Hybridization and the genomic basis of adaptive radiation in Caribbean pupfish and Cameroonian crater lake cichlids

Adaptive radiations have fascinated evolutionary biologists for centuries for the bursts of phenotypic, ecological and species diversity they contain. The availability of resources in new environments with few competitors has long been seen as the major force driving adaptive radiations, but it is an equally longstanding question why only some lineages rapidly diversify in response to such new ecological opportunities while others do not. Thus, the origins and major features of adaptive radiations are still controversial./nIn Chapter 1, I find evidence of introgression following past hybridization events in the genomes of species from a rare radiation of trophic specialist Cyprinodon pupfish endemic to San Salvador Island, Bahamas. Extensive histories of hybridization are quickly becoming another common feature that most classic adaptive radiations share, such hybridization with other species is now being viewed as another major force driving adaptive radiations in addition to ecological opportunity. Using whole genome resequencing of 42 individuals, I characterized signatures of genetic divergence and selection between the three species of the San Salvador Island radiation to identify regions of the genome involved in diversification processes on this island and found some of these regions also contain signatures of introgression, supporting a role for hybridization bringing in adaptive variation potentially relevant for the phenotypic and ecological divergence observed in trophic specialists of the radiation./nIn Chapter 2, I searched for genomic signatures of secondary contact and introgression in one of the most convincing examples of sympatric speciation in the wild: the Barombi Mbo cichlid radiation. Using whole genome resequencing of 28 individuals, I characterized genetic and functional diversity in regions of the genome that have experienced gene flow differently among the species to determine the role of gene flow in the speciation process. I discovered signatures of introgression that were not shared between all species in the radiation, suggesting that hybridization with allopatric populations did occur after species divergence had already begun within the radiation. Such evidence has previously been used to reject potential case studies of sympatric speciation because it’s likely that allopatric divergence contributed to the speciation events observed. However, amongst the sympatric species of the Barombi Mbo radiation, very few regions of the genome appear to have experienced differential introgression of genetic variation from allopatric outgroup populations and there was no clear evidence that introgression following the initial stages of diversification into different species in lake brought in essential adaptive genetic variation for ecological and morphological diversity. This finding emphasizes the equivocal support that simply documenting hybridization and secondary contact in a system has on its relevancy to speciation processes and suggest that we should not rule out the possibility of sympatric speciation in one of the most celebrated examples in nature quite yet./nIn Chapter 3, I reviewed theoretical models of speciation and revisit how we can connect them to the findings from recent genomic re-analyses of classic sympatric speciation case studies in the wild have revealed complex histories of secondary gene flow from outgroups. These documented histories of gene flow post-initial divergence have cast doubt on the status of sympatric speciation since they call in question whether any allopatric divergence in the outgroup populations has contributed to speciation processes within the sympatric speciation case study. I summarize theoretical differences among different types of sympatric speciation and speciation-with-gene-flow models, and propose genomic analyses for distinguishing which models apply to any given empirical case study based on the timing and function of adaptive introgression. Investigating whether secondary gene flow contributed to reproductive isolation in these empirical case studies will aid the field in better determining whether predictions of sympatric speciation theory are ultimately borne out in nature./nIn Chapter 4, I expanded on the findings of adaptive introgression in the rare radiation of trophic specialists pupfish on San Salvador Island to test the hybrid origins hypothesis that adaptive radiations originate from hybrid swarms. To do this, I reconstructed the spatial and temporal histories of adaptive alleles underlying major phenotypic axes of diversification from the genomes of 202 Caribbean pupfishes. Using a combination of population genomics, transcriptomics, and genome-wide association mapping, I demonstrate that this microendemic adaptive radiation of trophic specialists on San Salvador Island, Bahamas experienced twice as much adaptive introgression as generalist populations on neighboring islands. Additionally using selective sweep timing analyses, I find evidence that adaptive divergence occurred in stages of diversification across different sources of genetic variation and trait axes once the radiation started. First, standing regulatory variation in genes associated with feeding behavior were swept to fixation by selection, then standing regulatory variation in genes associated with craniofacial and muscular development and finally a de novo non-synonymous substitution in an osteogenic transcription factor swept to fixation most recently. These results support another major hypothesis about adaptive radiations: that they proceed in temporal stages of divergence along different trait axes. The results from this study overall demonstrate how ancient alleles maintained in distinct environmental refugia can be assembled into new adaptive combinations to form adaptive radiations./nFinally, in Chapter 5, I characterized a new intermediate ‘wide-mouth’ scale-eating ecomorph in the sympatric radiation of Cyprinodon pupfishes on San Salvador Island. Additionally, I leveraged this ecomorph’s shared ancestry and shared novel ecological niche with scale-eater C. desquamator to explore the evolutionary origins of novelty and the genetic divergence that occurs during such major ecological transitions as generalist to scale-eater. Evolutionary novelty is a hallmark of adaptive radiation, yet we still don’t know how such novelties evolve on a microevolutionary scale. This intermediate ecomorph consumes scales in the wild but is genetically diverged from its sister scale-eating species and morphologically distinct from all the other species in the radiation. I used the timing of selective sweeps on shared and unique adaptive variants in the two scale-eating specialists to characterize the adaptive walk from generalist to scale-eater. Shared adaptive regions swept first in both the specialist C. desquamator and the intermediate ‘wide-mouth’ ecomorph, followed by unique sweeps of introgressed variation in ‘wide-mouth’ and de novo variation in C. desquamator. Selection on the same adaptive alleles may have allowed both scale-eating species access to the same area of the fitness landscape but epistatic interactions with private mutations and introgressed variation in each lineage may have resulted in divergent paths to scale-eating, ultimately contributing to diverse evolutionary outcomes even from a shared starting point.

Advisor: Martin, Christopher H