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In the past decade, advances in genome sequencing have allowed researchers to uncover the history of hybridization in diverse groups of species, including our own. Although the field has made impressive progress in documenting the extent of natural hybridization, both historical and recent, there are still many unanswered questions about its genetic and evolutionary consequences. Recent work has suggested that the outcomes of hybridization in the genome may be in part predictable, but many open questions about the nature of selection on hybrids and the biological variables that shape such selection have hampered progress in this area. We synthesize what is known about the mechanisms that drive changes in ancestry in the genome after hybridization, highlight major unresolved questions, and discuss their implications for the predictability of genome evolution after hybridization.

Poison frogs bioaccumulate alkaloids for chemical defense from their arthropod diet. Although many alkaloids are accumulated without modification, some poison frog species can metabolize pumiliotoxin (PTX 251D ) into the more potent allopumiliotoxin (aPTX 267A ). Despite extensive research characterizing the chemical arsenal of poison frogs, the physiological mechanisms involved in the sequestration and metabolism of individual alkaloids remain unclear. We first performed a feeding experiment with the Dyeing poison frog ( Dendrobates tinctorius ) to ask if this species can metabolize PTX 251D into aPTX 267A and what gene expression changes are associated with PTX 251D exposure in the intestines, liver, and skin. We found that D . tinctorius can metabolize PTX 251D into aPTX 267A , and that PTX 251D exposure changed the expression level of genes involved in immune system function and small molecule metabolism and transport. To better understand the functional significance of these changes in gene expression, we then conducted a series of high-throughput screens to determine the molecular targets of PTX 251D and identify potential proteins responsible for metabolism of PTX 251D into aPTX 267A . Although screens of PTX 251D binding human voltage-gated ion channels and G-protein coupled receptors were inconclusive, we identified human CYP2D6 as a rapid metabolizer of PTX 251D in a cytochrome P450 screen. Furthermore, a CYP2D6-like gene had increased expression in the intestines of animals fed PTX, suggesting this protein may be involved in PTX metabolism. These results show that individual alkaloids can modify gene expression across tissues, including genes involved in alkaloid metabolism. More broadly, this work suggests that specific alkaloid classes in wild diets may induce physiological changes for targeted accumulation and metabolism.

The evolution of reproductive barriers is the first step in the formation of new species and can help us understand the diversification of life on Earth. These reproductive barriers often take the form of hybrid incompatibilities, in which alleles derived from two different species no longer interact properly in hybrids 1 – 3 . Theory predicts that hybrid incompatibilities may be more likely to arise at rapidly evolving genes 4 – 6 and that incompatibilities involving multiple genes should be common 7 , 8 , but there has been sparse empirical data to evaluate these predictions. Here we describe a mitonuclear incompatibility involving three genes whose protein products are in physical contact within respiratory complex I of naturally hybridizing swordtail fish species. Individuals homozygous for mismatched protein combinations do not complete embryonic development or die as juveniles, whereas those heterozygous for the incompatibility have reduced complex I function and unbalanced representation of parental alleles in the mitochondrial proteome. We find that the effects of different genetic interactions on survival are non-additive, highlighting subtle complexity in the genetic architecture of hybrid incompatibilities. Finally, we document the evolutionary history of the genes involved, showing signals of accelerated evolution and evidence that an incompatibility has been transferred between species via hybridization. Analysis of naturally hybridizing swordtail fish species reveals a mitonuclear genetic incompatibility among three genes that encode components of mitochondrial respiratory complex I, providing insights into the emergence of hybrid incompatibilities and reproductive barriers.

Hybridization between species is widespread across the tree of life. As a result, many species, including our own, harbor regions of their genome derived from hybridization. Despite the recognition that this process is widespread, we understand little about how the genome stabilizes following hybridization, and whether the mechanisms driving this stabilization tend to be shared across species. Here, we dissect the drivers of variation in local ancestry across the genome in replicated hybridization events between two species pairs of swordtail fish: Xiphophorus birchmanni × X . cortezi and X . birchmanni × X . malinche . We find unexpectedly high levels of repeatability in local ancestry across the two types of hybrid populations. This repeatability is attributable in part to the fact that the recombination landscape and locations of functionally important elements play a major role in driving variation in local ancestry in both types of hybrid populations. Beyond these broad scale patterns, we identify dozens of regions of the genome where minor parent ancestry is unusually low or high across species pairs. Analysis of these regions points to shared sites under selection across species pairs, and in some cases, shared mechanisms of selection. We show that one such region is a previously unknown hybrid incompatibility that is shared across X . birchmanni × X . cortezi and X . birchmanni × X . malinche hybrid populations.

Over the past 2 decades, biologists have come to appreciate that hybridization, or genetic exchange between distinct lineages, is remarkably common—not just in particular lineages but in taxonomic groups across the tree of life. As a result, the genomes of many modern species harbor regions inherited from related species. This observation has raised fundamental questions about the degree to which the genomic outcomes of hybridization are repeatable and the degree to which natural selection drives such repeatability. However, a lack of appropriate systems to answer these questions has limited empirical progress in this area. Here, we leverage independently formed hybrid populations between the swordtail fish Xiphophorus birchmanni and X . cortezi to address this fundamental question. We find that local ancestry in one hybrid population is remarkably predictive of local ancestry in another, demographically independent hybrid population. Applying newly developed methods, we can attribute much of this repeatability to strong selection in the earliest generations after initial hybridization. We complement these analyses with time-series data that demonstrates that ancestry at regions under selection has remained stable over the past approximately 40 generations of evolution. Finally, we compare our results to the well-studied X . birchmanni × X . malinche hybrid populations and conclude that deeper evolutionary divergence has resulted in stronger selection and higher repeatability in patterns of local ancestry in hybrids between X . birchmanni and X . cortezi .

Xyloplax is a genus of three species of sea stars previously found only on sunken wood in the deep ocean. Their circular and petaloid bodies, which lend them their common name “sea daisy”, and their presumed exclusive diet of wood make them an unusual and rare element of deep-sea ecosystems. We describe here the fourth species of Xyloplax from the eastern Pacific Ocean, Xyloplax princealberti n. sp., which ranges from offshore Canada to the Gulf of California (Mexico) and Costa Rica. Though sampled geographically close to another described species of Xyloplax from the northeastern Pacific, X. janetae, this new species is unique morphologically and according to available DNA data. The short abactinal spines are the most obvious feature that distinguishes X. princealberti n. sp. from other Xyloplax. The minimum distance for mitochondrial cytochrome c oxidase subunit I from Xyloplax princealberti n. sp. to the only other available Xyloplax, X. janetae, was 13.5%. We also describe Ridgeia vestimentiferan tubeworm bushes from active hydrothermal vents as a new Xyloplax habitat, the first record of a non-wood substrate, and a new reproductive strategy, simultaneous hermaphroditism, for this genus. We generated the first mitochondrial genome for a member of Xyloplax and analyzed it with other available asteroid data using nucleotide-coding or amino acid (for protein-coding genes) plus nucleotide coding (for rRNA genes). The nucleotide-coding results place Xylopax as part of the clade Velatida, consistent with a previous phylogenomic analysis that included Xyloplax princealberti n. sp. (as Xyloplax sp.), though the placement of Velatida within Asteroidea differed. The amino acid plus nucleotide coding recovered Velatida to be a grade with X. princealberti n. sp. as sister group to all other Asteroidea.

Recent scientific advances in ex situ system design and operation make it possible to complete gametogenic cycles of broadcast spawning corals. Breeding corals in aquaria is a critical advance for population management, particularly genetic rescue and assisted gene flow efforts. Genetic rescue projects for corals are already underway to bring threatened species into ex situ culture and propagation, thereby preserving standing genetic variation. However, while breeding corals is increasingly feasible, the consequences of the aquarium environment on the genetic and phenotypic composition of coral populations is not yet known. The aquarium environment may in itself be a selective pressures on corals, but it also presents relaxed selective pressures in other respects. In 2019 and 2020, gravid Acropora hyacinthus coral colonies were collected from Palauan reefs and shipped to the California Academy of Sciences (CAS) in San Francisco. In both years, gametes were batch-fertilized to produce larvae that were then settled and reared to recruits. As of April 2021, when they were sampled for sequencing, 23 corals produced at CAS in 2019 and 16 corals produced at CAS in 2020 had survived for two years and one year, respectively. We sequenced the full genomes of the 39 offspring corals and their 15 potential parents to a median 26x depth of coverage. We find clear differential parentage, with some parents producing the vast majority of offspring, while the majority of parents produced no surviving offspring. After scanning 12.9 million single nucleotide polymorphisms (SNPs), we found 887 SNPs that may be under selection in the aquarium environment, and we identified the genes and pathways these SNPs may affect. We present recommendations for preserving standing genetic variation in aquarium-bred corals based on the results of this pilot project.

In this thesis, I explore the consequences of hybridization, or genetic exchange between species, with a focus on divergent traits that have evolved between species. I performed these studies leveraging a system where natural hybridization is ongoing between species that vary in their sexual displays and ecology: the swordtail fishes Xiphophorus malinche and X. birchmanni. In my first chapter, I provide an introduction to the genomic consequences of hybridization, highlighting open questions around predicting the effects of different and interacting selective forces on hybrid genomes. In my second chapter, I explore the genetic basis of a sexually-selected ornament, called the sword. In my third and fourth chapters, I focused on divergence between species in thermal tolerance and offspring size. These two traits can be viewed as models of evolved differences between these species in response to the environment and allow me to explore the interplay between ecological adaptations in species and their breakdown in hybrids.

For over a century, evolutionary biologists have been motivated to understand the mechanisms through which organisms adapt to their environments. Coloration and pigmentation are remarkably variable within and between species and can serve as an important window into the mechanisms of adaptation. Here, we map the genetic basis of a newly described iridescence trait in swordtail fish to a single locus. Individuals with this trait appear to sparkle as they move through the water. We find that the trait is driven by the recent endogenization of a retrovirus that inserted near the gene . This insertion is associated with changes in the chromatin landscape, upregulation of , and accumulation of iridescent cells that adhere to the scales. Rather than causing diseases, our results demonstrate that invading endogenous retroviruses can also regulate novel trait variation in the host. Moreover, we find that this coloration trait may act as an important signal in interactions between fish and their predators in the natural environment.