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1. Pharyngeal Jaws Converge by Similar Means, Not to Similar Ends, When Minnows (Cypriniformes: Leuciscidae) Adapt to New Dietary Niches

   https://doi.org/10.1093/icb/icz090  

   Pos, Kelsie M; Farina, Stacy C; Kolmann, Matthew A; Gidmark, Nicholas J (June 2019, Integrative and Comparative Biology)

   Abstract Convergent evolution is at the forefront of many form-function studies. There are many examples of multiple independent lineages evolving a similar morphology in response to similar functional demands, providing a framework for testing hypotheses of form-function evolution. However, there are numerous clades with underappreciated convergence, in which there is a perceived homogeneity in morphology. In these groups, it can be difficult to investigate causal relationships of form and function (e.g., diet influencing the evolution of jaw morphology) without the ability to disentangle phylogenetic signal from convergence. Leuciscids (Cypriniformes: Leuciscidae; formerly nested within Cyprinidae) are a species-rich clade of fishes that have diversified to occupy nearly every freshwater trophic niche, yet are considered to have relatively low morphological diversity relative to other large freshwater clades. Within the North American leuciscids, many genera contain at least one herbivore, insectivore, and larvaphage. We created 3D models from micro-computed tomography scans of 165 leuciscid species to measure functionally relevant traits within the pharyngeal jaws of these fishes. Using a published phylogeny, we tested these metrics for evolutionary integration, phylogenetic signal, and correlation with diet. Measurements of the pharyngeal jaws, muscle attachment areas, and teeth showed strong positive evolutionary correlation with each other and negative evolutionary correlation with measurements of the inter-ceratobranchial ligament (ICB ligament). Using diet data from published literature, we found extensive dietary convergence within Leuciscidae. The most common transitions we found were between herbivorous and invertivorous taxa and between insectivore types (aquatic vs. terrestrial). We document a trade-off in which herbivorous leuciscids have large teeth, short ICB ligaments, and large muscle attachment areas, whereas insectivorous leuciscids showed the opposite pattern. Inverse patterns of morphological integration between the ICB ligament the rest of the pharyngeal jaw correspond this dietary trade-off, which indicates that coordinated evolution of morphological traits contributes to functional diversity in this clade. However, these patterns only emerge in the context of phylogeny, meaning that the pharyngeal jaws of North American leuciscids converge by similar means (structural changes in response to dietary demands), but not necessarily to similar ends (absolute phenotype). 

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2. Do Coral Reefs Promote Morphological Diversification? Exploration of Habitat Effects on Labrid Pharyngeal Jaw Evolution in the Era of Big Data

   https://doi.org/10.1093/icb/icz103  

   Evans, Kory M; Williams, Keiffer L; Westneat, Mark W (June 2019, Integrative and Comparative Biology)

   Abstract Coral reefs are complex marine habitats that have been hypothesized to facilitate functional specialization and increased rates of functional and morphological evolution. Wrasses (Labridae: Percomorpha) in particular, have diversified extensively in these coral reef environments and have evolved adaptations to further exploit reef-specific resources. Prior studies have found that reef-dwelling wrasses exhibit higher rates of functional evolution, leading to higher functional variation than in non-reef dwelling wrasses. Here, we examine this hypothesis in the lower pharyngeal tooth plate of 134 species of reef and non-reef-associated labrid fishes using high-resolution morphological data in the form of micro-computed tomography scans and employing three-dimensional geometric morphometrics to quantify shape differences. We find that reef-dwelling wrasses do not differ from non-reef-associated wrasses in morphological disparity or rates of shape evolution. However, we find that some reef-associated species (e.g., parrotfishes and tubelips) exhibit elevated rates of pharyngeal jaw shape evolution and have colonized unique regions of morphospace. These results suggest that while coral reef association may provide the opportunity for specialization and morphological diversification, species must still be able to capitalize on the ecological opportunities to invade novel niche space, and that these novel invasions may prompt rapid rates of morphological evolution in the associated traits that allow them to capitalize on new resources. 

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3. Functional coupling in the evolution of suction feeding and gill ventilation of sculpins (Perciformes: Cottoidei)

   https://doi.org/10.1093/icb/icz022  

   Farina, S. C.; Knope, M. L.; Corn, K. A.; Summers, A. P.; Bemis, W. E. (April 2019, Integrative and Comparative Biology)

   Abstract Suction feeding and gill ventilation in teleosts are functionally coupled, meaning that there is an overlap in the structures involved with both functions. Functional coupling is one type of morphological integration, a term that broadly refers to any covariation, correlation, or coordination among structures. Suction feeding and gill ventilation exhibit other types of morphological integration, including functional coordination (a tendency of structures to work together to perform a function) and evolutionary integration (a tendency of structures to covary in size or shape across evolutionary history). Functional coupling, functional coordination, and evolutionary integration have each been proposed to limit morphological diversification to some extent. Yet teleosts show extraordinary cranial diversity, suggesting that there are mechanisms within some teleost clades that promote morphological diversification, even within the highly integrated suction feeding and gill ventilatory systems. To investigate this, we quantified evolutionary integration among four mechanical units associated with suction feeding and gill ventilation in a diverse clade of benthic, primarily suction-feeding fishes (Cottoidei; sculpins and relatives). We reconstructed cottoid phylogeny using molecular data from 108 species, and obtained 24 linear measurements of four mechanical units (jaws, hyoid, opercular bones, and branchiostegal rays) from micro-CT reconstructions of 44 cottoids and 1 outgroup taxon. We tested for evolutionary correlation and covariation among the four mechanical units using phylogenetically corrected principal component analysis to reduce the dimensionality of measurements for each unit, followed by correlating phylogenetically independent contrasts and computing phylogenetic generalized least squares models from the first principle component axis of each of the four mechanical units. The jaws, opercular bones, and branchiostegal rays show evolutionary integration, but the hyoid is not positively integrated with these units. To examine these results in an ecomorphological context, we used published ecological data in phylogenetic ANOVA models to demonstrate that the jaw is larger in fishes that eat elusive or grasping prey (e.g., prey that can easily escape or cling to the substrate) and that the hyoid is smaller in intertidal and hypoxia-tolerant sculpins. Within Cottoidei, the relatively independent evolution of the hyoid likely has reduced limitations on morphological evolution within the highly morphologically integrated suction feeding and gill ventilatory systems. 

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4. Epigenetics and the evolution of form: Experimental manipulation of a chromatin modification causes species‐specific changes to the craniofacial skeleton

   https://doi.org/10.1111/ede.12461  

   DeLorenzo, Leah; Powder, Kara E. (October 2023, Evolution & Development)

   Abstract A central question in biology is the molecular origins of phenotypic diversity. While genetic changes are key to the genotype–phenotype relationship, alterations to chromatin structure and the physical packaging of histone proteins may also be important drivers of vertebrate divergence. We investigate the impact of such an epigenetic mechanism, histone acetylation, within a textbook example of an adaptive radiation. Cichlids of Lake Malawi have adapted diverse craniofacial structures, and here we investigate how histone acetylation influences morphological variation in these fishes. Specifically, we assessed the effect of inhibiting histone deacetylation using the drug trichostatin A (TSA) on developing facial structures. We examined this during three critical developmental windows in two cichlid species with alternate adult morphologies. Exposure to TSA during neural crest cell (NCC) migration and as postmigratory NCCs proliferate in the pharyngeal arches resulted in significant changes in lateral and ventral shape inMaylandia, but not inTropheops. This included an overall shortening of the head, widening of the lower jaw, and steeper craniofacial profile, all of which are paedomorphic morphologies. In contrast, treatment with TSA during early chondrogenesis did not result in significant morphological changes in either species. Together, these data suggest a sensitivity to epigenetic alterations that are both time‐ and species‐dependent. We find that morphologies are due to nonautonomous or potentially indirect effects on NCC development, including in part a global developmental delay. Our research bolsters the understanding that proper histone acetylation is essential for early craniofacial development and identifies a species‐specific robustness to developmental change. Overall, this study demonstrates how epigenetic regulation may play an important role in both generating and buffering morphological variation. 

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5. Many ways to build an angler: diversity of feeding morphologies in a deep-sea evolutionary radiation

   https://doi.org/10.1098/rsbl.2023.0049  

   Heiple, Zach; Huie, Jonathan M.; Medeiros, Aline P.; Hart, Pamela B.; Goatley, Christopher H.; Arcila, Dahiana; Miller, Elizabeth Christina (June 2023, Biology Letters)

   Almost nothing is known about the diets of bathypelagic fishes, but functional morphology can provide useful tools to infer ecology. Here we quantify variation in jaw and tooth morphologies across anglerfishes (Lophiiformes), a clade spanning shallow and deep-sea habitats. Deep-sea ceratioid anglerfishes are considered dietary generalists due to the necessity of opportunistic feeding in the food-limited bathypelagic zone. We found unexpected diversity in the trophic morphologies of ceratioid anglerfishes. Ceratioid jaws span a functional continuum ranging from species with numerous stout teeth, a relatively slow but forceful bite, and high jaw protrusibility at one end (characteristics shared with benthic anglerfishes) to species with long fang-like teeth, a fast but weak bite and low jaw protrusibility at the other end (including a unique ‘wolftrap’ phenotype). Our finding of high morphological diversity seems to be at odds with ecological generality, reminiscent of Liem's paradox (morphological specialization allowing organisms to have broader niches). Another possible explanation is that diverse ceratioid functional morphologies may yield similar trophic success (many-to-one mapping of morphology to diet), allowing diversity to arise through neutral evolutionary processes. Our results highlight that there are many ways to be a successful predator in the deep sea. 

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