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2024-05-10

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Perhaps one of the most apparent, yet captivating, natural phenomena is the diversity of shape and form which has evolved on Earth. Morphological evolution is shaped by numerous factors across multiple biological scales, yet there is still much to be discovered using novel techniques and integrative approaches. By combining insights from phylogenetic comparative methods, paleoclimatic models, geometric morphometrics, and comparative transcriptomics, my dissertation provides a multi-faceted approach to understanding the factors (ecological, environmental, and genetic) contributing to the evolution of body size and shape in two diverse groups of fishes. In Chapter 1, I use paleoclimate data in conjunction with a newly inferred phylogeny based on both extant and fossil species to examine how past ocean temperature is correlated with body size in tetraodontiform fishes (pufferfishes, boxfishes, ocean sunfishes, and allies). Numerous rules exist, which attempt to summarize the evolution of body size. These include Cope’s rule, which states lineages tend to increase in size over evolutionary time scales, and Bergmann’s rule which posits species tend to be larger in colder environments and smaller in warmer environments. These rules are generally well-supported in endotherms, but remain poorly understood in ectotherms. Using tetraodontiform fishes as a model clade, owing to their robust fossil record and disparity in body sizes, I find strong support for increasing body size over time in relation to decreasing oceanic temperatures. These results highlight the impact of paleoclimatic changes on aquatic ectotherms, which depend on their environment for temperature regulation and are potentially more susceptible to climatic changes compared with terrestrial vertebrates. In Chapter 2, I continue investigating morphological evolution of tetraodontiform fishes, a clade that is extremely well-suited for these types of questions due to their extraordinarily unique morphological diversity, including spines and spikes in porcupinefishes, box-like armor in boxfishes, and inflatable bodies in pufferfishes. Here, I utilize data from three-dimensional CT scans of both fossil and extant species to investigate widescale drivers of morphological evolution in relation to habitat and key innovations. Habitat transitions and evolutionary innovations have been previously linked to increases in morphological diversification, but it is unclear whether these are universal drivers. Using tetraodontiform fishes as a model system, I show that these general rules may be more nuanced than previously thought. Coral reefs have long been suggested to increase morphological diversification in fishes, however I find that species living in other habitats display higher rates of skull shape evolution, suggesting reef association alone is not sufficient to spur high evolutionary rates. Additionally, I investigate a morphological novelty—the tetraodontiform beak—which is a fusion of the teeth into a beaked mouth in several families. I find that beaked families exhibit higher rates of morphological evolution compared with non-beaked families, suggesting that the beak may be an evolutionary innovation facilitating their diversification. Lastly, in Chapter 3, I investigate morphological evolution through a genetic lens by employing comparative transcriptomics and differential expression analyses to identify candidate genes involved in miniaturization in gobiid fishes. While large body size is traditionally seen as advantageous, numerous transitions to miniaturization, the extreme reduction of adult body size, have evolved across the Tree of Life. Despite how common miniaturization appears, its genetic mechanisms are poorly understood. Miniaturization is especially common among fishes, with species in the family Gobiidae (gobies) being an exceptional case. Gobiid fishes are part of an ecological grouping called “cryptobenthic reef fishes” which are the poster child for small-bodied fishes. Even within the already small-bodied gobiid phylogeny, there are multiple, independent transitions to extreme small size, allowing for tests of genetic convergence within a comparative macroevolutionary framework. Here, I assemble the first de novo transcriptomes for six species of gobiid fishes, which represent three clades each containing a closely related large-bodied and small-bodied species. I identify sets of statistically significant orthologs which are differentially expressed between large-bodied and small-bodied species in each clade. From these, I identify several candidate genes potentially involved in miniaturization, including ybx1 and bzw2, both known to affect cell growth and development. These candidate genes offer insight into the genetic convergence on miniature body size and provide a framework for future studies. Overall, my dissertation provides new insights into the large-scale processes and dynamics which have shaped the evolution of morphological diversity in fishes. By combining data from both fossil and extant taxa, as well as analyzing the evolution of size and shape through both a morphological and genomic lens, we can appreciate the complexities and nuances of morphological evolution and gain a more complete picture of the evolutionary processes which shape life on our planet.

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evolution, morphology, fish

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