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Final Report Summary - FISHSPECIATIONGENOME (Fish Speciation and the Origin of Marine Biodiversity: A Comparative Genomics Approach)

Contact: Iria Fernandez-Silva (Dept. of Biochemistry, Genetics & Immunology, School of Biology, University of Vigo, Vigo 36310, Spain & California Academy of Sciences, 55 Music Concourse Drive, San Francisco, CA 94118, USA)
The FishSpeciationGenome Project seeks to address key evolutionary questions pertaining to the evolution of reef fishes. The mechanisms by which one species divides into two during the course of evolution are still unknown. The best understood mechanism is that by which two groups of individuals of the same species become geographically isolated and evolve independently until they accumulate enough differences to be considered different species. In terrestrial organisms this can happen when, for example, tectonic movements or sea level rises split a land mass in two. However, coral reef fishes and other marine organisms defy this view of speciation, because geographic barriers in the oceans are scarce and the initial life stages of these animals (eggs and larvae) can drift with oceanic currents over vast geographic areas. Yet, coral reefs are incredible diverse and harbor over 25% of all marine species.

The aim of the FishSpeciationGenome is to investigate the mechanisms of speciation by sequencing the genomes of a species complex of Pygmy Angelfishes (genus Centropyge). Species in this complex differ by color and have partially overlapping distribution ranges. Interestingly, where they overlap, they interbreed, defining two hybridization zones.
A first objective of our work was to investigate the role of hybridization in the evolution of coral reef fishes, as well as achieving a broader understanding of the evolutionary consequences of hybridization in the wild. The recent discovery of two regions in the tropical Indo-Pacific with high prevalence of hybrid fishes highlight the need for a thorough examination of reticulate evolution in this group.
We also expect to obtain information on the genomic mechanisms that maintain species barriers (i.e. prevent that these species fuse back into one after secondary contact). Finally we are interested in the genetic processes by which color differences evolve in coral reef fishes, a trait for which nothing is virtually known in spite of the relevant role it plays in the diversification of this group.
Our work will not only help us understand key processes in evolution but is also relevant for the conservation of marine biodiversity and management of marine resources.

Work progress and results
We collected fish specimens and tissue samples of: 1) each of the three parental species in the areas where only one species occurs to represent the pure types (Sri Lanka, Philippines, Moorea); 2) each of the parental species in the hybrid zones (Micronesia, and Christmas Island, and Cocos Keeling); 3) each of the hybrid combinations in the hybrid zones displaying a range of color variants.
We optimized the laboratory protocol for DNA sequencing libraries, based on the double-digest RAD sequencing method and sequenced individuals representative of the diversity described above. We also optimized a bioinformatics pipeline for the estimation of the genotypic data (Single Nucleotide Polymorphisms), estimation of population allele frequencies, and analyses of genetic structure, patterns of hybridization and introgression, and selective sweeps.

We also completed a draft genome assembly for Centropyge vrolikii, one of the firsts for a perciform fish, which represents the most common order of fishes in coral reefs. This was used as a reference to analyze our RAD sequencing data. However, given the high contiguity of our assembly, it will also be of great value for future research in fish genomics or vertebrate evolution.

The population genomics analyses illuminated the complex evolutionary history of Centropyge angelfishes and reveal patterns of ancient genomic introgression, in this group, which highlight the importance of hybridization in coral reef fishes. Our research also sheds light into the evolutionary mechanisms of color variation in angelfishes and points to the high potential of this species complex to investigate the genes controlling color variation in fishes.

The conclusions of this work advance our understanding of the evolutionary consequences of range shifts and hybridization. This knowledge is relevant from a basic research perspective and also for the conservation of biodiversity and management of marine resources. Shifts in distributional ranges and secondary contact of previously isolated species will become more prevalent as a consequence of ocean warming, increased maritime transportation and aquaculture.

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