RESUMEN
To investigate the origins and stages of vertebrate adaptive radiation, we reconstructed the spatial and temporal histories of adaptive alleles underlying major phenotypic axes of diversification from the genomes of 202 Caribbean pupfishes. On a single Bahamian island, ancient standing variation from disjunct geographic sources was reassembled into new combinations under strong directional selection for adaptation to the novel trophic niches of scale-eating and molluscivory. We found evidence for two longstanding hypotheses of adaptive radiation: hybrid swarm origins and temporal stages of adaptation. Using a combination of population genomics, transcriptomics, and genome-wide association mapping, we demonstrate that this microendemic adaptive radiation of novel trophic specialists on San Salvador Island, Bahamas experienced twice as much adaptive introgression as generalist populations on neighboring islands and that adaptive divergence occurred in stages. First, standing regulatory variation in genes associated with feeding behavior (prlh, cfap20, and rmi1) were swept to fixation by selection, then standing regulatory variation in genes associated with craniofacial and muscular development (itga5, ext1, cyp26b1, and galr2) and finally the only de novo nonsynonymous substitution in an osteogenic transcription factor and oncogene (twist1) swept to fixation most recently. Our results demonstrate how ancient alleles maintained in distinct environmental refugia can be assembled into new adaptive combinations and provide a framework for reconstructing the spatiotemporal landscape of adaptation and speciation.
Asunto(s)
Adaptación Fisiológica/genética , Especiación Genética , Peces Killi/genética , Filogenia , Análisis Espacio-Temporal , Vertebrados/genética , Animales , Bahamas , Región del Caribe , Proteínas de Peces/genética , Perfilación de la Expresión Génica/métodos , Estudio de Asociación del Genoma Completo/métodos , Genómica/métodos , Genotipo , Geografía , Peces Killi/anatomía & histología , Peces Killi/clasificación , Polimorfismo de Nucleótido Simple , Vertebrados/anatomía & histología , Vertebrados/clasificaciónRESUMEN
Dietary specialization on hard prey items, such as mollusks and crustaceans, is commonly observed in a diverse array of fish species. Many fish consume these types of prey by crushing the shell to consume the soft tissue within, but a few fishes extricate the soft tissue without breaking the shell using a method known as oral shelling. Oral shelling involves pulling a mollusc from its shell and it may be a way to subvert an otherwise insurmountable shell defence. However, the biomechanical requirements and potential adaptations for oral shelling are unknown. Here, we test the hypothesis that a novel nasal protrusion is an adaptation for oral shelling in the durophagous pupfish (Cyprinodon brontotheroides). We first demonstrate oral shelling in this species and then predict that a larger nasal protrusion would allow pupfish to consume larger snails. Durophagous pupfish are found within an endemic radiation of pupfish on San Salvador Island, Bahamas. We took advantage of closely related sympatric species and outgroups to test: (a) whether durophagous pupfish shell and consume more snails than other species, (b) if F1 and F2 durophagous hybrids consume similar amounts of snails as purebred durophagous pupfish, and (c) if nasal protrusion size in parental and hybrid populations increases the maximum size of consumed snails. We found that durophagous pupfish and their hybrids consumed the most snails, but did not find a strong association between nasal protrusion size and maximum snail size consumed within the parental or F2 hybrid population, suggesting that the size of their novel nasal protrusion does not provide a major benefit in oral shelling. Instead, we suggest that the nasal protrusion may increase feeding efficiency, act as a sensory organ, or is a sexually selected trait, and that a strong feeding preference may be most important for oral shelling.
Asunto(s)
Adaptación Fisiológica , Distribución Animal , Conducta Alimentaria/fisiología , Peces Killi/anatomía & histología , Peces Killi/fisiología , Animales , Bahamas , SimpatríaRESUMEN
The origins of novel trophic specialization, in which organisms begin to exploit resources for the first time, may be explained by shifts in behavior such as foraging preferences or feeding kinematics. One way to investigate behavioral mechanisms underlying ecological novelty is by comparing prey capture kinematics among species. We investigated the contribution of kinematics to the origins of a novel ecological niche for scale-eating within a microendemic adaptive radiation of pupfishes on San Salvador Island, Bahamas. We compared prey capture kinematics across three species of pupfish while they consumed shrimp and scales in the lab, and found that scale-eating pupfish exhibited peak gape sizes twice as large as in other species, but also attacked prey with a more obtuse angle between their lower jaw and suspensorium. We then investigated how this variation in feeding kinematics could explain scale-biting performance by measuring bite size (surface area removed) from standardized gelatin cubes. We found that a combination of larger peak gape and more obtuse lower jaw and suspensorium angles resulted in approximately 40% more surface area removed per strike, indicating that scale-eaters may reside on a performance optimum for scale biting. To test whether feeding performance could contribute to reproductive isolation between species, we also measured F1 hybrids and found that their kinematics and performance more closely resembled generalists, suggesting that F1 hybrids may have low fitness in the scale-eating niche. Ultimately, our results suggest that the evolution of strike kinematics in this radiation is an adaptation to the novel niche of scale eating.