Document Type

Article

Publication Date

2020

DOI

10.1073/pnas.2006511117

Publication Title

Proceedings of the National Academy of Sciences in the United States of America

Volume

117

Issue

52

Pages

33396-33403

Abstract

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.

Rights

© 2021 National Academy of Sciences

Publisher's version is available at https://doi.org/10.1073/pnas.2006511117

Data Availability

Article states: "Raw sequencing reads are available at National Center for Biotechnology Information Sequence Read Archive BioProject (number PRJNA630817). Alignments, trees, and code data have been deposited in Figshare (DOI: 10.6084/m9.figshare.13000100). All other study data are included in the article and supporting information."

"This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2006511117/-/DCSupplemental."

Original Publication Citation

Rincon-Sandoval, M., Duarte-Ribeiro, E., Davis, A. M., Santaquiteria, A., Hughes, L. C., Baldwin, C. C., Soto-Torres, L., Acero, P. A., Walker, H. J., Jr., Carpenter, K. E., Sheaves, M., Ortí, G., Arcila, D., & Betancur, R. R. (2020). Evolutionary determinism and convergence associated with water-column transitions in marine fishes. Proceedings of the National Academy of Sciences of the United States of America, 117(52), 33396-33403. https://doi.org/10.1073/pnas.2006511117

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