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Biology subjects

St John, M. E.

Publications and source records attributed to St John, M. E..

4 recordsLinked to original sources

Multiple performance peaks for scale-biting in an adaptive radiation of pupfishes

The physical interactions between organisms and their environment ultimately shape their rate of speciation and adaptive radiation, but the contributions of biomechanics to evolutionary divergence are frequently overlooked. Here we investigated an adaptive radiation of Cyprinodon pupfishes to measure the relationship between feeding kinematics and performance during adaptation to a novel trophic niche, lepidophagy, in which a predator removes only the scales, mucus, and sometimes tissue from their prey using scraping and biting attacks. We used high-speed video to film scale-biting strikes on gelatin cubes by scale-eater, molluscivore, generalist, and hybrid pupfishes and subsequently measured the dimensions of each bite. We then trained the SLEAP machine-learning animal tracking model to measure kinematic landmarks and automatically scored over 100,000 frames from 227 recorded strikes. Scale-eaters exhibited increased peak gape and greater bite length; however, substantial within-individual kinematic variation resulted in poor discrimination of strikes by species or strike type. Nonetheless, a complex performance landscape with two distinct peaks best predicted gel-biting performance, corresponding to a significant nonlinear interaction between peak gape and peak jaw protrusion in which scale-eaters and their hybrids occupied a second performance peak requiring larger peak gape and greater jaw protrusion. A bite performance valley separating scale-eaters from other species may have contributed to their rapid evolution and is consistent with multiple estimates of a multi-peak fitness landscape in the wild. We thus present an efficient deep-learning automated pipeline for kinematic analyses of feeding strikes and a new biomechanical model for understanding the performance and rapid evolution of a rare trophic niche.

evolutionary biology↗

Parallel genetic changes underlie integrated craniofacial traits in an adaptive radiation of trophic specialist pupfishes

Many factors such as divergence time, shared standing genetic variation, frequency of introgression, and mutation rates can influence the likelihood of whether populations adapt to similar environments via parallel or non-parallel genetic changes. However, the frequency of parallel vs non-parallel genetic changes resulting in parallel phenotypic evolution is still unknown. In this study, we used a QTL mapping approach to investigate the genetic basis of highly divergent craniofacial traits between scale- and snail-eating trophic specialist species across similar hypersaline lake environments in an adaptive radiation of pupfishes endemic to San Salvador Island, Bahamas. We raised F2 intercrosses of scale- and snail-eaters from two different lake populations of sympatric specialists, estimated linkage maps, scanned for significant QTL for 30 skeletal and craniofacial traits, and compared the location of QTL between lakes to quantify parallel and non-parallel genetic changes. We found strong support for parallel genetic changes in both lakes for five traits in which we detected a significant QTL in at least one lake. However, many of these shared QTL affected different, but highly correlated craniofacial traits in each lake, suggesting that pleiotropy and trait integration should not be neglected when estimating rates of parallel evolution. We further observed a 23-52% increase in adaptive introgression within shared QTL, suggesting that introgression may be important for parallel evolution. Overall, our results suggest that the same genomic regions contribute to parallel integrated craniofacial phenotypes across lakes. We also highlight the need for more expansive searches for shared QTL when testing for parallel evolution.

evolutionary biology↗

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

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.

evolutionary biology↗

Major stages of vertebrate adaptive radiation are assembled from a disparate spatiotemporal landscape

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. Ancient standing variation from disparate spatial sources was reassembled into new combinations which are under strong selection for adaptation to novel trophic niches on only a single island throughout the Caribbean. This occurred in three stages: first, standing variation associated with feeding behavior swept, then standing variation regulating craniofacial development and pigmentation, and finally de novo variation for craniofacial development. Our results provide clear support for two longstanding hypotheses about adaptive radiation and demonstrate how ancient alleles maintained for millennia in distinct environmental refugia can be assembled into new adaptive combinations. One Sentence SummaryAncient origins of adaptive radiation

evolutionary biology↗