Ancient inversion polymorphisms associate with sexually selected traits across natural guppy populations

Understanding the distribution, frequency, and long-term persistence of chromosomal inversions in natural populations is key to understanding population evolution and adaptive processes. Inversions often span multiple genes, are subject to strong selective pressures and can affect complex traits. Here, we used an unbiased method to identify inversions in guppies from three different Trinidadian rivers with paired high- and low-predation populations which differ in a wide range of morphological, behavioural and life-history traits. We identified 22 inversions, ranging in age from 1 to 6 million years, which are widespread across the genome and predate the colonisation of each river. We were able to verify the breakpoints for all but one of these inversions using linked reads. We find three inversions that are significantly associated with local adaptation syndromes in high- versus low-predation populations, however, none are reciprocally fixed throughout all three replicate rivers. Additionally, we observe seven additional inversions maintained in all three rivers without evidence of local adaptation. Simulations reveal that the level of inversion polymorphism that we observe is far greater than expected under a neutral model. We observed a significant overlap between polymorphic inversions and loci previously implicated in male ornament pattern variation in guppies, suggesting that negative frequency-dependent selection due to female preference for male pattern novelty might explain the maintenance of inversion polymorphism. Overall, our results show the role of sexual selection in the long-term maintenance of inversion polymorphisms, and an interplay between sexual and natural selection in frequency dynamics.