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The goal of this study is to identify novel differentially expressed genes contributing to the divergent craniofacial morphologies observed in larval San Salvador Island's pupfishes at hatching. We perform comparative transcriptomic analyses between specialized pupfish populations endemic to San Salvador Island and closely related outgroup pupfish species from North America. The San Salvador Island pupfishes exhibit remarkable trophic specialization and rapid craniofacial evolution, positioning them as ideal models for uncovering genetic mechanisms underlying craniofacial developmental variation relevant to human clinical phenotypes. 

Adaptive radiations offer an excellent opportunity to understand the eco-evolutionary dynamics of gut microbiota and host niche specialization. In a laboratory common garden, we compared the gut microbiota of two novel trophic specialists, a scale-eater and a molluscivore (which evolved from ancestral generalists), to a set of four outgroup generalist populations. We predicted an adaptive and highly divergent microbiome composition in the specialists matching their rapid rates of craniofacial diversification in the past 10 kya. We sequenced 16S rRNA amplicons of gut microbiomes from lab-reared fish fed the same high protein diet for one month. In contrast to our predictions, gut microbiota largely reflected 5 Mya phylogenetic divergence times among generalist populations in support of phylosymbiosis. However, we did find significant enrichment of Burkholderiaceae bacteria in both lab-reared scale-eater populations. These bacteria sometimes digest collagen, the major component of fish scales, supporting an adaptive shift. We also found some enrichment of Rhodobacteraceae and Planctomycetacia in lab-reared molluscivore populations, but these bacteria target cellulose. Minor shifts in gut microbiota appear adaptive for scale-eating in this radiation, whereas overall microbiome composition was phylogenetically conserved. This contrasts with predictions of adaptive radiation theory and observations of rapid diversification in all other trophic traits in these hosts, including craniofacial morphology, foraging behavior, aggression, and gene expression, suggesting that microbiome divergence proceeds as a nonadaptive radiation. 

Raw sequence reads of hybrids generated between Cyprinodon variegatus x C. brontotheroides x C. desquamator from Martin & Wainwright 2013, and Martin & Gould 2020. Sequences used in Patton et al., 2022, eLife. doi: https://doi.org/10.1101/2021.07.01.450666 

To investigate the origins and stages of vertebrate adaptive radiation, we reconstructed the spatial and temporal histories of genetic variants underlying major phenotypic axes of diversification from the genomes of 202 Caribbean pupfishes. On a single Bahamian island, ancient standing variation from disparate geographic sources was reassembled into new combinations under strong directional selection likely mediated by adaptation to novel trophic niches. 

Adaptive radiations involve astounding bursts of phenotypic, ecological, and species diversity. However, the microevolutionary processes that underlie the origins of these bursts are still poorly understood. We report the discovery of an intermediate wide-mouth scale-eating ecomorph in a sympatric radiation of Cyprinodon pupfishes, illuminating the transition from a widespread algae-eating generalist to a novel microendemic scale-eating specialist. We first show that this ecomorph occurs in sympatry with generalist C. variegatus and scale-eating specialist C. desquamator on San Salvador Island, Bahamas, but is genetically differentiated, morphologically distinct, and often consumes scales. We then compared the timing of selective sweeps on shared and unique adaptive variants in trophic specialists to characterize their adaptive walk. Shared adaptive regions swept first in both the specialist desquamator and the intermediate wide-mouth ecomorph, followed by unique sweeps of introgressed variation in wide-mouth and de novo variation in desquamator. The two scale-eating populations additionally shared 9% of their hard selective sweeps with molluscivores C. brontotheroides, despite no single common ancestor among specialists. Our work provides a new microevolutionary framework for investigating how major ecological transitions occur and illustrates how both shared and unique genetic variation can provide a bridge for multiple species to access novel ecological niches. 

A de novo assembly of C. bronthotheroides reference genome used for understanding the temporal and spatial dynamics of genetic variation that contributes to a rare radiation of trophic specialist pupfish on San Salvador Island, Bahamas.