Parallel Sympatric Divergence Driven by Disruptive Selection Acting on a Magic Temporal Isolation Trait in a Wild Annual Fish

Sympatric speciation has long been of key interest among biologists, investigating how selection drives speciation in the absence of geographic isolation. However, the evolutionary trajectories and genetic architectures that underlie sympatric ecological divergence remain poorly understood. For the annual fish, Neosalanx brevirostris, from lakes in the Yangtze River basin, two sympatric ecotypes exhibit differences in reproductive season, with one breeding in spring and the other in autumn. Reproductive timing is considered a 'magic trait' in sympatric speciation, as it is both ecologically relevant and facilitates assortative mating. Using population genomic approaches, we investigated the genetic architecture of the adaptive sympatric divergence in reproductive season and the evolutionary forces driving this divergence by comparing two breeding ecotype pairs from two lakes and their ancestral anadromous population. Population genetic structure results provided strong evidence that sympatric ecological divergence has evolved independently and repeatedly in both lakes. Furthermore, we identified a set of genome-wide candidate adaptive SNPs, which were present as standing genetic variations in ancestral population with high frequencies, and changes of allele frequency support that disruptive natural selection, induced by intensive resource competition, drove the reproductive season divergence. These adaptive SNPs were involved in various biological functions pertinent to reproductive timing, including photosensory, circadian entrainment, temperature sensing, and hormone signalling, highlighting the complex genetic architecture underlying reproductive seasonality. These findings provide valuable insights into the evolutionary trajectories and genetic architecture in the early stages of sympatric ecological divergence and speciation.