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Evolutionary determinism and convergence associated with water-column transitions in marine fishes

Significance Body shape is a strong predictor of habitat occupation in fishes, which changes rapidly at microevolutionary scales in well-studied freshwater systems such as sticklebacks and cichlids. Deep-bodied forms tend to occur in benthic habitats, while pelagic species typically have streamlined body plans. The recurrent evolution of this pattern across distantly related groups suggests that limited sets of high-fitness solutions exist due to environmental constraints. We rigorously test these observations showing that similar constraints operate at deeper evolutionary scales in a clade (Lutjanidae) of primarily benthic fish dwellers that repeatedly transitioned into midwater habitats in all major oceans throughout its 45-million-year history. Midwater species strongly converge in body shape, emphasizing evolutionary determinism in form and function along the benthic–pelagic axis. Repeatable, convergent outcomes are prima facie evidence for determinism in evolutionary processes. Among fishes, well-known examples include microevolutionary habitat transitions into the water column, where freshwater populations (e.g., sticklebacks, cichlids, and whitefishes) recurrently diverge toward slender-bodied pelagic forms and deep-bodied benthic forms. However, the consequences of such processes at deeper macroevolutionary scales in the marine environment are less clear. We applied a phylogenomics-based integrative, comparative approach to test hypotheses about the scope and strength of convergence in a marine fish clade with a worldwide distribution (snappers and fusiliers, family Lutjanidae) featuring multiple water-column transitions over the past 45 million years. We collected genome-wide exon data for 110 (∼80%) species in the group and aggregated data layers for body shape, habitat occupancy, geographic distribution, and paleontological and geological information. We also implemented approaches using genomic subsets to account for phylogenetic uncertainty in comparative analyses. Our results show independent incursions into the water column by ancestral benthic lineages in all major oceanic basins. These evolutionary transitions are persistently associated with convergent phenotypes, where deep-bodied benthic forms with truncate caudal fins repeatedly evolve into slender midwater species with furcate caudal fins. Lineage diversification and transition dynamics vary asymmetrically between habitats, with benthic lineages diversifying faster and colonizing midwater habitats more often than the reverse. Convergent ecological and functional phenotypes along the benthic–pelagic axis are pervasive among different lineages and across vastly different evolutionary scales, achieving predictable high-fitness solutions for similar environmental challenges, ultimately demonstrating strong determinism in fish body-shape evolution.