Temperature-dependent behaviours are genetically variable in the nematode Caenorhabditis briggsae

Abstract

SUMMARY Temperature-dependent behaviours inCaenorhabditis elegans, such as thermotaxis and isothermal tracking, are complex behavioural responses that integrate sensation, foraging and learning, and have driven investigations to discover many essential genetic and neural pathways. The ease of manipulation of the Caenorhabditis model system also has encouraged its application to comparative analyses of phenotypic evolution, particularly contrasts of the classic model C. elegans with C. briggsae. And yet few studies have investigated natural genetic variation in behaviour in any nematode. Here we measure thermotaxis and isothermal tracking behaviour in genetically distinct strains of C. briggsae, further motivated by the latitudinal differentiation in C. briggsae that is associated with temperature-dependent fitness differences in this species. We demonstrate that C. briggsae performs thermotaxis and isothermal tracking largely similar to that of C. elegans, with a tendency to prefer its rearing temperature. Comparisons of these behaviours among strains reveal substantial heritable natural variation within each species that corresponds to three general patterns of behavioural response. However, intraspecific genetic differences in thermal behaviour often exceed interspecific differences. These patterns of temperature-dependent behaviour motivate further development of C. briggsae as a model system for dissecting the genetic underpinnings of complex behavioural traits. Supplementary material available online at

Genome structure predicts modular transcriptome responses to genetic and environmental conditions

“…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. 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.…”

“…Here, we quantified transcriptome expression for C. briggsae nematodes from populations with distinct genetic backgrounds adapted to temperature differences associated with their origins in tropical vs. temperate latitudes (Poullet, Vielle, Gimond, Ferrari, & Braendle, ; Prasad, Croydon‐Sugarman, Murray, & Cutter, ; Stegeman, Bueno de Mesquita, Ryu, & Cutter, ). 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, ; Felix et al, ; Jovelin & Cutter, ; Thomas, Wang, & Jovelin, ).…”

Gametic selection, developmental trajectories, and extrinsic heterogeneity in Haldane's rule

“…In some cases, one sex is more strongly affected by environmental changes (e.g., Hutter and Ashburner 1987;Wade et al 1999). Temperature differences also appear to act as an important selective agent within C. briggsae (Prasad et al 2011;Stegeman et al 2013) and between C. briggsae and C. nigoni (Woodruff et al 2010). We therefore examined the effect of temperature on total offspring production and sex ratio of both pure C. nigoni crosses and C. nigoni hybridized with C. briggsae males (virtually no F1 hybrid males are produced in the reciprocal hybrid cross, precluding evaluation of their temperature sensitivity).…”

Full-genome evolutionary histories of selfing, splitting, and selection in Caenorhabditis

“…Indeed, this species is now an active target of research into the molecular basis of trait variation and adaptation (Baird et al 2005;Prasad et al 2011;Ross et al 2011;Stegeman et al 2013), the evolution of development (Delattre and Félix 2001;Hill et al 2006;Guo et al 2009;Marri and Gupta 2009), and speciation (Woodruff et al 2010;Baird and Stonesifer 2012;Kozlowska et al 2012;Yan et al 2012). Yet, the limited genomic scope of understanding for its natural variation constrains our ability to fully exploit it.…”