Cryptic intraspecific variation in sex determination in Caenorhabditis elegans revealed by mutations

Abstract

Sex determination mechanisms (SDMs) show striking diversity and appear to evolve rapidly. Although interspecific comparisons and studies of ongoing major transitions in sex determination (such as the establishment of new sex chromosomes) have shed light on how SDMs evolve, comparatively little attention has been paid to intraspecific variation with less drastic effects. In this study, I used mutant strains carrying a temperature-sensitive sex determination mutation, along with a second null mutation, in different wild genetic backgrounds to uncover hidden variation in the SDM of the model nematode Caenorhabditis elegans. I then used quantitative trait locus (QTL) mapping to begin to investigate its genetic basis.I identified several QTLs, and although this variation apparently involved genotype-by-temperature interactions, QTL effects were generally consistent across temperatures. These QTLs collectively and individually explained a relatively large fraction of the variance in tail morphology (a sexually dimorphic trait), and two QTLs contained no genes known to be involved in somatic sex determination. These results show the existence of within-species variation in sex determination in this species, and underscore the potential for microevolutionary change in this important developmental pathway.

Causes and Consequences of Genetic Background Effects Illuminated by Integrative Genomic Analysis

“…Instead, these networks occur in the context of all the alleles in the genome, which usually vary among individuals. There is substantial evidence that wild-type genetic background almost always modulates the phenotypic effects of mutations (e.g., McKenzie et al 1982;Threadgill et al 1995;Atallah et al 2004;Milloz et al 2008;Chandler 2010;Dowell et al 2010;Gerke et al 2010). The influence of wild-type genetic backgrounds also extends to interactions among mutations (Remold and Lenski 2004;Dworkin et al 2009;Wang et al 2013b), altering patterns of epistasis, and these complex interactions are likely widespread .…”

Hidden variation mapped

“…The extent of such cryptic genetic variation has so far been underestimated because of the difficulty in detecting it. In this issue, cryptic genetic variation affecting somatic sex determination mechanisms is revealed among wild isolates of the nematode Caenorhabditis elegans (Chandler, 2010). Using a quantitative genetic approach, the author detected several genomic regions underlying this variation.…”

“…These polymorphisms may not necessarily affect known components of the sex determination pathway, as cryptic variation could subtly affect sexual fate through genes whose effects were undetectable in classical genetic screens. Indeed, Chandler (2010) found that some QTLs (such as the chromosome IV QTL) map in intervals containing known sex determination genes, whereas others do not.…”

“…With these genotyping and phenotyping data, different statistical methods are then used to estimate the number and position of the genetic loci involved in the phenotypic variation (QTLs), as well as the intensity and sign of their effect, and possible epistasis between them. Chandler (2010) chose to use RILs, an approach which is becoming popular for QTL analyses in C. elegans (Kammenga et al, 2008;Rockman and Kruglyak, 2009). The construction of a large set of RILs is easy in C. elegans because of its short generation time and selfing mode of reproduction.…”

“…The two mutations tra-2(ar221ts) and xol-1(y9) originally obtained in the reference N2 background were introgressed by repeated outcrosses in the CB4856 background. The resulting strains exhibit different degrees of somatic masculinization, revealing cryptic genetic variation within C. elegans (Chandler, 2010). (c) Recombinant inbred lines (RILs) construction scheme.…”