CAREER: Cryptic origins of evolutionary novelty in Caribbean pupfishes: genomic, functional, and ecological conditions for crossing fitness valleys and colonizing adaptive peaks

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One of the most fascinating features of the natural world is the evolution of novelty, when existing structures take on new functions or new ecological roles. Think of the narwhal's tooth, the anglerfish's lure, or the lightning beetle's glowing abdomen. Novelty underlies major transitions in the history of life, including moving from sea to land and the origins of unique mammalian traits such as fur and lactation. However, this process is challenging to study because novel transitions are not often observed at their earliest stages. Missing the early stages means missing out on the opportunity for experimental studies. This research will use a rapidly evolving group of fish to study novel transitions. Since these fish exhibit novel skeletal structures, prey capture behaviors, and ecological niches, they are well-suited for such studies. This project will produce fundamental knowledge of how genes control facial structures and behavior; this knowledge will be useful in understanding variation in all vertebrates, including humans. In addition, a public database for managing endangered species in captivity will be created. New, research-immersive courses will be developed. These courses will provide valuable training in statistical programming and data analysis for undergraduates.This research spans genotype to ecosystem to address a fundamental question: how does novelty originate from the intersection of ecology, natural selection, performance, and genetics? Answering this question is key to understanding how microevolutionary processes promote macroevolutionary patterns of novelty across the tree of life. Conventional understanding suggests novelty arises from resource abundance in new environments. More recent laboratory studies suggest complex dynamics lead to the evolution of novelty. This project will help bridge the gap between these two fields. To do so, the research will experimentally investigate novel transitions to scale-eating and snail-eating. Both feeding modes originated from an ancestral diet of algae in Caribbean pupfishes. The researchers will employ: 1) field and laboratory experiments measuring selection on hybrid phenotypes across environments; 2) ecosystem-scale measurements of productivity; 3) functional studies of hybrid performance; and 4) quantitative genetic and genomic analyses of the genetic basis of adaptive traits and source of adaptive variation. Hybrid crosses among pupfish species will be reared in the lab. Their fitness will be measured within field enclosures in hypersaline lakes on San Salvador Island and neighboring Bahamian islands. Lake respiration and macroalgae biomass will be measured across these lakes to assess resource abundance. The age and origin of genetic variation associated with adaptive trophic morphology will be investigated using whole-genome resequencing, genetic crosses, association mapping, and introgression analysis.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.