Genetic Decoupling of Thermal Hardiness across Metamorphosis in Drosophila melanogaster

Abstract

As organisms age the environment fluctuates, exerting differential selection across ontogeny. In particular, highly seasonal environments expose life stages to often drastically different thermal environments. This developmental variation is particularly striking in organisms with complex life cycles, wherein life history stages also exhibit distinct morphologies, physiologies, and behaviors. Genes acting pleiotropically on thermal responses may produce genetic correlations across ontogeny, constraining the independent evolution of each life stage to their respective thermal environments. To investigate whether developmental genetic correlations constrain the evolution thermal hardiness of the fly Drosophila melanogaster, we applied quantitative genetic analyses to cold hardiness measured in both larvae and adults from isogenic lines of the Drosophila Genetic Reference Panel (DGRP), using survival at stressful low temperatures as the phenotypic metric. Using full genome resequencing data for the DGRP, we also implemented genome-wide association (GWA) analysis using Bayesian Sparse Linear Mixed Models (BSLMMs) to estimate associations between naturally segregating variation and cold hardiness for both larvae and adults. Quantitative genetic analyses revealed no significant genetic correlation for cold hardiness between life stages, suggesting complete genetic decoupling of thermal hardiness across the metamorphic boundary. Both quantitative genetic and GWA analyses suggested that polygenic variation underlies cold hardiness in both stages, and that associated loci largely affected one stage or the other, but not both. However, reciprocal enrichment tests and correlations between BSLMM parameters for each life stage support some shared physiological mechanisms that may reflect common cellular thermal response pathways. Overall, these results suggest no developmental genetic constraints on cold hardiness across metamorphosis in D. melanogaster, an important consideration in evolutionary models of responses to changing climates. Genetic correlations for environmental sensitivity across ontogeny remains largely unexplored in other organisms, thus assessing the generality of genetic decoupling will require further quantitative or population genetic analysis in additional species.

Do traits separated by metamorphosis evolve independently? Concepts and methods

“…Selection on larval and adult ability to resist extreme temperatures showed these traits are independent in Drosophila buzzatii flies [30] and in the butterfly Bicyclus anynana [31]. Phenomenological independence between temperature-stress resistance in insect larvae and adults is congruent with the recent discovery that, at the genome level, different combinations of genes affect cold hardiness in larvae and in adults in Drosophila melanogaster [32]. Even functionally related traits measured in the same organism can exhibit very different levels of genetic correlation.…”

Distinct cold tolerance traits independently vary across genotypes inDrosophila melanogaster

“…2016; Freda et al. 2017; Teets and Hahn 2018). Here we measured correlations between several cold tolerance traits and found them to be sparse and sex‐specific.…”

Integrating GWAS and Transcriptomics to Identify the Molecular Underpinnings of Thermal Stress Responses in Drosophila melanogaster

“…Neuronal failure operationally defines both CT min and CT max (Andersen et al, 2018;Andersen and Overgaard, 2019;Jørgensen et al, 2019), and dynamic stabilization of the neuromuscular circuit under temperature stress is a likely mechanism for altering thermal limits. Indeed, previous investigation of the genetic architecture of cold hardiness and electrophysiological analyses of the rapid hardening response both suggest an important role for stabilization of ion channels and cytoskeletal structures supporting the synapse and neuromuscular junction (Klose and Robertson, 2004;Robertson and Money, 2012;Freda et al, 2017). Aside from genes involved in neural morphogenesis, the GO term extracellular structure organization was overrepresented among cold tolerance genes, and this was the only overrepresented category that did not overlap with the differential expression categories.…”

“…For example, two plastic responses to cold, rapid cold hardening and developmental cold acclimation, have non-overlapping SNPs associated with them, although the genes associated with these traits share some functional similarities (Gerken et al, 2015). Similarly, Teets and Hahn (2018) found minimal overlap in genes associated with cold shock response and chill coma recovery, and Freda et al (2017) found no overlap in genes associated with adult and larval cold hardiness. The candidate genes identified in Teets and Hahn (2018) were functionally tested with RNAi, and knockdown of most genes affected cold tolerance, indicating that GWAS is a robust method for identifying genes with functional roles in thermal tolerance.…”