Pathways to polar adaptation in fishes revealed by long-read sequencing

Long-read sequencing is driving a new reality for genome science where highly contiguous assemblies can be produced efficiently with modest resources. Genome assemblies from long-read sequencing are particularly exciting for understanding the evolution of complex genomic regions that are often difficult to assemble. In this study, we leveraged long-read sequencing to generate a high-quality genome assembly for an Antarctic eelpout, Opthalmolycus amberensis, the first for the globally distributed family Zoarcidae. We used this assembly to understand how O. amberensis has adapted to the harsh Southern Ocean and compared it to another group of Antarctic fishes: the notothenioids. We showed that from a genome-wide perspective, selection has largely acted on different targets in eelpouts relative to notothenioids. However, we did find some overlap; in both groups, selection has acted on genes involved in membrane structure and DNA repair. We found evidence for historical shifts of transposable element activity in O. amberensis and other polar fishes, perhaps reflecting a response to environmental change. We were specifically interested in the evolution of two complex genomic regions known to underlie key adaptations to polar seas: hemoglobin and antifreeze proteins (AFPs). We observed unique evolution of the hemoglobin MN cluster in eelpouts and related fishes in the suborder Zoarcoidei relative to other teleosts. For AFPs, we identified the first species in the suborder with no evidence of afpIII sequences (Cebidichthys violaceus), potentially reflecting a lineage-specific loss of this gene cluster. Beyond polar fishes, our results highlight the power of long-read sequencing to understand genome evolution.

Genomic and biochemical evidence of dietary adaptation in a marine herbivorous fish

Adopting a new diet is a significant evolutionary change, and can profoundly affect an animal's physiology, biochemistry, ecology and genome. To study this evolutionary transition, we investigated the physiology and genomics of digestion of a derived herbivorous fish, Cebidichthys violaceus . We sequenced and assembled its genome (N50 = 6.7 Mb) and digestive transcriptome, and revealed the molecular changes related to digestive enzymes (carbohydrases, proteases and lipases), finding abundant evidence of molecular adaptation. Specifically, two gene families experienced expansion in copy number and adaptive amino acid substitutions: amylase and carboxyl ester lipase ( cel ), which are involved in the digestion of carbohydrates and lipids, respectively. Both show elevated levels of gene expression and increased enzyme activity. Because carbohydrates are abundant in the prickleback's diet and lipids are rare, these findings suggest that such dietary specialization involves both exploiting abundant resources and scavenging rare ones, especially essential nutrients, like essential fatty acids.

Physiological genomics of dietary adaptation in a marine herbivorous fish

Adopting a new diet is a significant evolutionary change and can profoundly affect an animal’s physiology, biochemistry, ecology, and its genome. To study this evolutionary transition, we investigated the physiology and genomics of digestion of a derived herbivorous fish, the monkeyface prickleback (Cebidichthys violaceus). We sequenced and assembled its genome and digestive transcriptome and revealed the molecular changes related to important dietary enzymes, finding abundant evidence for adaptation at the molecular level. In this species, two gene families experienced expansion in copy number and adaptive amino acid substitutions. These families, amylase, and bile salt activated lipase, are involved digestion of carbohydrates and lipids, respectively. Both show elevated levels of gene expression and increased enzyme activity. Because carbohydrates are abundant in the prickleback’s diet and lipids are rare, these findings suggest that such dietary specialization involves both exploiting abundant resources and scavenging rare ones, especially essential nutrients, like essential fatty acids.