Phylogenomics of Acanthomorpha: From Ancient Radiations to the Tips of the Tree
Date of Award
Spring 2023
Document Type
Dissertation
Degree Name
Doctor of Philosophy (PhD)
Department
Ecology and Evolutionary Biology
First Advisor
Near, Thomas
Abstract
Systematics—the study of organisms, their distinctive traits, their diversification, and their relationships with other lineages through time—is foundational to the study of evolution and the preservation of biodiversity. Beginning at the end of the twentieth century, advancements in molecular biology revolutionized the field of systematics by revealing wholly unexpected, close relationships between morphologically dissimilar groups and unshrouding hidden diversity within more recently diverged lineages. Among the groups that were dramatically restructured by the application of molecular systematics is the teleost fish lineage that dominates the world’s modern oceans, Acanthomorpha (the spiny-rayed fishes). Spiny-rayed fishes represent one quarter of living vertebrates, are the basis of most commercial fisheries, and include several important model organisms for genomics, developmental biology, and behavior. In this work, I apply phylogenomic methods to investigate diversification within two of the world’s most inclusive vertebrate clades, Acanthomorpha and its major sublineage Perciformes. I delimit relationships across timescales, spanning the Mesozoic Era to the tips of the tree, and provide insight on lineages with complex taxonomic histories.
In chapter one, I combine phylogenomic and comparative data to establish the impact of the Cretaceous-Paleogene (K-Pg) mass extinction—the event that eliminated over three-quarters of all animal species—on the promotion of adaptive morphological diversification in Acanthomorpha. Many of the group’s major sublineages originated around the K-Pg boundary, which has led to the hypothesis that the diversity of spiny-rayed fishes is a result of exceptional diversification following the K-Pg mass extinction. However, this hypothesis remains untested and is based largely on patterns observed in other major vertebrate lineages (e.g., placental mammals and birds). This chapter challenges the prevailing paradigm that lineage diversification of spiny-rayed fishes after the K-Pg was explosive. Instead, lineage diversification in Acanthomorpha is constant after the K-Pg boundary but is decoupled from phenotypic diversification. While lineages steadily arose after the K-Pg, our evidence points to a prolonged period of morphological innovation that coincides with major ecological changes in marine and freshwater environments, illuminating aquatic diversification dynamics that had been lost to a 20-million-year gap in the fossil record.
In chapter two, I explore the relationships of Perciformes, the historic wastebasket taxon for percomorph fishes that underwent extensive systematic treatment prior to and following the advent of molecular sequencing. The now over 3,200 species of fishes classified in Perciformes are distributed among a handful of well-supported, inclusive lineages, such as Percoidei, Scorpaenoidei, Cottoidea, and Zoarcoidea. However, even in the phylogenomic era, discordance persists between molecular hypotheses for the interrelationships of many perciform families, especially for the clade’s earliest-diverging lineages and for the groups that historically served as nested catch-all taxa for perciform fishes (e.g., Serranidae, Stichaeidae, Cottidae). I build upon prior efforts to improve our understanding of perciform systematics by collecting and using ultraconserved element loci to infer the relationships of over 90% the recognized perciform families (or equivalents). As is becoming increasingly common, I supplement traditional measures of nodal support with maximum likelihood site and gene concordance factors. Because there is no well-defined standard towards the interpretation of these concordance factors, I closely examine the estimates for widely accepted branches to establish dataset-specific bounds for moderate or good branch support. I argue that this systematic approach should be taken for any phylogenomic study that uses maximum likelihood concordance factors to strongly inform its conclusions. Despite the unprecedented level of sampling for a study of perciform phylogenomics as well as concordance across methods, I do not infer a fully resolved, well-supported tree for all of Perciformes. Instead, using the careful examination of branch support and earlier phylogenetic inferences, I validate many earlier findings, particularly regarding family-level relationships in Notothenioidei, Percoidei, and much of Scorpaenoidei, as well as intrafamilial relationships throughout the tree. I also highlight the novel or rare inferences made possible by our inclusion of certain enigmatic taxa and note where in the perciform tree phylogenetic conflict persists.
Finally, in chapter three I provide an example of how systematics can inform species delimitation and thereby inform decisions around the conservation of biodiversity. This chapter concerns the perciform fish that was the center of the earliest public controversy over the United States Endangered Species Act of 1973 (ESA), the legislation that set a global precedent for the enactment of domestic species protection programs. In the late 1970s, this unassuming native of the Tennessee River system, the Snail Darter (Percina tanasi), became known across U.S. households as the little fish that stopped a big federal dam project. The Snail Darter garnered more recent media attention when it was federally delisted in October 2022 due to substantial recovery efforts, and its history is either cast as an example of environmentalist overreach or celebrated as a conservation biology success story. In this chapter, I highlight a long-overlooked and unresolved component of the Snail Darter controversy: the darter’s species status. Given its historic and political significance, the Snail Darter is among the most intensely studied of any non-game fish, but its species status has never been re-assessed since its description in 1976. Though once the face of the Endangered Species Act, this chapter demonstrates that the Snail Darter was never an endangered species because it was never a species. This work builds upon the standard approach to species description, which relies on the explicit comparison of a newly described species to a closely related taxon. This explicit comparison between two taxa usually exists within an implicit comparative framework, wherein the biologist describing a new species is tacitly guided by the level of differentiation previously used to draw boundaries between species in the same genus or family. This chapter presents an explicit comparative framework for species delimitation, wherein genomic and morphological data is used to compare the boundary drawn between the Snail Darter and its most closely related taxon to the boundaries drawn between twelve other pairs of darter sister species. I find overwhelming proof that the iconic Snail Darter is not a distinct species and the straightforward, data-driven approach to species delimitation I outline can help direct the focus of biologists, conservationists, politicians, and governmental agencies in the protection of other imperiled species.
Recommended Citation
Ghezelayagh, Ava, "Phylogenomics of Acanthomorpha: From Ancient Radiations to the Tips of the Tree" (2023). Yale Graduate School of Arts and Sciences Dissertations. 1365.
https://elischolar.library.yale.edu/gsas_dissertations/1365
