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

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.

Detecting (non)parallel evolution in multidimensional spaces: angles, correlations and eigenanalysis

“…Parallel responses to similar selection pressures between lineages are often regarded as evidence for repeatability or predictability of phenotypic evolution under natural selection, and the prevalence and extent of such parallelism are under active debate (e.g. [9][10][11]).…”

Phylogenomics and body shape morphometrics reveal recent diversification in the goatfishes (Syngnatharia: Mullidae)

“…Given our current understanding of goatfish ecology and life history, high rates of larval dispersal and specialized feeding modes likely play a large role in driving recent bursts in diversification. Water column position has been shown to correlate with rates of morphological diversification, as benthic associated species may be associated with higher diversification rates compared to their pelagic counterparts (Friedman et al 2020; Rincon-Sandoval et al 2020). However, this trend has been shown to vary widely across clades depending on their developmental patterns and life history traits (Claverie and Wainwright 2014; McCord et al 2021).…”

Global patterns and drivers of beta diversity facets of reef fish faunas

“…Furthermore, within regions, the trait composition of species-poor reef fish assemblages was found to be strongly nested within the trait composition of species-rich ones (Bender et al, 2017), which explain the weak turnover of traits among tropical reef fish assemblages (see Figure 1). Overall, the high level of trait similarity between tropical reef fish assemblages is probably the result of evolutionary convergence, where independent lineages display similar traits (and occupy similar ecological niches), or environmental filtering or both processes (Mazel et al, 2017;Rincon-Sandoval et al, 2020).…”