Cryptic variation in vulva development by cis-regulatory evolution of a HAIRY-binding site

Abstract

Robustness to mutations is a general principle of biological systems that allows for the accumulation of cryptic variation. However, little is known about robustness and cryptic variation in core developmental pathways. Here we show through gonad-ablation screens in natural isolates of Pristionchus pacificus cryptic variation in nematode vulva development. This variation is mainly caused by cis-regulatory evolution in the conserved Notch ligand apx-1/Delta and involves binding sites for the transcription factor HAIRY. In some isolates, including a Bolivian strain, absence of a HAIRY-binding site results in Ppa-apx-1 expression in the vulva precursor cell P6.p and causes gonad-independent vulva differentiation. In contrast, a Californian strain that gained a HAIRY-binding site lacks Ppa-apx-1 vulval expression and shows gonad-dependence of vulva development. Addition of this HAIRY-binding site to the Bolivian Ppa-apx-1 promoter eliminates expression in the vulva. Our findings indicate significant cis-regulatory evolution in a core developmental pathway leading to intraspecific cryptic variation.

A locus inPristionchus pacificusthat is responsible for the ability to give rise to fertile offspring at higher temperatures

“…The 186 strains lost were either killed during the transfer process, crawled onto the wall of the petri dish and dried out, or because of genetic incompatibilities between the two parental strains. The number of strains lost is consistent with previous mapping panels made for P. pacificus (Kienle and Sommer, 2013). The phenotype of each surviving recombinant inbred line (RIL) was determined: 89 were Htt and 125 were Ltt, suggesting that there is some underestimation of the number of Htt strains possibly due to outbreeding suppression that would reduce the fitness of hybrids across all temperatures.…”

Oxygen-induced social behaviours inPristionchus pacificushave a distinct evolutionary history and genetic regulation fromCaenorhabditis elegans

“…While the insufficient number of recombination events among the 94 RILs did not permit the identification of individual candidate genes, it allows the conclusion that P. pacificus social behaviours are regulated by complex quantitative traits. Furthermore, these data indicate that a substantially larger number of RILs will be necessary to clone individual QTLs, an endeavour that was very successful for other variable traits in P. pacificus strains [30,31]. In C. elegans, a sequence polymorphism in npr-1 underlies the behavioural difference between social and solitary strains [14].…”

Genome-wide analysis of trans-splicing in the nematode Pristionchus pacificus unravels conserved gene functions for germline and dauer development in divergent operons

“…P. pacificus has been developed as a model system for studies of evolution, ecology, and comparative analysis with C. elegans (Hong and Sommer 2006;Sommer and McGaughran 2013). Such analyses have uncovered evolutionary diversifications in various processes such as vulva formation Wang and Sommer 2011;Kienle and Sommer 2013), gonad development (Rudel et al 2005(Rudel et al , 2008, dauer development (Ogawa et al 2009(Ogawa et al , 2011Sinha et al 2012a), innate immune response (Rae et al 2010;Sinha et al 2012b), and synaptic connectivity (Bumbarger et al 2013), during the evolutionary time separating the two species. A genome-wide characterization of the trans-splicing landscape and annotation of operonic genes in related nematode models such as P. pacificus is therefore an important first step in identifying conserved roles for operons in these two species.…”