The first genotypic fitness network in a vertebrate reveals that hybridization increases access to novel fitness peaks

Abstract

AbstractEstimating 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 the process by which fitness valleys are crossed remains 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, visualize the first genotypic fitness networks in a vertebrate system, and measure the accessibility of adaptive walks on the fitness landscape. 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 (mettle21e) was also misexpressed in hybrids, suggesting a potential intrinsic genetic incompatibility. We then constructed genotypic fitness networks from adaptive alleles and showed that scale-eating specialists are most isolated on these networks. Furthermore, only introgressed and de novo variants, not standing genetic variation, increased the accessibility of genotypic fitness paths from generalist to specialists. Our results suggest that adaptive introgression and de novo mutations provided key connections in adaptive walks necessary for crossing fitness valleys and triggering the evolution of novelty during adaptive radiation.SignificanceThe fitness landscape describes the complex relationship between genotype or phenotype and fitness and is the conceptual bridge between micro- and macroevolution. There are many studies of phenotypic fitness landscapes across a range of animal and plant taxa, but studies of the genotypic fitness landscape remain limited to microbial systems and the function of individual proteins. Here, we conducted the first study investigating the genotypic fitness landscape for organismal fitness in an exceptionally young vertebrate adaptive radiation including a generalist algivore, molluscivore, and scale-eating pupfish. We show that hybridization and de novo mutations increase the availability of accessible pathways to new fitness peaks on the fitness landscape, enabling the evolution of novelty.