Functional convergence of genomic and transcriptomic genetic architecture underlying sociability in a live-bearing fish

The organization and coordination of fish schools provide a valuable model to investigate the genetic architecture of affiliative behaviors and dissect the mechanisms underlying social behaviors and personalities. We used quantitative genetic methods in replicate guppy selection lines that vary in schooling propensity to investigate the genetic basis of sociability phenotypes. Alignment and attraction, the two major traits forming the sociability personality axis in this species, showed heritability estimates at the upper end of the range previously described for social behaviors, with important variation across sexes. Consistent with findings in collective motion patterns, experimental evolution of schooling propensity increases the sociability of female, but not male, guppies when swimming with unfamiliar conspecifics, a highly relevant trait in a species with fission-fusion social systems in natural populations. Our results from PoolSeq and RNASeq convergently identify genes involved in neuron migration and synaptic function, highlighting a crucial role of glutamatergic synaptic function and calcium-dependent signaling processes in the evolution of schooling.