A genomics perspective on the evolution of Caribbean acroporid corals

Abstract

Reef-building corals globally face an increasing assortment of existential threats, ranging from disease outbreaks to intensifying climate change, resulting in wide-scale population declines. Until recently, our understanding of coral evolutionary genetics, as well as any potential to respond to such threats, was limited by available technologies. Next-Generation Sequencing (NGS) revolutionized the scale and capacity for whole genome and transcriptome analyses, particularly for non-model organisms such as corals, by producing exponentially more sequencing data at a fraction of the cost. My thesis focuses on using advances in NGS sequencing to expand the genomic resources available for Caribbean Acroporids. To explore the genetics of Caribbean Acropora corals, I first sequenced, de novo assembled, and annotated the genome of the Caribbean staghorn coral, Acropora cervicornis, and compared protein annotations to four other anthozoan genomes. Second, I leveraged the staghorn coral reference genome with double digest restriction-site associated DNA (ddRADseq) to explore genic speciation and evolutionary impact of one-way differential introgressive hybridization in the Caribbean between A. cervicornis, and its congener A. palmata. Lastly, with ddRADseq data from 161 A. cervicornis individuals collected across the Florida Reef Track (FRT), I examined the remaining population structure and genetic connectivity of coral populations managed as part of ongoing conservation efforts. In chapter one, I produce a well-annotated 400 Mb draft genome of A. cervicornis from an adult coral individual. The study of coral genetics is complicated by the particular life histories of these sessile organisms, which propagate mainly through asexual fragmentation and spawn sexually once a year, if they do so at all. Considered to be "holobionts", adult corals are comprised of not just coral tissue, but also symbiotic dinoflagellates called Symbiodiniaceae, which are difficult to physiologically separate prior to extracting DNA. Using a menthol-bleaching protocol before DNA extraction and sequencing, we were able to effectively separate, sequence, and assemble the staghorn coral genome de novo, and identify over 24,000 complete gene models. After functionally annotating the predicted proteins with SwissProt and KEGG annotations, we conducted comparative analysis between A. cervicornis and four other anthozoan genomes, including the Pacific congener A. digitifera. These data revealed unexpected differences between the Caribbean and Pacific Acroporids, such as extensive gene missingness in the genome of A. digitifera. Additionally, we identified potential genes within A. cervicornis related to the production of essential amino acids, such as cysteine-biosynthesis, which were not found in A. digitifera. In chapter two, I leverage the genomic resources created in chapter one, along with additional ddRADseq data to explore the genic speciation as well as the evolutionary impact of one-way differential introgressive hybridization within Caribbean Acropora. Compared to the hundreds of sympatric Acroporids found across Pacific reefs, the Caribbean Acroporid hybridization model offers relative simplicity with only two species of Acropora, the staghorn coral Acropora cervicornis, and the elkhorn coral Acropora palmata, which hybridize to form Acropora prolifera. Our data of 13,410 shared SNPs from 191 A. cervicornis and 29 A. palmata individuals revealed strong genetic differentiation with a global Fst of 0.25 and significantly less admixture than expected, indicating that these species are on distinct evolutionary trajectories. Admixture and clustering data demonstrate a disconnect between known mitochondrial (mtDNA) introgression histories and recent genomic signatures of introgression. Additionally, we identified 473 outlier loci spread evenly across the genome that demonstrate that there is strong and consistent selection against introgression in the Caribbean, suggesting hybridization is ecologically rare and many generations removed from these individuals. Lastly, admixture results unexpectedly detected bi-directional signatures of introgression or unsorted ancestral polymorphism, a pattern not seen in any previous work, nor our mtDNA data. For chapter three, I explore the population structure of staghorn corals across reefs from the Upper, Middle, and Lower Keys of the FRT. Over the last 30 years, White Band Disease (WBD) and other factors have crippled Caribbean Acropora populations, killing off over 90% of live coral cover. Given the ecological importance of these foundational species, as well as their slow recovery, conservation efforts have proliferated across the Caribbean with the goal of restoring staghorn corals. To ensure the long-term ecological resilience of populations restored from nursery-raised corals, conservation planning efforts face key challenges, such as maintaining sufficient levels of population genetic diversity as well as considering existing genetic structure, which can reveal sexual recruitment patterns as well as local adaptations. Our data of over 15K SNPs revealed three distinct genetic populations of A. cervicornis across the FRT, as well as high levels of standing genetic diversity. Importantly, the Upper Keys were dominated by one population, while the Lower Keys were dominated by a different genetic population, suggesting conservation should be locally focused. Interestingly, the third genetic population is comprised of recently backcrossed individuals confined to only a few reefs, suggesting that recently backcrossed individuals may give the appearance of fine-scale structure.