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

Rincon-Sandoval, Melissa, Duarte-Ribeiro, Emanuell, Davis, Aaron M., Santaquiteria, Aintzane, Hughes, Lily C., Baldwin, Carole C., Soto-Torres, Luisangely, Acero P, Arturo, Walker, H.J., Carpenter, Kent E., Sheaves, Marcus, Orti, Guillermo, Arcila, Dahiana, and Betancur-R, Ricardo (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). pp. 33396-33403.

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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 (similar to 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.

Item ID: 66055
Item Type: Article (Research - C1)
ISSN: 1091-6490
Keywords: phylogenomics, macroevolution, habitat transitions, benthic-pelagic axis, Lutjanidae
Copyright Information: © 2020 Published under the PNAS license.
Additional Information:

This article will be freely available from the publishers website from 17 June 2021.

Funders: National Science Foundation (NSF), Colciencias (Columbian Department for the Adminstration of Science, Technology and Innovation), University of Oklahoma
Projects and Grants: NSF grant DEB-1932759, NSF grant DEB-1929248, NSF grant DEB-1457426, NSF grant DEB-1541554, NSF grant DEB-1541552, NSF grant DEB-2015404, Colciencias postdoctoral fellowship grant 848-2019
Date Deposited: 17 Feb 2021 17:59
FoR Codes: 31 BIOLOGICAL SCIENCES > 3105 Genetics > 310509 Genomics @ 50%
31 BIOLOGICAL SCIENCES > 3104 Evolutionary biology > 310404 Evolution of developmental systems @ 50%
SEO Codes: 18 ENVIRONMENTAL MANAGEMENT > 1805 Marine systems and management > 180501 Assessment and management of benthic marine ecosystems @ 100%
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