Hybridization alters the shape of the genotypic fitness landscape, increasing access to novel fitness peaks during adaptive radiation

Estimating the complex relationship between fitness and genotype or
phenotype (i.e. the adaptive landscape) is one of the central goals of
evolutionary biology. 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. We leveraged whole-genome sequencing of 139
hybrids from two independent field fitness experiments to identify the
genomic basis of fitness, estimate genotypic fitness networks, 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 out of the 13 regions most strongly associated with
fitness 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 reduced fitness
landscape ruggedness as compared to standing variation, increasing the
accessibility of genotypic fitness paths from generalist to specialists.
Our results suggest that adaptive introgression and de
novo mutations alter the shape of the fitness landscape,
providing key connections in adaptive walks circumventing fitness valleys
and triggering the evolution of novelty during adaptive radiation.