Evolutionary Inference from Admixed Genomes: Implications of Hybridization for Biodiversity Dynamics and Conservation

Hybridization as a macroevolutionary mechanism has been historically underappreciated among vertebrate biologists. Yet, the advent and subsequent proliferation of next-generation sequencing methods has increasingly shown hybridization to be a pervasive agent influencing evolution in many branches of the Tree of Life (to include ancestral hominids). Despite this, the dynamics of hybridization with regards to speciation and extinction remain poorly understood. To this end, I here examine the role of hybridization in the context of historical divergence and contemporary decline of several threatened and endangered North American taxa, with the goal to illuminate implications of hybridization for promoting—or impeding—population persistence in a shifting adaptive landscape. Chapter I employed population genomic approaches to examine potential effects of habitat modification on species boundary stability in co-occurring endemic fishes of the Colorado River basin (Gila robusta and G. cypha). Results showed how one potential outcome of hybridization might drive species decline: via a breakdown in selection against interspecific heterozygotes and subsequent genetic erosion of parental species. Chapter II explored long-term contributions of hybridization in an evolutionarily recent species complex (Gila) using a combination of phylogenomic and phylogeographic modelling approaches. Massively parallel computational methods were developed (and so deployed) to categorize sources of phylogenetic discordance as drivers of systematic bias among a panel of species tree inference algorithms. Contrary to past evidence, we found that hypotheses of hybrid origin (excluding one notable example) were instead explained by gene-tree discordance driven by a rapid radiation. Chapter III examined patterns of local ancestry in the endangered red wolf genome (Canis rufus) – a controversial taxon of a long-standing debate about the origin of the species. Analyses show how pervasive autosomal introgression served to mask signatures of prior isolation—in turn misleading analyses that led the species to be interpreted as of recent hybrid origin. Analyses also showed how recombination interacts with selection to create a non-random, structured genomic landscape of ancestries with, in the case of the red wolf, the ‘original’ species tree being retained only in low-recombination ‘refugia’ of the X chromosome. The final three chapters present bioinformatic software that I developed for my dissertation research to facilitate molecular approaches and analyses presented in Chapters I–III. Chapter IV details an in-silico method for optimizing similar genomic methods as used herein (RADseq of reduced representation libraries) for other non-model organisms. Chapter V describes a method for parsing genomic datasets for elements of interest, either as a filtering mechanism for downstream analysis, or as a precursor to targeted-enrichment reduced-representation genomic sequencing. Chapter VI presents a rapid algorithm for the definition of a ‘most parsimonious’ set of recombinational breakpoints in genomic datasets, as a method promoting local ancestry analyses as utilized in Chapter III. My three case studies and accompanying software promote three trajectories in modern hybridization research: How does hybridization impact short-term population persistence? How does hybridization drive macroevolutionary trends? and How do outcomes of hybridization vary in the genome? In so doing, my research promotes a deeper understanding of the role that hybridization has and will continue to play in governing the evolutionary fates of lineages at both contemporary and historic timescales

gila_ub_snps.tar

Data files containing an all-SNP alignment (in pyRAD .snps format), unlinked SNPs (=1 sampled per locus) in phylip format, and a filtered unlinked SNP alignment in phylip format. A filtered dataset of unlinked SNPs were used to run STRUCTURE and DAPC. See Methods for more details

Data from: Hybridization drives genetic erosion in sympatric desert fishes of western North America

Many species have evolved or currently coexist in sympatry due to differential adaptation in a heterogeneous environment. However, anthropogenic habitat modifications can either disrupt reproductive barriers or obscure environmental conditions which underlie fitness gradients. In this study, we evaluated the potential for an anthropogenically-mediated shift in reproductive boundaries that separate two historically sympatric fish species (Gila cypha and G. robusta) endemic to the Colorado River Basin using ddRAD sequencing of 368 individuals. We first examined the integrity of reproductive isolation while in sympatry and allopatry, then characterized hybrid ancestries using genealogical assignment tests. We tested for localized erosion of reproductive isolation by comparing site-wise genomic clines against global patterns and identified a breakdown in the drainage-wide pattern of selection against interspecific heterozygotes. This, in turn, allowed for the formation of a hybrid swarm in one tributary, and asymmetric introgression where species co-occur. We also detected a weak but significant relationship between genetic purity and degree of consumptive water removal, suggesting a role for anthropogenic habitat modifications in undermining species boundaries or expanding historically limited introgression. In addition, results from basin-wide genomic clines suggested that hybrids and parental forms are adaptively non-equivalent. If so, then a failure to manage for hybridization will exacerbate the long-term extinction risk in parental populations. These results reinforce the role of anthropogenic habitat modification in promoting interspecific introgression in sympatric species by relaxing divergent selection. This, in turn, underscores a broader role for hybridization in decreasing global biodiversity within rapidly deteriorating environments

gila_ub_introgress.tar.gz

Gzipped tar archive containing input files and R code for running genomic cline analyse

gila_ub_sra_metadata

Sample metadata for linking between NCBI SRA accession names (raw data) and sample names in datasets used for analyse

gila_ub.vcf.tar.gz

VCF file for running admixture. Analyses were completed using an open source pipeline by Steve Mussman, available at https://github.com/stevemussmann/admixturePipeline, which completes per-locus filtering (e.g. by coverage, minor allele freuency) internally using command-line options

gila_newhyb.tar.gz

Outputs and datafiles for running newhybrids and associated power analyses in the hybriddetective R packag

Taxonomic hypotheses and the biogeography of speciation in the Tiger Whiptail complex (Aspidoscelis tigris: Squamata, Teiidae)

Biodiversity in southwestern North America has a complex biogeographic history involving tectonism interspersed with climatic fluctuations. This yields a contemporary pattern replete with historic idiosyncrasies often difficult to interpret when viewed from through the lens of modern ecology. The Aspidoscelis tigris (Tiger Whiptail) complex (Squamata: Teiidae) is one such group in which taxonomic boundaries have been confounded by a series of complex biogeographic processes that have defined the evolution of the clade. To clarify this situation, we first generated multiple taxonomic hypotheses, which were subsequently tested using mitochondrial DNA sequences (ATPase 8 and 6) evaluated across 239 individuals representing five continental members of this complex. We then evaluated the manner by which our models parsed phylogenetic and biogeographic patterns. We found considerable variation among species ‘hypotheses,’ which we interpret as reflecting inflated levels of inter-population genetic divergence caused by historical demographic expansion and contraction cycles. Inter-specific boundaries with A. marmoratus juxtaposed topographically with the Cochise Filter Barrier that separates Sonoran and Chihuahuan deserts (interpreted herein as an example of ‘soft’ allopatry). Patterns of genetic divergence were consistent across the Cochise Filter Barrier, regardless of sample proximity. Surprisingly, this also held true for intraspecific comparisons that spanned the Colorado River. These in turn suggest geomorphic processes as a driver of speciation in the A. tigris complex, with intraspecific units governed by local demographic processes

Taxonomic hypotheses and the biogeography of speciation in the Tiger Whiptail complex (Aspidoscelis tigris: Squamata, Teiidae)

Biodiversity in southwestern North America has a complex biogeographic history involving tectonism interspersed with climatic fluctuations. This yields a contemporary pattern replete with historic idiosyncrasies often difficult to interpret when viewed from through the lens of modern ecology. The Aspidoscelis tigris (Tiger Whiptail) complex (Squamata: Teiidae) is one such group in which taxonomic boundaries have been confounded by a series of complex biogeographic processes that have defined the evolution of the clade. To clarify this situation, we first generated multiple taxonomic hypotheses, which were subsequently tested using mitochondrial DNA sequences (ATPase 8 and 6) evaluated across 239 individuals representing five continental members of this complex. We then evaluated the manner by which our models parsed phylogenetic and biogeographic patterns. We found considerable variation among species ‘hypotheses,’ which we interpret as reflecting inflated levels of inter-population genetic divergence caused by historical demographic expansion and contraction cycles. Inter-specific boundaries with A. marmoratus juxtaposed topographically with the Cochise Filter Barrier that separates Sonoran and Chihuahuan deserts (interpreted herein as an example of ‘soft’ allopatry). Patterns of genetic divergence were consistent across the Cochise Filter Barrier, regardless of sample proximity. Surprisingly, this also held true for intraspecific comparisons that spanned the Colorado River. These in turn suggest geomorphic processes as a driver of speciation in the A. tigris complex, with intraspecific units governed by local demographic processes

Microbial biogeography through the lens of exotic species: the recent introduction and spread of the freshwater diatom Discostella asterocostata in the United States

The large population sizes and high dispersal potential of microbes suggests that a given microbial species should be found in all suitable habitats worldwide. Consequently, microbes should not exhibit the kinds of biogeographic patterns seen in macroorganisms. This paradigm is challenged by a growing list of exotic microbes with biogeographic disjunctions that instead promotes microbial dispersal as inherently limited. We sampled water bodies in the United States and compiled records from the literature and public databases to characterize the distribution of the freshwater planktonic diatom, Discostella asterocostata (Xie, Lin, and Cai) Houk and Klee. Discostella asterocostata was thought to be restricted to the Far East, but we report its presence in ecologically similar water bodies across the eastern United States. Populations from the U.S. and China are indistinguishable morphometrically, suggesting they may be recently separated—a hypothesis supported by paleolimnological data, which support an introduction of D. asterocostata into the U.S. as recently as the mid-1980s. The overlapping distributions of D. asterocostata and invasive carp species, in both their native and nonnative ranges, highlighted Asian carp as a possible vector for introduction of the diatom in the U.S. The existence of exotic diatoms underscores natural constraints on microbial dispersal, resulting in biogeographic distributions that can be upended through human activity