The genetic architecture and evolution of continuous reaction norms: dissecting the thermal performance curve

Abstract

n n n n n n Genotypes can seldom achieve maximal performance across all environments theyinhabit. Instead, increased performance in one environment often comes at a cost of lowerperformance in another. Such effects are the consequence of genotype-by-environmentinteractions, which are usually studied using reaction normsmfunctions describing therelationship between trait and environment. When the environmental variable iscontinuous rather than discrete, a continuous reaction norm is investigated, also known asfunction-valued or infinite dimensional traits. Through the study of continuous reactionnorms, trade-offs that shape evolutionary trajectories can be identified. Whilst reactionnorms have been studied extensively, we know little about their genetic basis, specificallytheir mutational inputs and the types of genes and genetic effects involved.n n n n n n Thermal performance curves (TPC) are a specific, but common, class of continuousreaction norm mapping the response of a performance-associated trait to environmentaltemperature. TPCs are commonly used to explore the trade-offs involved in thermaladaption for ectothermic organisms. Three major lmodesr of variation have been identified;a lfaster-slowerr axis representing overall increases or decreases in performanceregardless of temperature, a lhotter-colderr axis representing a trade-off between hot andcold temperatures, and a lgeneralist-specialistr axis which explores a trade-off between therange of temperatures across which an organism can perform effectively and the maximallevel of performance it can achieve. In this thesis, I have conducted three empirical studiesusing locomotor activity in two Drosophila species to investigate the genetic architecture ofTPCs.n n n n n n My first study investigated the contribution of new mutations to TPCs through amutation accumulation assay followed by an eigendecomposition of the mutationalvariance-covariance matrix, M. Three independent axes of mutational variance wereinvestigated that corresponded to the three major axes of TPC variation. In contrast to itsnear-absence from standing variation in this species, a lfaster-slowerr axis, accounted formost mutational variance (75% in males and 66% in females) suggesting selection mayeasily fix or remove these types of mutations in outbred populations. Axes resembling thelhotter-colderr and lgeneralist-specialistr modes of variation contributed less mutationalvariance but nonetheless point to an appreciable input of new mutations to the two majortrade-offs involved in thermal adaptation.n n n n n n In my second study, I began to dissect the genotype-phenotype map for TPCs. Amultivariate quantitative trait loci (QTL) analysis was performed on a panel of recombinantinbred lines (RILs) derived from an inter-population cross of Drosophila serrata. I foundthat vectors of QTL effects across temperatures were well-aligned with the major axes ofgenetic variance in the RIL population. Most QTL effects resembled either a lfaster-slowerror lhotter-colderr axis whereas very few resembled lgeneralist-specialistr like variation andthose that did had small effects. Strong and directionally-biased transgressive segregationwas also detected, consistent with weak selection between the two founder populationsand a highly polygenic basis to TPC variation.n n n n n n In the final study, I dissected the genetic architecture locomotor activity TPCs in asingle population of Drosophila melanogaster. A genome-wide association study (GWAS)was conducted by assaying the TPC variation in 152 lines from the Drosophila GeneticReference Panel (DGRP). The analysis was performed on four major components of theTPCs that were statistically extracted using a function-valued trait analysis (TMV) and onthe first five principal component (PC) scores in an attempt to identify genomic elementsunderlying the biologically important axes of TPC variation. I identified polymorphismsassociated with loverall heightr, optimum temperature, lgeneralist-specialistr and maximumperformance TPC components of variation and the first five PC axes. Intriguingly, forcomponents underlying thermal trade-offs, I observed strong skew in the direction in whichthe minor-frequency allele affected a TPC component and some of the PC axes,suggesting a role for natural selection in shaping standing variation. Although mostsignificant variants were located within or near coding genes, they were located in areasmore consistent with the regulation of gene expression than altering coding sequences,suggesting that changes in gene expression may be particularly important. Limitedpleiotropic effects were detected between different TPC components possibly reflectingtheir highly optimised statistical partitioning along different trade-off axes. Gene ontologyterm enrichment analysis, revealed a degree of functional independence between thedifferent modes of variation, which may translate into evolutionary independence betweenthem. Where functional overlap did occur, it primarily involved neurological functioning andresponses to stimuli.n n n n n n My thesis places TPCs as highly complex traits, integrating a significant number ofbiological functions. It is clear that genetic variance is far from being equally distributedacross the three major components of variationmlikely a consequence of both contrasting ivmutational inputs and differences in the efficacy of natural selection to shape standingvariation. A role for selection in shaping standing variation is implicated in both speciesthrough either mismatches between patterns of mutational and standing variation orassociations between allele frequency and the directions of additive effects on phenotype.Whilst this thesis has outlined the evolutionary genetic architecture of a single type of TPC,genomic-level investigation into these continuous reaction norms is only beginning.