Genomic Insights into Coral Evolution and Adaptation: A Comparative Study of Caribbean Reef-Builders
Restricted (Penn State Only)
- Author:
- Locatelli, Nicolas
- Graduate Program:
- Biology
- Degree:
- Doctor of Philosophy
- Document Type:
- Dissertation
- Date of Defense:
- June 11, 2024
- Committee Members:
- Elizabeth Mcgraw, Program Head/Chair
Zachary Szpiech, Major Field Member
Iliana B Baums, Special Member
Todd Lajeunesse, Chair of Committee
Emily Davenport, Major Field Member & Dissertation Advisor
Jason Keagy, Outside Unit & Field Member - Keywords:
- coral
evolution
genome
assembly
synteny
GWAS
polygenic
speciation
Acropora
Orbicella
Siderastrea
Dendrogyra
Colpophyllia
gene duplication
coalescent
heat stress - Abstract:
- Caribbean reefs became functionally isolated from other tropical seas to the east after the closure of the Mediterranean basin 12-16 million years ago and to the west with the closure of the Isthmus of Panama ~3 million years ago. Over these timescales, species in each region may have adapted to changing climates in potentially different ways. The widespread and rapid decline of reef communities in the Caribbean region as a result of disease and anthropogenic stressors has increased demands for genomic resources to design effective restoration measures that counter the loss of genetic diversity in the region. In the first and second chapters of this dissertation, I generated four reference genomes for major reef-building coral species in the Caribbean, Acropora cervicornis, Colpophyllia natans, Dendrogyra cylindrus, and Siderastrea siderea. Additionally, I constructed a linkage map for Acropora cervicornis and performed comparative analyses between A. cervicornis and its sister species, A. palmata, to understand the unique ways in which the Caribbean Acropora and the genus Acropora have adapted to changing conditions through time. In Acroporidae and Acropora, I found phylogenetically significant gene family expansions in gene ontology terms related to symbiont maintenance, cell-cell adhesion, and cell recognition. These results suggest that maintaining symbiont communities and concerted development or communication across the complex colony morphologies characteristic of the genus were important in its long-term evolutionary success. In the comparative analyses of C. natans, D. cylindrus, and S. siderea, I found that S. siderea has a genome roughly twice as large (822Mb) as other sequenced species of corals. Despite this, I found no evidence for the increase in genome size being driven by whole genome duplication. Instead, I found that this genome size expansion was largely driven by duplication mechanisms of all types (e.g. tandem and segmental duplications). These results support the hypothesis that gene duplications are a key driver of genome evolution in stony corals. In the third chapter of this dissertation, I explored the evolutionary processes that drive the speciation of corals. The Caribbean genus Orbicella has a complex evolutionary history with three extant lineages, O. faveolata, O. franksi, and O. annularis, and many extinct relatives. In support of previous studies, I found that the population genomic data generated here provides further support that O. faveolata and O. annularis genetically cluster based on geographic location. However, a novel result is that O. franksi consists of three cryptic, diverged lineages that do not assort based on sampling location. In these lineages, the most differentiated regions of the genome are associated with light sensing genes and sperm production and binding, providing support for the hypothesis that these cryptic lineages are diverging based on spawning time (light sensing genes) and gamete compatibility (sperm-related genes). Coalescent simulations and demographic analyses using the population genomic data revealed a history of bottlenecks and gene flow between the three species and a fourth extinct lineage (Oextinct), potentially the extinct congener, O. nancyi. Gene flow between the three species was highest following the onset of the Pleistocene, potentially driven by the rising and falling sea levels that compressed niche space and brought the species into contact with one another. Since the divergence of Oextinct 567,000 years ago, gene flow has been very low and has predominantly been unidirectional from Oextinct into O. franksi. Based on the results described above, the Caribbean Orbicella species are genetically well isolated at present despite their complex evolutionary history. Further work is required to understand the ecological significance and restoration implications of the divergent lineages within O. franksi. Reference panels are important tools for genetic management of species, yet none are currently available for corals. In the fourth and final chapter of this dissertation, I generated a population reference panel for A. palmata and evaluated imputation efficacy and accuracy in this non-model species. The panel allows for accurate imputation of sparse single nucleotide polymorphism data (SNP), such as those obtained from the Axiom™ Coral-Algae Genotyping Array. With accurately imputed data, I performed genome-wide association (GWA) analyses of phenotype data from a short-term acute heat stress experiment. In these experiments, ED50 and decline width (DW) trait values were measured. These phenotypes are associated with a 50% decline in photosynthetic capacity and the width of the photosynthetic decline curve, respectively. I found that these traits are highly polygenic and that genetics do play a large role in the heat stress response of corals. With identified loci, I calculated polygenic risk scores for each phenotype and generated bivariate risk scores for all 1,285 A. palmata samples previously genotyped on the Axiom™ Coral-Algae Genotyping Array. Polygenic risk scores for ED50 and DW were estimated with 538 and 229 single nucleotide polymorphisms, respectively, and had R2 values of 0.43 and 0.27 with their respective phenotype values. Using binary survival data from the 2023 Florida mass mortality and bleaching event, this research highlighted that surviving colonies exhibited higher ED50 and lower DW polygenic risk scores (both considered more thermally tolerant) than colonies that died during the event. These results suggest that these phenotypes and the associated polygenic risk scores have real life applicability to predicting heat resilience in A. palmata, although other factors such as disease resilience and symbiont genetics certainly play a key role in survival through long-term heat stress on wild reefs. Taken together, the chapters here increase the genomic resources available for the coral research community and for restoration practitioners. Further, these endeavors have bolstered our understanding of the evolutionary history of shallow, reef-building corals that characterize our modern reefs.