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.]
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.more » « less
- NSF-PAR ID:
- Publisher / Repository:
- Proceedings of the National Academy of Sciences
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Page Range / eLocation ID:
- p. 33396-33403
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
Evolutionary transitions between marine and freshwater ecosystems have occurred repeatedly throughout the phylogenetic history of fishes. The theory of ecological opportunity predicts that lineages that colonize species-poor regions will have greater potential for phenotypic diversification than lineages invading species-rich regions. Thus, transitions between marine and freshwaters may promote phenotypic diversification in trans-marine/freshwater fish clades. We used phylogenetic comparative methods to analyze body size data in nine major fish clades that have crossed the marine/freshwater boundary. We explored how habitat transitions, ecological opportunity, and community interactions influenced patterns of phenotypic diversity. Our analyses indicated that transitions between marine and freshwater habitats did not drive body size evolution, and there are few differences in body size between marine and freshwater lineages. We found that body size disparity in freshwater lineages is not correlated with the number of independent transitions to freshwaters. We found a positive correlation between body size disparity and overall species richness of a given area, and a negative correlation between body size disparity and diversity of closely related species. Our results indicate that the diversity of incumbent freshwater species does not restrict phenotypic diversification, but the diversity of closely related taxa can limit body size diversification. Ecological opportunity arising from colonization of novel habitats does not seem to have a major effect in the trajectory of body size evolution in trans-marine/freshwater clades. Moreover, competition with closely related taxa in freshwaters has a greater effect than competition with distantly related incumbent species.
Divergence in body shape is one of the most widespread and repeated patterns of morphological variation in fishes and is associated with habitat specification and swimming mechanics. Such ecological diversification is the first stage of the explosive adaptive radiation of cichlid fishes in the East African Rift Lakes. We use two hybrid crosses of cichlids (
Metriaclimasp .× Aulonocarasp. and Labidochromissp .× Labeotropheussp., >975 animals total) to determine the genetic basis of body shape diversification that is similar to benthic‐pelagic divergence across fishes. Using a series of both linear and geometric shape measurements, we identified 34 quantitative trait loci (QTL) that underlie various aspects of body shape variation. These QTL are spread throughout the genome, each explaining 3.2–8.6% of phenotypic variation, and are largely modular. Further, QTL are distinct both between these two crosses of Lake Malawi cichlids and compared to previously identified QTL for body shape in fishes such as sticklebacks. We find that body shape is controlled by many genes of small effect. In all, we find that convergent body shape phenotypes commonly observed across fish clades are most likely due to distinct genetic and molecular mechanisms.
Water mixing is a critical mechanism in marine habitats that governs many important processes, including nutrient transport. Physical mechanisms, such as winds or tides, are primarily responsible for mixing effects in shallow coastal systems, but the sheltered habitats adjacent to mangroves experience very low turbulence and vertical mixing. The significance of biogenic mixing in pelagic habitats has been investigated but remains unclear. In this study, we show that the upside-down jellyfish
Cassiopeasp. plays a significant role with respect to biogenic contributions to water column mixing within its shallow natural habitat ( m deep). The mixing contribution was determined by high-resolution flow velocimetry methods in both the laboratory and the natural environment. We demonstrate that Cassiopeasp. continuously pump water from the benthos upward in a vertical jet with flow velocities on the scale of centimeters per second. The volumetric flow rate was calculated to be 212 L⋅h-1for average-sized animals (8.6 cm bell diameter), which translates to turnover of the entire water column every 15 min for a median population density (29 animals per m2). In addition, we found Cassiopeasp. are capable of releasing porewater into the water column at an average rate of 2.64 mL⋅h−1per individual. The release of nutrient-rich benthic porewater combined with strong contributions to water column mixing suggests a role for Cassiopeasp. as an ecosystem engineer in mangrove habitats.
Habitat occupancy can have a profound influence on macroevolutionary dynamics, and a switch in major habitat type may alter the evolutionary trajectory of a lineage. In this study, we investigate how evolutionary transitions between marine and freshwater habitats affect macroevolutionary adaptive landscapes, using needlefishes (Belonidae) as a model system. We examined the evolution of body shape and size in marine and freshwater needlefishes and tested for phenotypic change in response to transitions between habitats. Using micro-computed tomographic (μCT) scanning and geometric morphometrics, we quantified body shape, size, and vertebral counts of 31 belonid species. We then examined the pattern and tempo of body shape and size evolution using phylogenetic comparative methods. Our results show that transitions from marine to freshwater habitats have altered the adaptive landscape for needlefishes and expanded morphospace relative to marine taxa. We provide further evidence that freshwater taxa attain reduced sizes either through dwarfism (as inferred from axial skeletal reduction) or through developmental truncation (as inferred from axial skeletal loss). We propose that transitions to freshwater habitats produce morphological novelty in response to novel prey resources and changes in locomotor demands. We find that repeated invasions of different habitats have prompted predictable changes in morphology.more » « less