Comparative Transcriptomics Reveals Patterns of Adaptive Evolution Associated with Depth and Age Within Marine Rockfishes (Sebastes)

Abstract

The genetic underpinnings that contribute to ecological adaptation and speciation are not completely understood, especially within marine ecosystems. These evolutionary processes can be elucidated by studying adaptive radiations, because they provide replicates of divergence within a given environment or time-frame. Marine rockfishes (genus Sebastes) are an adaptive radiation and unique model system for studying adaptive evolution in the marine realm. We investigated molecular evolution associated with ecological (depth) and life history (lifespan) divergence in 2 closely related clades of Sebastes. Brain transcriptomes were sequenced via RNA-Seq from 3 species within the subgenus Pteropodus and a pair of related congeners from the subgenus Sebastosomus in order to identify patterns of adaptive evolution. De novo assemblies from these transcriptomes were used to identify 3867 orthologous clusters, and genes subject to positive selection were identified based on all 5 species, depth, and lifespan. Within all our analyses, we identified hemoglobin subunit α to be under strong positive selection and is associated with the depth of occurrence. In our lifespan analysis we identified immune function genes under positive selection in association with maximum lifespan. This study provides insight on the molecular evolution of rockfishes and these candidate genes may provide a better understanding of how these subgenera radiated within the Northeast Pacific.

Keywords: RNA-Seq; brain; depth; hemoglobin; longevity; positive selection.

Figure 1.

A cladogram that depicts the evolutionary relationships of the species used in this study. Located at the nodes are the estimated time since the divergence of the most recent common ancestor based on the Hyde and Vetter (2007) study. Sebastes carnatus, S. maliger, and S. nebulosus are species from the subgenus Pteropodus. Sebastes serranoides and S. mystinus represent species from the subgenus Sebastosomus.

Figure 2.

Annotated PSGs plotted in ReviGO for all 4 analyses: (A) All-Sites–212 GOs, (B) Depth–111 GOs, Sebastes mystinus Branch–124 GOs, and (C) Lifespan–75 GOs. Color and size indicates log Ka/Ks values and the y axis has no intrinsic value. The diameter of the circle indicates a high Ka/Ks value (large) and low Ka/Ks value (small). All GOs were viewed only for biological processes.

Figure 3.

A ML phylogeny of all HBA genes identified from out 5 transcriptomic datasets. The HBA_2a clade (blue box) contains gene sequences found under selection within our PAML analyses with 2 additional rockfish species (S. nigrocinctus and S. rubrivinctus). The HBA_2b clade contains sequences which were only identified in S. nigrocinctus and S. rubrivinctus. The HBA_1 clade (green box) which was not identified in our PAML analyses (S. nigrocinctus contained an orthologous sequence to this clade but a S. nebulosus orthologous sequence was not detected). Omega values (M0) are presented for the 2 highlighted rockfish clades by using PAML (Yang 1997) and bootstrap values over 70 are displayed.

Figure 4.

Venn diagram of all annotated PSGs from All-Sites, Depth, and Lifespan PAML analyses. Values indicate the number of annotated genes that pertain to a given category and meet the BH corrected P values (α = 0.05).