Hybridization alters the shape of the genotypic fitness landscape, increasing access to novel fitness peaks during adaptive radiation
Authors: Austin Patton 1; Emilie Richards 1; Katelyn Gould 2; Logan Buie 2; Christopher Martin 1
Affiliations: 1) University of California, Berkeley, CA; 2) University of North Carolina, Chapel Hill, NC
Keywords: Speciation & hybridization
Estimating the complex relationship between fitness and genotype or phenotype (i.e. the adaptive landscape) is one of the central goals of evolutionary biology. Empirical fitness landscapes have now been estimated for numerous systems, from phage to proteins to finches. However, adaptive walks connecting genotypes to organismal fitness, speciation, and novel ecological niches are still poorly understood and processes for surmounting fitness valleys remain controversial. One outstanding system for addressing these connections is a recent adaptive radiation of ecologically and morphologically novel pupfishes (a generalist, molluscivore, and scale-eater) endemic to San Salvador Island, Bahamas. Here, we leveraged whole-genome sequencing of 139 hybrids from two independent field fitness experiments to identify the genomic basis of fitness, estimate genotypic fitness landscapes, and measure the accessibility of adaptive walks. We identified 132 SNPs that were significantly associated with fitness in field enclosures. Six fitness-associated regions contained differentially expressed genes and fixed SNPs between trophic specialists; one gene (mettl21e) was also misexpressed in lab-reared hybrids, suggesting a potential intrinsic genetic incompatibility. We then constructed genotypic fitness networks from adaptive alleles and show that scale-eating specialists are the most isolated of the three species on these networks. Intriguingly, introgressed and de novo variants altered the topography of the fitness landscape, increasing the accessibility of genotypic fitness paths from generalist to specialists as compared to standing variation. Our results suggest that adaptive introgression and de novo mutations alter the shape of the fitness landscape, mitigating the need to cross adaptive valleys in adaptive walks, thus triggering the evolution of novelty during adaptive radiation.