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.

Keywords: Lutjanidae; benthic–pelagic axis; habitat transitions; macroevolution; phylogenomics.

Fig. 1.

Phylogeny, habitat transitions, and biogeography of snappers and fusiliers. The tree shown is derived from a concatenation-based maximum-likelihood analysis of 1,115 exons, with node ages estimated from a time-calibrated analysis using seven calibration points in MCMCTree. The habitat reconstructions for benthic and midwater lineages, shown as colored branches in the tree, account for phylogenetic uncertainty (28 trees) and habitat coding ambiguity (13 tips with uncertain or multistate habitats; see Dataset S2). The color gradients along branches denote habitat transitions; the purple branches indicate lineages with ambiguous habitats based on reconstructions using alternative coding schemes (SI Appendix, Figs. S8–S11). The colored circles indicate colonization events (inferred with BioGeoBEARS; see also SI Appendix, Figs. S8 and S12–S14) of the Atlantic (yellow circles) and the tropical eastern Pacific (purple circles) from Indo-Pacific lineages (center of origin; green circle). The arrows in the maps depict reconstructed colonization routes by different lineages in three time slices: 50 to 12 Ma (mean, 31 Ma), before the closure of Tethys Seaway; 12 to 2.8 Ma (mean, 7.4 Ma), after closure of Tethys Seaway and before the closure of the Isthmus of Panama; and 2.8 Ma to present (mean, 1.4 Ma), after the closure of the Isthmus of Panama. The thickness of the arrows is proportional to the number of lineages that colonized via each route; for some lineages, colonization routes are uncertain, and thus all alternative routes are depicted. The arrows in the central panel show the transition rates between benthic and pelagic habitats, as estimated with HiSSE (see also SI Appendix, Tables S10–S12).

Fig. 2.

The traitgram-informed morphospaces for lutjanids illustrating ecomorphological partitioning and convergence across benthic and midwater lineages, as estimated using the full-body dataset. The contour lines represent the two-dimensional density distributions of the species in each habitat state. The traitgrams overlain along PC axes depict the phylogeny in Fig. 1, including the ancestral habitat reconstructions estimated with SIMMAP (A, PC1 versus PC2; B, PC3 versus PC4). The color gradients along branches denote habitat transitions; the purple branches and data points indicate lineages with ambiguous habitats based on alternative coding schemes. The branches shifting from red to blue along PC1 extremes highlight convergent evolution in midwater lineages. The parenthetical values indicate the total variance explained by each PC axis.

Fig. 3.

The model-fitting comparisons and lineage diversification parameters estimated by accounting for phylogenetic uncertainty (28 trees) and habitat coding ambiguity (13 tips with uncertain or multistate habitats). The comparisons of alternative models of morphological evolution using the full-body dataset: (A) distribution of the Akaike information criterion (AIC) values for the four alternative models of continuous trait evolution (BM, OU, BMM, and OUM) and (B) AIC weights (AICw) of each alternative model and tree. The comparisons for alternative models of lineage diversification: (C) distribution of AIC values for seven alternative SSE models (SI Appendix, Tables S2–S4) and (D) AICw for each SSE model based on each of the 28 trees. The estimated lineage diversification parameters: (E) net-diversification values for the three habitat states and (F) transition rates (Q) between benthic and midwater states.