A process of convergent amplification and tissue‐specific expression dominates the evolution of toxin and toxin‐like genes in sea anemones

• Published in: Molecular ecology 2019-05, Vol.28 (9), p.2272-2289
• Main Authors: Surm, Joachim M., Smith, Hayden L., Madio, Bruno, Undheim, Eivind A.B., King, Glenn F., Hamilton, Brett R., Burg, Chloé A., Pavasovic, Ana, Prentis, Peter J.
• Format: Article
• Language: English
• Subjects: Amplification; Animals; Biological evolution; Cnidaria; Cnidarian Venoms - chemistry; Cnidarian Venoms - genetics; Convergence; Copy number; Evolution; Evolutionary genetics; Gene Expression; Gene families; Gene sequencing; Genes; Inertia; Localization; Mass Spectrometry; mass spectrometry imaging; Mass spectroscopy; Phylogenetics; Phylogeny; Predators; Prey; Ribonucleic acid; RNA; RNA‐seq; Sea Anemones - genetics; Selection, Genetic; selective pressure; Sequence Analysis, RNA; Tissues; Toxins; venom
• ISSN: 0962-1083; 1365-294X
• DOI: 10.1111/mec.15084

Members of phylum Cnidaria are an ancient group of venomous animals and rely on a number of specialized tissues to produce toxins in order to fulfil a range of ecological roles including prey capture, defence against predators, digestion and aggressive encounters. However, limited comprehensive analyses of the evolution and expression of toxin genes currently exist for cnidarian species. In this study, we use genomic and transcriptomic sequencing data to examine gene copy number variation and selective pressure on toxin gene families in phylum Cnidaria. Additionally, we use quantitative RNA‐seq and mass spectrometry imaging to understand expression patterns and tissue localization of toxin production in sea anemones. Using genomic data, we demonstrate that the first large‐scale expansion and diversification of known toxin genes occurs in phylum Cnidaria, a process we also observe in other venomous lineages, which we refer to as convergent amplification. Our analyses of selective pressure on sea anemone toxin gene families reveal that purifying selection is the dominant mode of evolution for these genes and that phylogenetic inertia is an important determinant of toxin gene complement in this group. The gene expression and tissue localization data revealed that specific genes and proteins from toxin gene families show strong patterns of tissue and developmental‐phase specificity in sea anemones. Overall, convergent amplification and phylogenetic inertia have strongly influenced the distribution and evolution of the toxin complement observed in sea anemones, while the production of venoms with different compositions across tissues is related to the functional and ecological roles undertaken by each tissue type.