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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.

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Populations may adapt to similar environments via parallel or non-parallel genetic changes, but the frequency of these alternative mechanisms and underlying contributing factors are still poorly understood outside model systems. We used QTL mapping to investigate the genetic basis of highly divergent craniofacial traits between the scale-eater (Cyprinodon desquamator) and molluscivore (C. brontotheroides) pupfish adapting to two different hypersaline lake environments on San Salvador Island, Bahamas. We lab-reared F2 scale-eater x molluscivore intercrosses from two different lake populations, estimated linkage maps, scanned for significant QTL for 29 skeletal and craniofacial traits, female mate preference, and sex. We compared the location of QTL between lakes to quantify parallel and non-parallel genetic changes. We detected significant QTL for six craniofacial traits in at least one lake. However, nearly all shared QTL loci were associated with a different craniofacial trait within each lake. Therefore, our estimate of parallel evolution of craniofacial genetic architecture could range from one out of six identical trait QTL (low parallelism) to five out of six integrated trait QTL (high parallelism). We suggest that pleiotropy and trait integration can affect estimates of parallel evolution, particularly within rapid radiations. We also observed increased adaptive introgression in shared QTL regions, suggesting that gene flow contributed to parallel evolution. Overall, our results suggest that the same genomic regions may contribute to parallel adaptation across integrated suites of craniofacial traits, rather than specific traits, and highlight the need for a more expansive definition of parallel evolution.

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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.

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The effect of the environment on fitness in natural populations is a fundamental question in evolutionary biology. However, experimental manipulations of both environment and phenotype at the same time are rare. Thus, the relative importance of the competitive environment versus intrinsic organismal performance in shaping the location, height, and fluidity of fitness peaks and valleys remains largely unknown. Here, we experimentally tested the effect of competitor frequency on the complex fitness landscape driving adaptive radiation of a generalist and two trophic specialist pupfishes, a scale-eater and molluscivore, endemic to hypersaline lakes on San Salvador Island (SSI), Bahamas. We manipulated phenotypes, by generating 3407 F4/F5 lab-reared hybrids, and competitive environment, by altering the frequency of rare transgressive hybrids between field enclosures in two independent lake populations. We then tracked hybrid survival and growth rates across these four field enclosures for 3-11 months. In contrast to competitive speciation theory, we found no evidence that the frequency of hybrid phenotypes affected their survival. Instead, we observed a strikingly similar fitness landscape to a previous independent field experiment, each supporting multiple fitness peaks for generalist and molluscivore phenotypes and a large fitness valley isolating the divergent scale-eater phenotype. These features of the fitness landscape were stable across manipulated competitive environments, multivariate trait axes, and spatiotemporal heterogeneity. We suggest that absolute performance constraints and divergent gene regulatory networks shape macroevolutionary (interspecific) fitness landscapes in addition to microevolutionary (intraspecific) competitive dynamics. This interplay between organism and environment underlies static and dynamic features of the adaptive landscape.

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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.

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Behavioral changes in a new environment are often assumed to precede the origins of evolutionary novelties. Here, we examined whether an increase in aggression is associated with a novel scale-eating trophic niche within a recent radiation of Cyprinodon pupfishes endemic to San Salvador Island, Bahamas. We measured aggression using multiple behavioral assays and used transcriptomic analyses to identify differentially expressed genes in aggression and other behavioral pathways across 3 sympatric species in the San Salvador radiation (generalist, snail-eating specialist, and scale-eating specialist) and 2 generalist outgroups. Surprisingly, we found increased behavioral aggression and differential expression of aggression-related pathways in both the scale-eating and snail-eating specialists, despite their independent evolutionary origins. Increased behavioral aggression varied across both sex and stimulus context in both species. Our results indicate that aggression is not unique to scale-eating specialists. Instead, selection may increase aggression in other contexts such as niche specialization in general or mate competition. Alternatively, increased aggression may result from indirect selection on craniofacial traits, pigmentation, or metabolism-all traits which are highly divergent, exhibit signs of selective sweeps, and are affected by aggression-related genetic pathways which are differentially expressed in this system. In conclusion, the evolution of a novel predatory trophic niche within a recent adaptive radiation does not have clear-cut behavioral origins as previously assumed, highlighting the multivariate nature of adaptation and the complex integration of behavior with other phenotypic traits.

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Lepidophagy is comparatively rare amongst teleost fishes, yet our understanding of this specialization is lacking. Therefore we examined the digestive tract features of Pachypterus khavalchor using morphological, osteological, histological and histochemical techniques to comprehend and relate structural organization of digestive tract with scale eating habit. Morphologically, the alimentary canal is defined by a short and muscular esophagus, well-developed stomach and comparatively short intestine. Gut content analysis and intestinal coefficient value (0.53 ± 0.01) revealed that P. khavalchor exhibit both carnivory and lepidophagy. However, P. khavalchor primarily feeds on the scales (67.47%) and other chitin-rich material like aquatic insects (17.62%), aquatic larvae (8.66%) which affirms its solid association with chitinase producing endosymbionts in the gut. Lepidophagy is further supported by the osteological observations. The perfect segregation of the functions such as food capture, ingestion and processing amongst the different types of teeth located in the oral cavity and pharyngeal region thus could be taken as evolutionary adaptations in scale eaters to support lepidophagy. Specialized arrangement of the esophageal and stomach epithelial folds could be altogether taken as an adaptation with the end goal to frame the scale stacks and accordingly facilitate the handling and processing of chitin-rich bolus. The esophageal mucosa is simple squamous epithelium instead of stratified epithelium with numerous goblet cells to withstand the mechanical harm by hard-food stuff like scales. The cardiac and fundic regions exhibited large number tubular gastric glands with simple columnar epithelium. Surface cells of all three stomach regions stained positive for PAS staining. The intestine is without pyloric caeca and is divided into anterior and posterior region. Histologically it is characterized by simple columnar epithelium with brush border and numerous goblet cells throughout its length. Presence of large number microvilli on anterior and posterior intestine was noticeable. Intestinal goblet cells reacted positively to PAS, AB (pH 1) and AB (pH 2.5). Secretions of goblet cells are important for lubricating and protecting the epithelium. The results of present investigation improve the understanding of the digestive physiology of scale eaters in general and P. khavalchor in particular. Overall, our data indicates that though P. khavalchor predominantly feeds on scale, the digestive physiology is adapted to support dual feeding habit (lepidophagy and carnivory).

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Although rare within the context of 30 000 species of extant fishes, scale-feeding as an ecological strategy has evolved repeatedly across the teleost tree of life. Scale-feeding (lepidophagous) fishes are diverse in terms of their ecology, behaviour, and specialized morphologies for grazing on scales and mucus of sympatric species. Despite this diversity, the underlying ontogenetic changes in functional and biomechanical properties of associated feeding morphologies in lepidophagous fishes are less understood. We examined the ontogeny of feeding mechanics in two evolutionary lineages of scale-feeding fishes: Roeboides, a characin, and Catoprion, a piranha. We compare these two scale-feeding taxa with their nearest, non-lepidophagous taxa to identify traits held in common among scale-feeding fishes. We use a combination of micro-computed tomography scanning and iodine staining to measure biomechanical predictors of feeding behaviour such as tooth shape, jaw lever mechanics and jaw musculature. We recover a stark contrast between the feeding morphology of scale-feeding and non-scale-feeding taxa, with lepidophagous fishes displaying some paedomorphic characters through to adulthood. Few traits are shared between lepidophagous characins and piranhas, except for their highly-modified, stout dentition. Given such variability in development, morphology and behaviour, ecological diversity within lepidophagous fishes has been underestimated.

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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.

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Aggressive mimicry is an adaptive tactic of parasitic or predatory species that closely resemble inoffensive models in order to increase fitness via predatory gains. Although similarity of distantly related species is often intuitively implicated with mimicry, the exact mechanisms and evolutionary causes remain elusive in many cases. Here, we report a complex aggressive mimicry strategy in Plecodus straeleni, a scale-eating cichlid fish from Lake Tanganyika, which imitates two other cichlid species. Employing targeted sequencing on ingested scales, we show that P. straeleni does not preferentially parasitize its models but­contrary to prevailing assumptions­targets a variety of co-occurring dissimilar looking fish species. Combined with tests for visual resemblance and visual modelling from a prey perspective, our results suggest that complex interactions among different cichlid species are involved in this mimicry system.

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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.

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