Evolutionary Genomic Responses in Antarctic Notothenioid Fishes
As plate tectonics pushed Antarctica into a polar position, by ~34 million years ago, the continent and its surrounding Southern Ocean (SO) became geographically and thermally isolated by the Antarctic Circumpolar Current. Terrestrial and marine glaciation followed, resulting in extinctions as well as the survival and radiation of unique flora and fauna. The notothenioid fish survived and arose from a common ancestral stock into tax with 120 species that dominates today's SO fish fauna. The Notothenioids evolved adaptive traits including novel antifreeze proteins for survival in extreme cold, but also suffered seemingly adverse trait loss including red blood cells in the icefish family, and the ability to mount cellular responses to mitigate heat stress ? otherwise ubiquitous across all life. This project aims to understand how the notothenoid genomes have changed and contributed to their evolution in the cold. The project will sequence, analyze and compare the genomes of two strategic pairs of notothenioid fishes representing both red-blooded and white-blooded species. Each pair will consist of one Antarctic species and one that has readapted to the temperate waters of S. America or New Zealand. The project will also compare the Antarctic species genomes to a genome of the closet non-Antarctic relative representing the temperate notothenioid ancestor. The work aims to uncover the mechanisms that enabled the adaptive evolution of this ecologically vital group of fish in the freezing Southern Ocean, and shed light on their adaptability to a warming world. The finished genomes will be made available to promote and advance Antarctic research and the project will host a symposium of Polar researchers to discuss the cutting edge developments regarding of genomic adaptations in the polar region.
Despite subzero, icy conditions that are perilous to teleost fish, the fish fauna of the isolated Southern Ocean (SO) surrounding Antarctica is remarkably bountiful. A single teleost group - the notothenioid fishes - dominate the fauna, comprising over 120 species that arose from a common ancestor. When Antarctica became isolated and SO temperatures began to plunge in early Oligocene, the prior temperate fishes became extinct. The ancestor of Antarctic notothenioids overcame forbidding polar conditions and, absent niche competition, it diversified and filled the SO. How did notothenioids adapt to freezing environmental selection pressures and achieve such extraordinary success? And having specialized to life in chronic cold for 30 myr, can they evolve in pace with today's warming climate to stay viable? Past studies of Antarctic notothenioid evolutionary adaptation have discovered various remarkable traits including the key, life-saving antifreeze proteins. But life specialized to cold also led to paradoxical trait changes such as the loss of the otherwise universal heat shock response, and of the O2-transporting hemoglobin and red blood cells in the icefish family. A few species interestingly regained abilities to live in temperate waters following the escape of their ancestor out of the freezing SO.
This proposed project is the first major effort to advance the field from single trait studies to understanding the full spectrum of genomic and genetic responses to climatic and environmental change during notothenioid evolution, and to evaluate their adaptability to continuing climate change. To this end, the project will sequence the genomes of four key species that embody genomic responses to different thermal selection regimes during notothenioids' evolutionary history, and by comparative analyses of genomic structure, architecture and content, deduce the responding changes. Specifically, the project will (i) obtain whole genome assemblies of the red-blooded T. borchgrevinki and the S. American icefish C. esox; (ii) using the finished genomes from (i) as template, obtain assemblies of the New Zealand notothenioid N. angustata, and the white-blooded icefish C. gunnari, representing a long (11 myr) and recent (1 myr) secondarily temperate evolutionary history respectively. Genes that are under selection in the temperate environment but not in the Antarctic environment can be inferred to be directly necessary for that environment and the reverse is also true for genes under selection in the Antarctic but not in the temperate environment. Further, genes important for survival in temperate waters will show parallel selection between N. angustata and C. esox despite the fact that the two fish left the Antarctic at far separated time points. Finally, gene families that expanded due to strong selection within the cold Antarctic should show a degradation of duplicates in the temperate environment. The project will test these hypotheses using a number of techniques to compare the content and form of genes, the structure of the chromosomes containing those genes, and through the identification of key characters, such as selfish genetic elements, introns, and structural variants.
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