Adaptation and molecular evidence for convergence in decapod crustaceans from deep-sea hydrothermal vent environments

Hydrothermal vents are unique deep-sea environments exhibiting extreme temperature gradients and toxic concentrations of H₂ S that limit the growth of biological communities. Notably, some decapod crustaceans are the dominant organisms inhabiting these environments, and share similar phenotypic and physiological traits, such as white body coloration and chemosynthetic capacity. However, a lack of genomic information has precluded an understanding of these convergent phenotypes. Here, comparative transcriptomic analyses were performed in 14 decapod species, including four deep-sea hydrothermal vent species and 10 shallow-water relatives. Phylogenetic analysis suggested that the four deep-sea species stemmed from different ancestors despite being geographically close, and therefore their similar traits were probably the product of convergent evolution rather than lineal inheritance. A total of 391 positively selected genes, 109 parallel substituted genes and 33 significantly expanded gene families were identified in the deep-sea decapods. Among these, only the SNARE interactions in vesicular transport pathway was significantly enriched, with both positively selected genes and parallel substituted genes, suggesting that specific macromolecule transport might be a strong convergent evolution trait in deep-sea decapods. Furthermore, many genes involved in protein synthesis, processing and energy metabolism were detected under convergent evolution, suggesting a role for adaptive evolution in association with a specific metabolic pathway in response to chemosynthetic nutrition patterns. Moreover, our study suggests that convergently evolved white body colour might have resulted from the contraction of the crustacyanin gene family and the low content of astaxanthin in the body of deep-sea decapods. Therefore, this study provides valuable genetic evidence for convergent evolution in deep-sea decapods.