Function of a novel nasal protrusion for oral-shelling within an adaptive radiation of pupfishes

Abstract

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 mollusk from its shell and may be a way to subvert an otherwise insurmountable shell defense. 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 a durophagous pupfish (Cyprinodon brontotheroides). We first demonstrate oral shelling in this species and then predicted 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: 1) whether durophagous pupfish shell and consume more snails than other species, 2) if F1 and F2 durophagous hybrids consume similar amounts of snails as purebred durophagous pupfish, and 3) to determine if nasal protrusion size in parental and hybrid populations increases the maximum diameter snail consumed. 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 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. Significance StatementSpecialization on hard-shell prey items (i.e. durophagy) is a common dietary niche among fishes. Oral shelling is a rare technique used by some durophagous fish to consume prey items like snails; however, adaptations for oral shelling are still unknown. Here, we document the first evidence of oral shelling in a cyprinodontiform fish, the durophagous pupfish (Cyprinodon brontotheroides), and experimentally test whether its novel nasal protrusion is an adaptation for oral shelling using hybrid feeding trials.