Date of Award

2024-08-01

Degree Name

Doctor of Philosophy

Department

Biological Sciences

Advisor(s)

Philip Lavretsky

Abstract

Speciation is not a discrete event but rather a gradual process that occurs along a continuum. Initially, populations remain genetically and reproductively connected, but they become reproductively isolated as the process of speciation progresses. Advances in DNA sequencing technology has helped our understanding of the processes that contribute to changes in the genetic composition of populations over the progression of speciation, also known as drivers of evolution (i.e. genetic drift, mutation, selection, and gene flow). Among them, hybridization, or the interbreeding between distinct lineages, is increasingly recognized as a natural process that can have significant consequences to the speciation process. In particular, the frequency and directionality of introgressive hybridization (i.e., gene flow) dictates the extent of its impact(s) on the evolutionary trajectories. Importantly, the proximate result from gene flow is also tied to the directionality and strength of natural selection, as well as intensity of genetic drift. Here, I test hypotheses surrounding early species divergence, including the influence of these different evolutionary mechanisms on the process. Using a whole-genome sequencing approach, I aim to understand the genetic and evolutionary consequences of natural and human-mediated gene flow in a recently radiated avian system, the Mallard Complex. Importantly, I use inferences made from my study system to also inform conservation practices. In Chapter 1, I focused on the genomic consequences of hybrid speciation by comparing the full genomes of a putative young homoploid hybrid species, the Hawaiian duck (Anas wyvilliana). I conducted full genome comparison of the Hawaiian duck to its parental species, the island endemic Laysan duck (Anas layanensis) and a mainland generalist mallard (Anas platyrhynchos). I found that the Hawaiian duckâ??s genome is indeed a mosaic of genetic ancestry from both parental taxa, with a predominant contribution from the Laysan duck. Although the extent of reproductive isolation from either parental species is still unknown, I found potential genes associated with reproductive barriers, particularly on the Z-sex chromosome, related to fertilization, male courtship, and embryo development. Overall, my results are consistent with the hypothesis that the Hawaiian duck evolved via hybrid speciation and shed light on genes potentially advantageous for the emergence and persistence of this nascent hybrid species in the Hawaiian Islands. In Chapter two, I continue to focus on the Hawaiian duck that is currently threatened by introgressive hybridization from domestic mallards, highlighting the pressing conservation concern of potential genomic extinction and loss of adaptiveness for native species because of the extensive introgression of non-native genes. To alleviate or reverse trends for such scenarios requires the direct integration of genomic data within a model framework for effective management. Towards this end, I developed the simRestore R program as a decision-making tool that integrates ecological and genomic information to simulate ancestry outcomes from optimized conservation strategies. The program optimizes supplementation and removal strategies across generations until a set native genetic threshold is reached within the studied population. Importantly, in addition to helping with initial decision-making, simulations can be updated with the outcomes of ongoing efforts, allowing for the adaptive management of populations. After demonstrating functionality, I apply and optimize among actionable management strategies for the endangered Hawaiian duck for which the current primary threat is genetic extinction through ongoing anthropogenic hybridization with feral mallards. Simulations demonstrate that supplemental and removal efforts can be strategically tailored to move the genetic ancestry of Hawaii's hybrid populations towards Hawaiian duck without completely starting over. Further, I discuss ecological parameter sensitivity, including which factors are most important to ensure genetic outcomes (i.e. number of offspring). Finally, to facilitate use, the program is also available online as a Shiny Web application. My third Chapter focuses on understanding the diverse signals present in the speciesâ?? genomes that reflect the interplay of genetic drift, selection, and gene flow during the speciation process. Although unraveling the adaptive histories of species often includes determining how directional selection uniquely acts across respective genomes, it is equally important to establish what, if any, parts remain under purifying selection for ancestral state(s). Yet, this is only possible in sufficiently divergent genomes, allowing for the identification of both genomic islands and evolutionary valleys. To this end, my research involves comparing the full genomes of 11 of 14 species within the Mallard Complex, which represent successful adaptive radiation and the speciation continuum, to understand how directional and purifying selection have shaped derived and ancestral states, respectively. First, phylogenetic and demographic analyses support the "out of Africa" hypothesis of the Mallard Complex, dating back between 1 and 2 million years, with recent divergences occurring in the last 500,000 years among North American species. Second, while genomic islands of differentiation were identified in 44 pairwise species comparisons representing early and moderate stages of divergence, genomic valleys of ancestral retention were observed in all comparisons representing all stages of divergence. Finally, surveying gene ontology (GO) terms revealed a striking pattern in which valleys of similarity are linked to fundamental organismal functions and survival, and which outnumber islands of differentiation associated with adaptation to environmental challenges. Overall, my findings underscore the importance of analyzing species representing the speciation continuum to identify regions under divergent and purifying selection and discern potential stochastic mirages because of genetic drift.

Finally, Chapter four examines the consequences of domestic introgression into the genomes of their wild counterparts using the Hawaiian duck, New Zealand grey duck (Anas superciliosa), North American mallard and their respectively domestic breeds as study system. Using whole-genome re-sequencing, I analyzed domestic and wild congeners, along with resulting hybrids representing different levels of admixture across these regions. Assessing genetic diversity, runs of homozygosity, and demographic parameters for each genome, I consistently found that wild genomes exhibited higher genetic diversity, lower runs of homozygosity, and reduced inbreeding coefficients compared to their domestic counterparts. Across ecoregions, the strongest statistical correlation between ancestry and summary statistics was observed in North America, where domestic game-farm mallards are regularly introduced and interact with wild populations. Conversely, in regions like New Zealand and Hawaii, where stocking efforts have declined or populations are small, I identified evidence of adaptive selection and genetic drift as dominant forces shaping genomes. Furthermore, I illustrated how demographic history inferences using genomes derived from domestication or hybrid origins can be severely biased, leading to distorted estimates of effective population size (NE) and divergence times. Ultimately, I concluded that relying on highly inbred individuals to supplement populations of wild conspecifics not only exacerbates hybridization but might also intensify inbreeding, leading to important adaptive and conservation implications.

Overall, my dissertation investigates the intricate dynamics of speciation within the Mallard Complex, emphasizing the continuous nature of this evolutionary process. By recognizing speciation as a gradual continuum rather than discreet event(s), I have uncovered the multifaceted roles of natural selection, genetic drift, and gene flow in driving genetic divergence and ultimately species formation. Through meticulous genomic analyses and simulations, I have elucidated the genetic and evolutionary consequences of hybridization. Importantly, my work resulted in the development of a novel decision-making tool, simRestore, which integrates ecological and genomic data to inform conservation strategies for threatened species. Ultimately, this research underscores the importance of studying the dynamics of hybridization at both evolutionary and contemporary scales to advance our knowledge of speciation mechanisms and their implications for the conservation of Biodiversity.

Language

en

Provenance

Received from ProQuest

File Size

388 p.

File Format

application/pdf

Rights Holder

Flor Brigitte Hernandez Camacho

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