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.
Evolutionary comparisons between major environmental divides, such as between marine and freshwater systems, can reveal the fundamental processes governing diversification dynamics. Although processes may differ due to the different scales of their biogeographic barriers, freshwater and marine environments nevertheless offer similar opportunities for diversification in benthic, demersal, and pelagic habitats. Here, we compare the evolutionary patterns and processes shaping teleost diversity in each of these three habitats and between marine and freshwater systems. Using specimens from the National Museum of Natural History, we developed a data set of linear measurements capturing body shape in 2266 freshwater and 3344 marine teleost species. With a novel comparative approach, we contrast the primary axis of morphological diversification in each habitat with the major axis defined by phylogenetic signal. By comparing angles between these axes, we find that fish in corresponding habitats have more similar primary axes of morphological diversity than would be expected by chance, but that different historical processes underlie these parallel patterns in freshwater and marine environments. Marine diversification is more strongly aligned with phylogenetic signal and shows a trend toward lineages occupying separate regions of morphospace. In contrast, ecological signal appears to be a strong driver of diversification in freshwater lineages through repeated morphological evolution in densely packed regions of morphospace. In spite of these divergent histories, our findings reveal that habitat has driven convergent patterns of evolutionary diversification on a global scale. [Benthic–pelagic axis; body shape; convergent evolution; morphological diversification; phylogenetic signal.]
more » « less- NSF-PAR ID:
- 10307072
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Systematic Biology
- ISSN:
- 1063-5157
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Premise The evolution of carnivorous pitcher traps across multiple angiosperm lineages represents a classic example of morphological convergence. Nevertheless, no comparative study to‐date has examined pitcher evolution from a quantitative morphometric perspective.
Methods In the present study, we used comparative morphometric approaches to quantify the shape space occupied by
Heliamphora pitchers and to trace evolutionary trajectories through this space to examine patterns of divergence and convergence within the genus. We also investigated pitcher development, and, how the packing of pitchers is affected by crowding, a common condition in their natural environments.Results Our results showed that
Heliamphora pitchers have diverged along three main axes in morphospace: (1) pitcher curvature; (2) nectar spoon elaboration; and (3) pitcher stoutness. Both curvature and stoutness are correlated with pitcher size, suggesting structural constraints in pitcher morphological evolution. Among the four traits (curvature, spoon elaboration, stoutness, and size), all but curvature lacked phylogenetic signal and showed marked convergence across the phylogeny. We also observed tighter packing of pitchers in crowded conditions, and this effect was most pronounced in curved, slender pitchers.Conclusions Overall, our study demonstrates that diversification and convergent evolution of carnivory‐related traits extends to finer evolutionary timescales, reinforcing the notion that ecological specialization may not necessarily be an evolutionary dead end.
