Abstract
The standard reference Caenorhabditis elegans strain, N2, has evolved marked behavioral changes in social feeding behavior since its isolation from the wild. We show that the causal, laboratory-derived mutations in two genes, npr-1 and glb-5, confer large fitness advantages in standard laboratory conditions. Using environmental manipulations that suppress social/solitary behavior differences, we show the fitness advantages of the derived alleles remained unchanged, suggesting selection on these alleles acted through pleiotropic traits. Transcriptomics, developmental timing, and food consumption assays showed that N2 animals mature faster, produce more sperm, and consume more food than a strain containing ancestral alleles of these genes regardless of behavioral strategies. Our data suggest that the pleiotropic effects of glb-5 and npr-1 are a consequence of changes to O2 -sensing neurons that regulate both aerotaxis and energy homeostasis. Our results demonstrate how pleiotropy can lead to profound behavioral changes in a popular laboratory model.
Highlights
It is tempting to compare the endless forms of life and create adaptive hypotheses to explain their differences
Our work suggests that fitness gains are due to increases in food consumption and changes in reproductive timing, mediated by O2-sensing body cavity neurons that are required for social feeding behaviors
We further investigated the developmental regulation of these 652 genes using previously published transcriptomics data isolated from hermaphrodites or males at specific developmental time points (Boeck et al, 2016) (Figure 5d)
Summary
It is tempting to compare the endless forms of life and create adaptive hypotheses to explain their differences. With declining costs of DNA sequencing, researchers can identify genes and regions of DNA that are likely to be under selection They must be careful before leaping to the conclusion that behavioral differences linked to genetic changes are adaptive. A small number (~100) of new mutations that arose and fixed in the N2 strain following isolation from the wild have been identified (McGrath et al, 2011), including a neomorphic, missense mutation in the neuropeptide receptor gene npr-1 and a recessive, 765 bp duplication in the nematode-specific globin gene glb-5 These mutations were originally identified for their role in foraging and aerotaxis behaviors and were initially thought to represent natural genetic variants (de Bono and Bargmann, 1998; Persson et al, 2009) (Figure 1a). Our work demonstrates that even when alleles are identified that confer fitness advantages, care must be taken in inferring the phenotypes that are responsible due to the pleiotropic actions of genetic changes
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