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Population Genomics of Holacanthus Angelfishes in the Tropical Eastern Pacific

  • Author(s): Gatins, Remy
  • Advisor(s): Bernardi, Giacomo
  • et al.
Abstract

Connectivity refers to the amount of gene flow present between populations of the same species. The transfer of genetic material between populations allows species to increase their genetic diversity, thus allowing advantageous mutations to spread. When gene flow between populations becomes restricted, each population may evolve independently, diverging into what could eventually become two different species. In reef fishes, speciation events such as these are common particularly in peripheral populations that disperse to remote islands. Species that occupy small geographic ranges (e.g., endemics) tend to have low genetic diversity, thus being more vulnerable to strong environmental changes. A region where connectivity has been relatively understudied is the Tropical Eastern Pacific (TEP), which exhibits high level of endemism of shore fishes and is biogeographically isolated from other provinces. Despite having had multiple speciation events of marine organisms in the TEP, most connectivity studies of this region show high gene flow across long distances. However, the majority of these studies rely on single mitochondrial DNA markers. In this study I use Restriction Site Associated DNA sequencing (RADseq) to obtain 1000s of loci per individual to compare intra- and inter-specific populations of Holacanthus angelfishes in the TEP. For my first chapter, I assembled the whole genome of Holacanthus passer using a combination of high coverage long- (Oxford Nanopore) and short-read (Illumina) technology to further our understanding of the evolutionary history of H. passer. The draft genome resulted in a final assembly of 583 Mb contained in 476 contigs with a contig N50 length of 5.7 Mb. The genome contained 97.5% complete conserved actinopterygian orthologs, making it comparable, if not superior, to many chromosome-level genome assemblies of fishes. Using whole-genome sequence information, the demographic history of H. passer indicates a population expansion in the TEP preceded the last glacial maximum, as supported by other studies. For my second chapter, I used RADseq markers to detect genetic breaks and genetic diversity hotspots for intra-specific populations of H. passer across the TEP. I obtained a total of 19,809 polymorphic loci that revealed high gene flow along the TEP coastline (FST = 0.00) as predicted by the literature. However, pairwise differentiation detected weak but significant structure between Panama and the Sea of Cortez (0.002 < FST < 0.005; 0.007 < p < 0.043), driven principally by isolation by distance. Interestingly, we detected a temporal discord between individuals collected in Panama 10 years apart and did not show this same genetic signal. In addition, we detected 28 outlier loci that revealed subtle genetic signatures that differentiated populations from the mainland and oceanic islands. My third chapter took a broader approach to assess the inter-specific genomic signatures of Holacanthus angelfishes in the TEP. H. passer is mainly found on the mainland in the TEP, while its sister species H. clarionensis is endemic to the Revillagigedo Archipelago, and H. limbaughi is endemic to Clipperton Island. RADseq markers detected three hybrid individuals between H. passer and H. clarionensis but none with the third sister species, H. limbaughi. Moreover, equal amounts of ancestral variation of H. passer among H. clarionensis individuals and the lack of F2 or back-cross hybrids suggests that hybrids are sterile and provides evidence of incomplete lineage sorting. Although H. limbaughi and H. clarionensis are presumed to have diverged around the same time from H. passer, H. limbaughi’s smaller effective population size may have led to a faster rate of lineage sorting. Overall, this study highlights the power of using genome-wide markers (e.g., RADseq) to deliver a higher resolution perspective on the population dynamics within the TEP while giving insight into the evolutionary mechanisms that drove divergence of Holacanthus species.

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