The Orphan Gene dauerless Regulates Dauer Development and Intraspecific Competition in Nematodes by Copy Number Variation

Abstract

Many nematodes form dauer larvae when exposed to unfavorable conditions, representing an example of phenotypic plasticity and a major survival and dispersal strategy. In Caenorhabditis elegans, the regulation of dauer induction is a model for pheromone, insulin, and steroid-hormone signaling. Recent studies in Pristionchus pacificus revealed substantial natural variation in various aspects of dauer development, i.e. pheromone production and sensing and dauer longevity and fitness. One intriguing example is a strain from Ohio, having extremely long-lived dauers associated with very high fitness and often forming the most dauers in response to other strains´ pheromones, including the reference strain from California. While such examples have been suggested to represent intraspecific competition among strains, the molecular mechanisms underlying these dauer-associated patterns are currently unknown. We generated recombinant-inbred-lines between the Californian and Ohioan strains and used quantitative-trait-loci analysis to investigate the molecular mechanism determining natural variation in dauer development. Surprisingly, we discovered that the orphan gene dauerless controls dauer formation by copy number variation. The Ohioan strain has one dauerless copy causing high dauer formation, whereas the Californian strain has two copies, resulting in strongly reduced dauer formation. Transgenic animals expressing multiple copies do not form dauers. dauerless is exclusively expressed in CAN neurons, and both CAN ablation and dauerless mutations increase dauer formation. Strikingly, dauerless underwent several duplications and acts in parallel or downstream of steroid-hormone signaling but upstream of the nuclear-hormone-receptor daf-12. We identified the novel or fast-evolving gene dauerless as inhibitor of dauer development. Our findings reveal the importance of gene duplications and copy number variations for orphan gene function and suggest daf-12 as major target for dauer regulation. We discuss the consequences of the novel vs. fast-evolving nature of orphans for the evolution of developmental networks and their role in natural variation and intraspecific competition.

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].…”

Deep taxon sampling reveals the evolutionary dynamics of novel gene families in Pristionchus nematodes

“…Although extensive comparative genomic studies did show some evidence of horizontal gene transfer (Dieterich et al 2008;Rödelsperger and Sommer 2011;Meyer et al 2016), this process could only explain the origin of a handful of orphan gene families. In addition to the high abundance of orphan genes within the genome of P. pacificus, we recently showed that most orphan genes are real (Prabh and Rödelsperger 2016) and they can regulate ecologically relevant traits (Mayer et al 2015).…”

Parallel adaptation to higher temperatures in divergent clades of the nematodePristionchus pacificus

“…with evidence for intraspecific competition, this suggests a process of incipient 106" speciation in P. pacificus [25,26].…”

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