 1991; Scheiner & Lyman, 1989; Stanley et al., 2017), and theoretical and empirical studies have shown that natural selection may favor genetic variants that increase plasticity in organisms adapting to heterogeneous environments across generations (Gilchrist, 1995; Price et al, 2003).…”