Genetically distinct behavioral modules underlie natural variation in thermal performance curves

Abstract

Article SummaryPlastic responses to environmental inputs, reaction norm phenotypes that can be summarized with parameters of fits to a mathematical function, are pervasive across diverse organismal traits and crucial to organismal fitness. We quantified the nematode Caenorhabditis briggsae's behavioral thermal performance curves as function-valued traits for 23 wild isolate genotypes and 153 recombinant inbred lines. We identified quantitative trait loci on multiple chromosomes that define genetically distinct behavioral modules contributing to the emergent overall behavioral thermal performance curve. These findings highlight how dynamic behavioral responses to environmental inputs can evolve through independent changes to genetically distinct modular components of such complex phenotypes.

Genome structure predicts modular transcriptome responses to genetic and environmental conditions

“…GO term enrichment in M7 indicates disproportionate representation of genes with nervous system function, including 11 GABA and 11 acetylcholine receptor activity genes, such as the ortholog of C. elegans nicotinic acetylcholine receptor acr‐9 . This nervous system enrichment of M7 is salient due to the HK104 and AF16 strains of C. briggsae differing in rearing‐dependent thermal taxis and locomotion (Stegeman et al, , ), a suite of behaviours under neural control.…”

“…Other autosomes, however, were especially enriched (or under‐enriched) for genes in particular modules; for example, genes from M21 were 2.3‐fold enriched on chromosome III and genes from M16 were 2.0‐fold enriched on chromosome V (Figure ). Given the extreme enrichment on chromosome V for M16 and its genotype‐specific expression response at 30°C (Figure ), it is notable that a quantitative trait locus (QTL) mapping study in C. briggsae found QTL on chromosome V to control differences in heat‐sensitive movement behaviours (Stegeman et al, ).…”

“…Given this ecological context, along with resources such as recombinant inbred line (RIL) libraries and chromosome‐scale genome assembly (Ross et al, ; Stegeman, Baird, Ryu, & Cutter, ), C. briggsae represents a valuable system to understand the links between temperature and genetic background in differential gene expression. The exemplar tropical and temperate genotypes used as RIL parents (AF16 and HK104), the focus of the present study, exhibit diverse temperature‐dependent phenotypic differences consistent with adaptive differentiation of the phylogeographic groups overall, including for fecundity (~2‐fold difference at 14°C and ~4‐fold difference at 30°C), motility and gamete developmental traits (Poullet et al, ; Prasad et al, ; Stegeman et al, , ). By rearing these animals at hot and cold sublethal temperatures near their fertile limits, as well as under benign thermal conditions, we characterize genotypic and environmentally induced differential gene expression across the genome.…”

“…Global collections and population genomic analyses of C. briggsae wild isolates from tropical and temperate regions show that they form distinct phylogeographic groups (Cutter, Félix, Barriere, & Charlesworth, 2006;Felix et al, 2013;Jovelin & Cutter, 2011;Thomas, Wang, & Jovelin, 2015). Given this ecological context, along with resources such as recombinant inbred line (RIL) libraries and chromosomescale genome assembly (Ross et al, 2011;Stegeman, Baird, Ryu, & Cutter, 2019), C. briggsae represents a valuable system to understand the links between temperature and genetic background in differential gene expression. The exemplar tropical and temperate genotypes used as RIL parents (AF16 and HK104), the focus of the present study, exhibit diverse temperature-dependent phenotypic differences consistent with adaptive differentiation of the phylogeographic groups overall, including for fecundity (~2-fold difference at 14°C and ~4-fold difference at 30°C), motility and gamete developmental traits (Poullet et al, 2015;Prasad et al, 2011;Stegeman et al, 2019Stegeman et al, , 2013.…”

Genome structure predicts modular transcriptome responses to genetic and environmental conditions

“…Given the extreme enrichment on Chromosome V for M16 and its genotype-specific expression 445 response at 30°C (Figure 3), it is notable that a quantitative trait locus (QTL) mapping study in 446 C. briggsae found QTL on Chromosome V to control differences in heat-sensitive movement 447 behaviors (Stegeman et al 2019). 448…”