Diadromy Drives Elevated Rates of Trait Evolution and Ecomorphological Convergence in Clupeiformes (Herring, Shad, and Anchovies).

AbstractMigration can have a profound influence on rates and patterns of phenotypic evolution. Diadromy is the migration between marine and freshwater habitats for feeding and reproduction that can require individuals to travel tens to thousands of kilometers. The high energetic demands of diadromy are predicted to select for ecomorphological traits that maximize swimming and locomotor efficiency. Intraspecific studies have shown repeated instances of divergence among diadromous and nondiadromous populations in locomotor and foraging traits, which suggests that at a macroevolutionary scale diadromous lineages may experience convergent evolution onto one or multiple adaptive optima. We tested for differences in rates and patterns of phenotypic evolution among diadromous and nondiadromous lineages in Clupeiformes, a clade that has evolved diadromy more than 10 times. Our results show that diadromous clupeiforms show convergent evolution for some locomotor traits and faster rates of evolution, which we propose are adaptive responses to the locomotor demands of migration. We also find evidence that diadromous lineages show convergence into multiple regions of multivariate trait space and suggest that these respective trait spaces are associated with differences in migration and trophic ecology. However, not all locomotor traits and no trophic traits show evidence of convergence or elevated rates of evolution associated with diadromy. Our results show that long-distance migration influences the tempo and patterns of phenotypic evolution at macroevolutionary scales, but there is not a single diadromous syndrome.

Accelerated Diversification Explains the Exceptional Species Richness of Tropical Characoid Fishes.

The Neotropics harbor the most species-rich freshwater fish fauna on the planet, but the timing of that exceptional diversification remains unclear. Did the Neotropics accumulate species steadily throughout their long history, or attain their remarkable diversity recently? Biologists have long debated the relative support for these museum and cradle hypotheses, but few phylogenies of megadiverse tropical clades have included sufficient taxa to distinguish between them. We used 1288 ultraconserved element loci spanning 293 species, 211 genera, and 21 families of characoid fishes to reconstruct a new, fossil-calibrated phylogeny and infer the most likely diversification scenario for a clade that includes a third of Neotropical fish diversity. This phylogeny implies paraphyly of the traditional delimitation of Characiformes because it resolves the largely Neotropical Characoidei as the sister lineage of Siluriformes (catfishes), rather than the African Citharinodei. Time-calibrated phylogenies indicate an ancient origin of major characoid lineages and reveal a much more recent emergence of most characoid species. Diversification rate analyses infer increased speciation and decreased extinction rates during the Oligocene at around 30 Ma during a period of mega-wetland formation in the proto-Orinoco-Amazonas. Three species-rich and ecomorphologically diverse lineages (Anostomidae, Serrasalmidae, and Characidae) that originated more than 60 Ma in the Paleocene experienced particularly notable bursts of Oligocene diversification and now account collectively for 68% of the approximately 2150 species of Characoidei. In addition to paleogeographic changes, we discuss potential accelerants of diversification in these three lineages. While the Neotropics accumulated a museum of ecomorphologically diverse characoid lineages long ago, this geologically dynamic region also cradled a much more recent birth of remarkable species-level diversity. [Biodiversity; Characiformes; macroevolution; Neotropics; phylogenomics; ultraconserved elements.].

Migratory lineages rapidly evolve larger body sizes than non-migratory relatives in ray-finned fishes.

Migratory animals respond to environmental heterogeneity by predictably moving long distances in their lifetime. Migration has evolved repeatedly in animals, and many adaptations are found across the tree of life that increase migration efficiency. Life-history theory predicts that migratory species should evolve a larger body size than non-migratory species, and some empirical studies have shown this pattern. A recent study analysed the evolution of body size between diadromous and non-diadromous shads, herrings, anchovies and allies, finding that species evolved larger body sizes when adapting to a diadromous lifestyle. It remains unknown whether different fish clades adapt to migration similarly. We used an adaptive landscape framework to explore body size evolution for over 4500 migratory and non-migratory species of ray-finned fishes. By fitting models of macroevolution, we show that migratory species are evolving towards a body size that is larger than non-migratory species. Furthermore, we find that migratory lineages evolve towards their optimal body size more rapidly than non-migratory lineages, indicating body size is a key adaption for migratory fishes. Our results show, for the first time, that the largest vertebrate radiation on the planet exhibited strong evolutionary determinism when adapting to a migratory lifestyle.

The role of abiotic and biotic factors in the unequal body shape diversification of a Gondwanan fish radiation (Otophysi: Characiformes).

Understanding why some clades diversify greatly while others do not is a major goal of evolutionary biology. Both abiotic and biotic factors are important in driving unequal morphological diversity across the tree of life. However, few studies have quantified how abiotic habitat and community composition differences influence unequal morphological diversification in spatiotemporally diffuse radiations. We use geometric morphometrics, abiotic habitat data generated by Geographic Information Systems (GIS) analyses, evolutionary simulations, and phylogenetic comparative methods to determine whether random evolution, habitat variation, competition for niches, or a combination of factors influenced the unequal body shape diversity of a Gondwanan freshwater fish radiation. We find that Neotropical characiform lineages, which exhibit substantially more body shape diversity than their African counterparts, occupy significantly more slope and elevation habitats than African lineages. Differences in habitat occupation between the continental radiations occur through a combination of likely competition with cypriniform fishes in Africa restricting access to higher slope and elevation habitats and significantly more low-elevation and slope habitats available in the Neotropics. Our findings suggest that spatiotemporally widespread radiations, like Characiformes, do not diversify across homogenized habitats and biotic assemblages, with differences in community structure and physical habitat playing an important role in driving unequal morphological diversification.

High-latitude ocean habitats are a crucible of fish body shape diversification.

A decline in diversity from the equator to the poles is a common feature of Earth's biodiversity. Here, we examine body shape diversity in marine fishes across latitudes and explore the role of time and evolutionary rate in explaining the diversity gradient. Marine fishes' occupation of upper latitude environments has increased substantially over the last 80 million years. Fishes in the highest latitudes exhibit twice the rate of body shape evolution and one and a third times the disparity compared to equatorial latitudes. The faster evolution of body shape may be a response to increased ecological opportunity in polar and subpolar oceans due to (1) the evolution of antifreeze proteins allowing certain lineages to invade regions of cold water, (2) environmental disturbances driven by cyclical warming and cooling in high latitudes, and (3) rapid transitions across depth gradients. Our results add to growing evidence that evolutionary rates are often faster at temperate, not tropical, latitudes.

Simultaneous integration and modularity underlie the exceptional body shape diversification of characiform fishes.

Evolutionary biology has long striven to understand why some lineages diversify exceptionally while others do not. Most studies have focused on how extrinsic factors can promote differences in diversification dynamics, but a clade's intrinsic modularity and integration can also catalyze or restrict its evolution. Here, we integrate geometric morphometrics, phylogenetic comparative methods and visualizations of covariance to infer the presence of distinct modules in the body plan of Characiformes, an ecomorphologically diverse fish radiation. Strong covariances reveal a cranial module, and more subtle patterns support a statistically significant subdivision of the postcranium into anterior (precaudal) and posterior (caudal) modules. We uncover substantial covariation among cranial and postcranial landmarks, indicating body-wide evolutionary integration as lineages transition between compressiform and fusiform body shapes. A novel method of matrix subdivision reveals that within- and among-module covariation contributes substantially to the overall eigenstructure of characiform morphospace, and that both phenomena led to biologically important divergence among characiform lineages. Functional integration between the cranium and post-cranial skeleton appears to have allowed lineages to optimize the aspect ratio of their bodies for locomotion, while the capacity for independent change in the head, body and tail likely eased adaptation to diverse dietary and hydrological regimes. These results reinforce a growing consensus that modularity and integration synergize to promote diversification.

Patterns of Phenotypic Evolution Associated with Marine/Freshwater Transitions in Fishes.

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.

Adaptation to herbivory and detritivory drives the convergent evolution of large abdominal cavities in a diverse freshwater fish radiation (Otophysi: Characiformes).

Convergent evolution is often interpreted as evidence of natural selection favoring an optimal phenotype during adaptation. Morphological convergence is frequently found among lineages that converge on diet, but most studies have focused on morphological traits that relate exclusively to food handling and processing. In vertebrates, there is a strong inverse relationship between intestine length and trophic level. However, little is known about whether adaptation to a low trophic level influences the evolution of abdominal cavities that can accommodate larger intestines. Here, I reconstruct the evolutionary history of trophic ecology and examine abdominal cavity shape across 157 species of the fish order Characiformes to determine whether adaptation to an herbivorous-detritivorous diet drives convergent evolution of large abdominal cavities. Herbivorous-detritivorous species evolved significantly larger abdominal cavities than other trophic groups and repeatedly converged on a similar abdominal cavity morphology. Other trophic groups evolved abdominal cavity morphologies either stochastically or by selective pressures from an untested ecological character. These findings demonstrate that the selective demands of a larger intestinal tract promote the repeated convergence of a large abdominal cavity within herbivorous-detritivorous characiform fishes, while allowing other lineages to evolve randomly or adapt in response to other selection pressures, contributing to the overall body shape diversity of the order.

Patterns of Body Shape Diversity and Evolution in Intertidal and Subtidal Lineages of Combtooth Blennies (Blenniidae).

Marine intertidal zones can be harsher and more dynamic than bordering subtidal zones, with extreme and temporally variable turbulence, water velocity, salinity, temperature, and dissolved oxygen levels. Contrasting environmental conditions and ecological opportunities in subtidal versus intertidal habitats may generate differing patterns of morphological diversity. In this study we used phylogenetic comparative methods, measurements of body length, and two-dimensional landmarks to characterize body shape and size diversity in combtooth blennies (Ovalentaria: Blenniidae) and test for differences in morphological diversity between intertidal, subtidal, and supralittoral zones. We found that subtidal combtooth blennies have significantly higher body shape disparity and occupy a region of morphospace three times larger than intertidal lineages. The intertidal morphospace was almost entirely contained within the subtidal morphospace, showing that intertidal combtooth blennies did not evolve unique body shapes. We found no significant differences in body size disparity between tidal zones, no correlations between body shape and tidal zone or body size and tidal zone, and no body shape convergence associated with tidal zone. Our findings suggest that a subset of combtooth blenny body shapes are suitable for life in both subtidal and intertidal habitats. Many species in regions of morphospace unique to subtidal combtooth blennies exhibit distinct microhabitat use, which suggests subtidal environments promoted morphological diversification via evolutionary microhabitat transitions. In contrast, limited intertidal body shape diversity may be due to strong selective pressures that constrained body shape evolution and environmental filtering that prevented colonization of intertidal zones by certain subtidal body shapes.

Habitat transitions alter the adaptive landscape and shape phenotypic evolution in needlefishes (Belonidae).

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.

Ancient and contingent body shape diversification in a hyperdiverse continental fish radiation.

The characiform fishes of the Neotropics and Africa radiated remarkably in ecomorphology, but the macroevolutionary processes responsible for their biodiversity remain unexplored, and the degree to which their continental diversification parallels classic adaptive radiations remains untested. We reconstruct their diversification using a new fossil-calibrated molecular phylogeny, dietary information, and geometric morphometrics. Though body shape diversified early in a manner consistent with an ancient continental adaptive radiation, trophic shifts did not always coincide with shape changes. With the notable exception of piscivores, lineages that converged in diet did not converge closely in body shape. Shifts in habitat or other variables likely influenced body shape evolution in addition to changes in diet, and the clade's history departs from many classic adaptive radiations in lakes or on islands, in which trophic convergence drives morphological convergence. The contrast between the Neotropical radiation's exhaustive exploration of morphospace and the more restrained diversification in Africa suggests a major role for contingency in characiform evolution, with the presence of cypriniform competitors in the Old World, but not the New, providing one possible explanation. Our results depict the clearest ecomorphological reconstruction to date for Characiformes and set the stage for studies further elucidating the processes underlying its diversification.

Littorally adaptive? Testing the link between habitat, morphology, and reproduction in the intertidal sculpin subfamily Oligocottinae (Pisces: Cottoidea).

While intertidal habitats are often productive, species-rich environments, they are also harsh and highly dynamic. Organisms that live in these habitats must possess morphological and physiological adaptations that enable them to do so. Intertidal fishes are generally small, often lack scales, and the diverse families represented in intertidal habitats often show convergence into a few general body shapes. However, few studies have quantified the relationship between phenotypes and intertidal living. Likewise, the diversity of reproductive traits and parental care in intertidal fishes has yet to be compared quantitatively with habitat. We examine the relationship of these characters in the sculpin subfamily Oligocottinae using a phylogenetic hypothesis, geometric morphometrics, and phylogenetic comparative methods to provide the first formal test of associations between fish phenotypes and reproductive characters with intertidal habitats. We show that the ability to live in intertidal habitats, particularly in tide pools, is likely a primitive state for Oligocottinae, with a single species that has secondarily come to occupy only subtidal habitats. Contrary to previous hypotheses, maximum size and presence of scales do not show a statistically significant correlation with depth. However, the maximum size for all species is generally small (250 mm or less) and all show a reduction in scales, as would be expected for an intertidal group. Also contrary to previous hypotheses, we show that copulation and associated characters are the ancestral condition in Oligocottinae, with copulation most likely being lost in a single lineage within the genus Artedius. Lastly, we show that body shape appears to be constrained among species with broader depth ranges, but lineages that occupy only a narrow range of intertidal habitats display novel body shapes, and this may be associated with habitat partitioning, particularly as it relates to the degree of wave exposure.

Systematic assessment of the Leporinus desmotes species complex, with a description of two new species

Members of the Leporinus desmotes species complex can be distinguished from other barred or banded congeners by the combination of nine distinct black bars across the head and trunk and long, pointed, laterally compressed and upward curving symphyseal dentary teeth. A taxonomic reassessment of this complex revealed two new species, one from the Orinoco and Negro rivers of Venezuela and Brazil, and the other from the Xingu and Tapajós rivers of Brazil. Both species are similar to L. desmotes and L. jatuncochi, but differ significantly in body shape morphology, coloration, and/or circumpeduncular scale counts. Genetic evidence also contributes to the recognition of both new species. This contribution also maps the geographic distribution of the four known species, and highlights the presence of an unusual meristic polymorphism within Leporinus desmotes sensu stricto that may suggest the presence of even more unrecognized diversity.(AU)

As espécies do complexo Leporinus desmotes diferem da maioria dos congêneres com base nas nove barras transversais escuras ao redor da cabeça e do corpo, e do dente sinfisiano do dentário alongado, comprimido lateralmente e ligeiramente curvado para cima. Uma revisão taxonômica desse complexo revelou a existência de duas espécies novas, uma dos rios Orinoco e Negro na Venezuela e Brasil, e outra das drenagens dos rios Xingu e Tapajós, no Brasil. As duas espécies novas são similares à L. desmotes e L. jatuncochi, das quais diferem significativamente por uma combinação de forma do corpo, coloração e número de séries de escamas ao redor do pedúnculo caudal. Dados genéticos também corroboram o reconhecimento das duas espécies novas. Esta contribuição ainda traz novos dados sobre a distribuição geográfica de cada uma das espécies do complexo, e discute a presença de um incomum polimorfismo no número de escamas ao redor do pedúnculo caudal em Leporinus desmotes stricto sensu, que sugere a presença de uma diversidade ainda maior de espécies não descritas.(AU)