Investigating Patterns and Processes of Diversification in the Adaptive Radiation of Antarctic Notothenioid Fishes
Date of Award
Fall 2023
Document Type
Dissertation
Degree Name
Doctor of Philosophy (PhD)
Department
Ecology and Evolutionary Biology
First Advisor
Near, Thomas
Abstract
The Antarctic continental shelf, isolated from all other marine habitats by vast geographic distances, a deep circumpolar current, and subzero water temperatures, offers some of the most remote and extreme habitats on earth. Far from representing a frozen wasteland, however, the region has experienced periodic cycles of warming and cooling that have profoundly shaped the physical environment and biodiversity of the Southern Ocean during the last 40 million years. Specifically, the onset of rapid global cooling at the Eocene-Oligocene boundary saw the replacement of a cosmopolitan temperate ichthyofauna by a single endemic clade of teleost fishes – the Antarctic notothenioids. Fortified by antifreeze proteins enabling them to withstand the extreme cold of the Southern Ocean, the notothenioids were able to diversify into a wide range of ecological niches in the absence of competition from other marine fish lineages. Subsequent cycles of global warming and cooling are hypothesized to have driven ensuing pulses of lineage diversification in the notothenioids, with cycles of glacial advance and retreat promoting recurrent generation of ecological opportunities for diversification. However, our understanding of the impacts of ancient climate change on the evolutionary diversification of notothenioids is still quite limited. For instance, the lack of a detailed comparative phylogeographic study of notothenioid fishes at a continental geographic scale precludes a deeper understanding of how climatic and oceanographic factors have influenced patterns of population structure and connectivity for circum-Antarctic notothenioid species. Additionally, it remains unclear how existing patterns of phenotypic and ecological trait disparity within notothenioid subclades have been shaped by repeated onsets of ecological opportunity. This dissertation bridges the disciplines of microevolution and macroevolution to investigate how the paleoclimatic history of Antarctica has shaped dynamics of notothenioid diversification. A critical first step toward understanding how diversity has been generated and maintained in the Antarctic notothenioids involves the construction of a strongly-supported phylogenetic framework for the group. In Chapter 1, I review the current state of affairs with regard to notothenioid phylogenetics and taxonomy, focusing on how advances in molecular phylogenetic approaches have dramatically altered our understanding of notothenioid systematics in the 21st century. I then integrate molecular and morphological data to delimit species and infer phylogenetic relationships within the Antarctic barbeled plunderfishes (Artedidraconidae), a notothenioid lineage that is considered to harbor considerable taxonomic and phylogenetic uncertainty. Chapter 2 of my dissertation integrated phylogenomic, population genetic, and coalescent-based analyses of genomic-scale DNA sequence data with an investigation of phenotypic variation to delimit species boundaries within the artedidraconid subclade Pogonophryne. These analyses provided evidence to support a dramatic reduction of recognized species diversity from 29 to 5 valid species as well as identifying genetic and phenotypic evidence for a putatively new Pogonophryne species. In Chapter 3, genomic and phenotypic data were integrated to infer the phylogenetic relationships among all species of plunderfishes and to propose a taxonomic classification for the group that reflects the inferred phylogenetic relationships. Collectively, these three chapters highlight the utility of an integrative approach to taxonomy and yield phylogenetic information that is crucial for future investigations of the factors promoting diversification within notothenioids. The objective of Chapter 4 was to evaluate the factors modulating patterns of population genetic structure and connectivity across multiple widespread notothenioid species, which may shed light on the mechanisms contributing to speciation in this marine adaptive radiation. I leveraged genome-wide DNA sequence data to compare population genetic structure across four widespread notothenioid species that differ in their ecologies and life history strategies. Molecular population genetic analyses reveal contrasting patterns of population structure among our focal notothenioids, ranging from virtual panmixia to strong geographic structure across geographically-distant regions of the Antarctic continental shelf. I then used a predictive phylogeographic approach to evaluate whether contrasting phylogeographic patterns could be predicted by a series of life history traits collected for each focal notothenioid species. This approach identified body size, fecundity, and egg size as the most important variables in predicting patterns of genetic structure across notothenioids, thereby illustrating the utility of integrating organismal trait data into traditional comparative phylogeographic frameworks. Finally, Chapter 5 of my dissertation was motivated to understand the factors that promote ecomorphological differentiation in the Antarctic notothenioids. I integrated data on phylogeny, body shape and size, diet, and habitat usage to examine patterns of phenotypic and ecological diversification within two notothenioid subclades that have been identified as nested evolutionary radiations: the icefishes (Channichthyidae) and the notoperches (Trematominae). Within both subclades, I find evidence of high trait divergence between closely-related species and multiple instances of trait convergence among distantly-related species, suggesting repeated diversification of lineages into overlapping regions of trait space. These patterns are consistent with a scenario in which periodic glacial disturbances provided repeated bouts of ecological opportunities for diversification over the course of the notothenioid adaptive radiation.
Recommended Citation
Parker, Chantal Elyse, "Investigating Patterns and Processes of Diversification in the Adaptive Radiation of Antarctic Notothenioid Fishes" (2023). Yale Graduate School of Arts and Sciences Dissertations. 1144.
https://elischolar.library.yale.edu/gsas_dissertations/1144