Oxygen-induced social behaviours in Pristionchus pacificus have a distinct evolutionary history and genetic regulation from Caenorhabditis elegans

Abstract

Wild isolates of the nematode Caenorhabditis elegans perform social behaviours, namely clumping and bordering, to avoid hyperoxia under laboratory conditions. In contrast, the laboratory reference strain N2 has acquired a solitary behaviour in the laboratory, related to a gain-of-function variant in the neuropeptide Y-like receptor NPR-1. Here, we study the evolution and natural variation of clumping and bordering behaviours in Pristionchus pacificus nematodes in a natural context, using strains collected from 22 to 2400 metres above sea level on La Réunion Island. Through the analysis of 106 wild isolates, we show that the majority of strains display a solitary behaviour similar to C. elegans N2, whereas social behaviours are predominantly seen in strains that inhabit high-altitude locations. We show experimentally that P. pacificus social strains perform clumping and bordering to avoid hyperoxic conditions in the laboratory, suggesting that social strains may have adapted to or evolved a preference for the lower relative oxygen levels available at high altitude in nature. In contrast to C. elegans, clumping and bordering in P. pacificus do not correlate with locomotive behaviours in response to changes in oxygen conditions. Furthermore, QTL analysis indicates clumping and bordering to represent complex quantitative traits. Thus, clumping and bordering behaviours represent an example of phenotypic convergence with a different evolutionary history and distinct genetic control in both nematode species.

Succession and dynamics of Pristionchus nematodes and their microbiome during decomposition of Oryctes borbonicus on La Réunion Island

“…Studies on La R eunion Island in the Indian Ocean revealed that P. pacificus has invaded this island multiple times independently with different carrier beetles, resulting in this island harboring the complete worldwide diversity of P. pacificus haplotypes (Herrmann et al, 2010;Morgan et al, 2012). Indeed, the population structure and evolutionary history of P. pacificus on La R eunion Island provided a paradigm for detailed studies of the nematodesadaptations to new environments 2014;2016;Morgan et al, 2014;Moreno et al, 2016). Among several P. pacificus hosts on La R eunion, the endemic rhinoceros beetle Oryctes borbonicus represents an interesting study system because more than 90% of beetle individuals harbor P. pacificus dauer larvae (Morgan et al, 2012).…”

Differential variant calling in mutants from diverse genetic backgrounds: A case study in the nematode Pristionchus pacificus

“…We propose that a heuristic variant calling procedure simultaenously taking into account the mutant and the wildtype sample is enough to define more reliable sets of candidate mutations. b) The strain RSB001 shows a so called bordering behaviour, which has also been observed in C. elegans but has a different genetic basis [18]. c) A single wildtype worm of P. pacificus .…”

“…Based on world-wild field trips to sample more nematode strains, we have recently discovered one P. pacificus strain, RSB001, on a high altitude location on la Reunion Island in the Indian Ocean that shows a so called bordering behaviour ( Fig. 1a,b) that has also been observed in C. elegans [17] but is not controlled by the same gene [18]. Whole genome resequencing data has shown that this and other strains of the same genetic lineage are roughly 1% divergent from the standard P. pacificus reference strain PS312 (isolated in California, USA) [15,19].…”

Social creatures: Model animal systems for studying the neuroendocrine mechanisms of social behaviour

“…Interestingly, strains of another free‐living nematode species, Pristionchus pacificus, which is only distantly related to C. elegans , also display oxygen‐induced social behaviour. However, this behaviour is not regulated by npr‐1 …”