A multi-peak performance landscape for scale biting in an adaptive radiation of pupfishes.

The physical interactions between organisms and their environment ultimately shape diversification rates, but the contributions of biomechanics to evolutionary divergence are frequently overlooked. Here, we estimated a performance landscape for biting in an adaptive radiation of Cyprinodon pupfishes, including scale-biting and molluscivore specialists, and compared performance peaks with previous estimates of the fitness landscape in this system. We used high-speed video to film feeding strikes on gelatin cubes by scale eater, molluscivore, generalist and hybrid pupfishes and measured bite dimensions. We then measured five kinematic variables from 227 strikes using the SLEAP machine-learning model. We found a complex performance landscape with two distinct peaks best predicted gel-biting performance, corresponding to a significant non-linear interaction between peak gape and peak jaw protrusion. Only scale eaters and their hybrids were able to perform strikes within the highest performance peak, characterized by larger peak gapes and greater jaw protrusion. A performance valley separated this peak from a lower performance peak accessible to all species, characterized by smaller peak gapes and less jaw protrusion. However, most individuals exhibited substantial variation in strike kinematics and species could not be reliably distinguished by their strikes, indicating many-to-many mapping of morphology to performance. The two performance peaks observed in the lab were partially consistent with estimates of a two-peak fitness landscape measured in the wild, with the exception of the new performance peak for scale eaters. We thus reveal a new bimodal non-linear biomechanical model that connects morphology to performance to fitness in a sympatric radiation of trophic niche specialists.

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.

Building trophic specializations that result in substantial niche partitioning within a young adaptive radiation.

Dietary partitioning often accompanies the increased morphological diversity seen during adaptive radiations within aquatic systems. While such niche partitioning would be expected in older radiations, it is unclear how significant morphological divergence occurs within a shorter time period. Here we show how differential growth in key elements of the feeding mechanism can bring about pronounced functional differences among closely related species. An incredibly young adaptive radiation of three Cyprinodon species residing within hypersaline lakes in San Salvador Island, Bahamas, has recently been described. Characterized by distinct head shapes, gut content analyses revealed three discrete feeding modes in these species: basal detritivory as well as derived durophagy and lepidophagy (scale-feeding). We dissected, cleared and stained, and micro-CT scanned species to assess functionally relevant differences in craniofacial musculoskeletal elements. The widespread feeding mode previously described for cyprinodontiforms, in which the force of the bite may be secondary to the requisite dexterity needed to pick at food items, is modified within both the scale specialist and the durophagous species. While the scale specialist has greatly emphasized maxillary retraction, using it to overcome the poor mechanical advantage associated with scale-eating, the durophage has instead stabilized the maxilla. In all species the bulk of the adductor musculature is composed of AM A1. However, the combined masses of both adductor mandibulae (AM) A1 and A3 in the scale specialist were five times that of the other species, showing the importance of growth in functional divergence. The scale specialist combines plesiomorphic jaw mechanisms with both a hypertrophied AM A1 and a slightly modified maxillary anatomy (with substantial functional implications) to generate a bite that is both strong and allows a wide range of motion in the upper jaw, two attributes that normally tradeoff mechanically. Thus, a significant feeding innovation (scale-eating, rarely seen in fishes) may evolve based largely on allometric changes in ancestral structures. Alternatively, the durophage shows reduced growth with foreshortened jaws that are stabilized by an immobile maxilla. Overall, scale specialists showed the most divergent morphology, suggesting that selection for scale-biting might be stronger or act on a greater number of traits than selection for either detritivory or durophagy. The scale specialist has colonized an adaptive peak that few lineages have climbed. Thus, heterochronic changes in growth can quickly produce functionally relevant change among closely related species.

Mutilating predation in the Cheirodontinae Odontostilbe pequira (Characiformes: Characidae)

We observed individuals of Odontostilbe pequira, a small characid, approaching and biting individuals of larger-bodied fishes of other species. This observation was made in two clear water headwater streams of the Cuiabá basin, Paraguay River system, located in Nobres, Mato Grosso State, Brazil, which led us to investigate the behavioral interactions of these fish. We characterized behavioral interactions between species by direct underwater observations using snorkelling and video recordings. Additionally, we proceeded diet analyses of O. pequira, obtaining intestinal coefficient and the index of alimentary importance. During underwater observations we checked the relative frequency of attacks by O. pequira on larger fish species. Odontostilbe pequira attacked individually or in large groups, and the anostomid Leporinus friderici was the preferred target prey species, while Prochilodus lineatus was apparently avoided. Our study sustains that O. pequira is omnivorous, with a diet that varies seasonally. It feeds mainly on plants, but also on animal prey, including the scales of small fishes, and, possibly, the mucus and epidermis of larger fish species. We suggest the term "mutilating predation" to describe the latter relationship.

Observamos indivíduos de Odontostilbe pequira, um caracídeo pequeno, abordando e mordendo peixes maiores de outras espécies. Essa observação foi feita em dois riachos de cabeceira com águas cristalinas na bacia do rio Cuiabá, sistema do rio Paraguai, localizados em Nobres, Mato Grosso, Brasil, o que nos levou a investigar a interação comportamental desses peixes. Nós o fizemos através de observações subaquáticas diretas usando mergulho livre e vídeo. Adicionalmente, realizamos a análise da dieta de O. pequira, obtendo seu coeficiente intestinal e índice de importância alimentar. Nas observações subaquáticas avaliamos a frequência relativa dos ataques de O. pequira sobre peixes maiores. Odontostilbe pequira ataca individualmente ou em grupos grandes, o anostomídeo Leporinus friderici foi a presa preferida, enquanto Prochilodus lineatus foi evitado. Este estudo sustenta que O. pequira é um peixe onívoro cuja dieta varia sazonalmente. Ele come principalmente plantas, mas também presas animais, como escamas de peixes pequenos e, possivelmente, muco e epiderme de peixes maiores. Sugerimos o termo "predação mutilante" para descrever essa relação.