Evolutionary patterns and repeated adaptive strategies of deep-sea anemones

Abstract

Sea anemones occupy the full depth of the oceans, yet their evolutionary patterns and adaptive strategies to the enigmatic deep sea have remained contentious and poorly resolved. Here, we assemble genomes (n = 13) and transcriptomes for 15 species collected between 432 and 6,000 m and integrate them with all publicly available actiniarian data. Phylogenomic analyses reveal a mosaic topology among deep-sea and shallow-water clades. Using a novel framework that contrasts convergent gene-loss patterns, we show that a large number of light-associated gene families-- including the complete circadian toolkit--were independently deleted after lineages entered the aphotic realm, whereas comparable loss in shallow taxa is negligible, providing decisive support for a shallow-water origin followed by multiple descents. Intriguingly, some deep-sea lineages further streamline energy budgets by recurrent loss or pseudogenisation of key meiotic genes (e.g., Meiosin, Ythdc2, Spo11, Rad21, Mlh3), indicating a shift towards asexual reproduction. Despite this extensive genomic erosion, deep-sea anemones exhibit sophisticated molecular tuning: specific amino-acid substitutions enhance protein stability and activity under deep-sea conditions, while selective expansions of gene families related to neural excitability, membrane systems, etc., likely mitigate the suppressive environmental effects on vital physiological processes. Enzyme activity assays in the yeast system confirm that the deep-sea variants exhibit superior activity and enhanced growth at 4{degrees}C. These results define a "loss-optimization-innovation" triad that underlies bathymetric adaptations and may apply to other deep-sea fauna worldwide.