Alternating regimes of shallow and deep-sea diversification explain a species-richness paradox in marine fishes.

The deep sea contains a surprising diversity of life, including iconic fish groups such as anglerfishes and lanternfishes. Still, >65% of marine teleost fish species are restricted to the photic zone <200 m, which comprises less than 10% of the ocean's total volume. From a macroevolutionary perspective, this paradox may be explained by three hypotheses: 1) shallow water lineages have had more time to diversify than deep-sea lineages, 2) shallow water lineages have faster rates of speciation than deep-sea lineages, or 3) shallow-to-deep sea transition rates limit deep-sea richness. Here we use phylogenetic comparative methods to test among these three non-mutually exclusive hypotheses. While we found support for all hypotheses, the disparity in species richness is better described as the uneven outcome of alternating phases that favored shallow or deep diversification over the past 200 million y. Shallow marine teleosts became incredibly diverse 100 million y ago during a period of warm temperatures and high sea level, suggesting the importance of reefs and epicontinental settings. Conversely, deep-sea colonization and speciation was favored during brief episodes when cooling temperatures increased the efficiency of the ocean's carbon pump. Finally, time-variable ecological filters limited shallow-to-deep colonization for much of teleost history, which helped maintain higher shallow richness. A pelagic lifestyle and large jaws were associated with early deep-sea colonists, while a demersal lifestyle and a tapered body plan were typical of later colonists. Therefore, we also suggest that some hallmark characteristics of deep-sea fishes evolved prior to colonizing the deep sea.

The rise of biting during the Cenozoic fueled reef fish body shape diversification.

Diversity of feeding mechanisms is a hallmark of reef fishes, but the history of this variation is not fully understood. Here, we explore the emergence and proliferation of a biting mode of feeding, which enables fishes to feed on attached benthic prey. We find that feeding modes other than suction, including biting, ram biting, and an intermediate group that uses both biting and suction, were nearly absent among the lineages of teleost fishes inhabiting reefs prior to the end-Cretaceous mass extinction, but benthic biting has rapidly increased in frequency since then, accounting for about 40% of reef species today. Further, we measured the impact of feeding mode on body shape diversification in reef fishes. We fit a model of multivariate character evolution to a dataset comprising three-dimensional body shape of 1,530 species of teleost reef fishes across 111 families. Dedicated biters have accumulated over half of the body shape variation that suction feeders have in just 18% of the evolutionary time by evolving body shape ∼1.7 times faster than suction feeders. As a possible response to the ecological and functional diversity of attached prey, biters have dynamically evolved both into shapes that resemble suction feeders as well as novel body forms characterized by lateral compression and small jaws. The ascendance of species that use biting mechanisms to feed on attached prey reshaped modern reef fish assemblages and has been a major contributor to their ecological and phenotypic diversification.

What is a mammalian omnivore? Insights into terrestrial mammalian diet diversity, body mass and evolution.

Mammalian omnivores are a broad group of species that are often treated uniformly in ecological studies. Here, we incorporate omnivorous dietary differences to investigate previously found mammalian macroevolutionary and macroecological trends. We investigate the frequency with which vertebrate prey, invertebrate prey, fibrous plant material and non-fibrous plant material co-occur in the diets of terrestrial mammals. We quantify the body size distributions and phylogenetic signal of different omnivorous diets and use multistate reversible jump Markov chain Monte Carlo methods to assess the transition rates between diets on the mammalian phylogenetic tree. We find omnivores that consume all four food types are relatively rare, as most omnivores consume only invertebrate prey and non-fibrous plants. In addition, omnivores that only consume invertebrate prey, many of which are from Rodentia, are on average smaller than omnivores that incorporate vertebrate prey. Our transition models have high rates from invertivorous omnivory to herbivory, and from vertivory to prey mixing and ultimately invertivory. We suggest prey type is an important aspect of omnivore macroevolution and macroecology, as it is correlated with body mass, evolutionary history and diet-related evolutionary transition rates. Future work should avoid lumping omnivores into one category given the ecological variety of omnivore diets and their strong evolutionary influence.

The deep sea is a hot spot of fish body shape evolution.

Deep-sea fishes have long captured our imagination with striking adaptations to life in the mysterious abyss, raising the possibility that this cold, dark ocean region may be a key hub for physiological and functional diversification. We explore this idea through an analysis of body shape evolution across ocean depth zones in over 3000 species of marine teleost fishes. We find that the deep ocean contains twice the body shape disparity of shallow waters, driven by elevated rates of evolution in traits associated with locomotion. Deep-sea fishes display more frequent adoption of forms suited to slow and periodic swimming, whereas shallow living species are concentrated around shapes conferring strong, sustained swimming capacity and manoeuvrability. Our results support long-standing impressions of the deep sea as an evolutionary hotspot for fish body shape evolution and highlight that factors like habitat complexity and ecological interactions are potential drivers of this adaptive diversification.

Ecology shapes the evolutionary trade-off between predator avoidance and defence in coral reef butterflyfishes.

Antipredator defensive traits are thought to trade-off evolutionarily with traits that facilitate predator avoidance. However, complexity and scale have precluded tests of this prediction in many groups, including fishes. Using a macroevolutionary approach, we test this prediction in butterflyfishes, an iconic group of coral reef inhabitants with diverse social behaviours, foraging strategies and antipredator adaptations. We find that several antipredator traits have evolved adaptively, dependent primarily on foraging strategy. We identify a previously unrecognised axis of diversity in butterflyfishes where species with robust morphological defences have riskier foraging strategies and lack sociality, while species with reduced morphological defences feed in familiar territories, have adaptations for quick escapes and benefit from the vigilance provided by sociality. Furthermore, we find evidence for the constrained evolution of fin spines among species that graze solely on corals, highlighting the importance of corals, as both prey and structural refuge, in shaping fish morphology.

Phylogeny and tempo of diversification in the superradiation of spiny-rayed fishes.

Spiny-rayed fishes, or acanthomorphs, comprise nearly one-third of all living vertebrates. Despite their dominant role in aquatic ecosystems, the evolutionary history and tempo of acanthomorph diversification is poorly understood. We investigate the pattern of lineage diversification in acanthomorphs by using a well-resolved time-calibrated phylogeny inferred from a nuclear gene supermatrix that includes 520 acanthomorph species and 37 fossil age constraints. This phylogeny provides resolution for what has been classically referred to as the "bush at the top" of the teleost tree, and indicates acanthomorphs originated in the Early Cretaceous. Paleontological evidence suggests acanthomorphs exhibit a pulse of morphological diversification following the end Cretaceous mass extinction; however, the role of this event on the accumulation of living acanthomorph diversity remains unclear. Lineage diversification rates through time exhibit no shifts associated with the end Cretaceous mass extinction, but there is a global decrease in lineage diversification rates 50 Ma that occurs during a period when morphological disparity among fossil acanthomorphs increases sharply. Analysis of clade-specific shifts in diversification rates reveal that the hyperdiversity of living acanthomorphs is highlighted by several rapidly radiating lineages including tunas, gobies, blennies, snailfishes, and Afro-American cichlids. These lineages with high diversification rates are not associated with a single habitat type, such as coral reefs, indicating there is no single explanation for the success of acanthomorphs, as exceptional bouts of diversification have occurred across a wide array of marine and freshwater habitats.

Tempo of trophic evolution and its impact on mammalian diversification.

Mammals are characterized by the complex adaptations of their dentition, which are an indication that diet has played a critical role in their evolutionary history. Although much attention has focused on diet and the adaptations of specific taxa, the role of diet in large-scale diversification patterns remains unresolved. Contradictory hypotheses have been proposed, making prediction of the expected relationship difficult. We show that net diversification rate (the cumulative effect of speciation and extinction), differs significantly among living mammals, depending upon trophic strategy. Herbivores diversify fastest, carnivores are intermediate, and omnivores are slowest. The tempo of transitions between the trophic strategies is also highly biased: the fastest rates occur into omnivory from herbivory and carnivory and the lowest transition rates are between herbivory and carnivory. Extant herbivore and carnivore diversity arose primarily through diversification within lineages, whereas omnivore diversity evolved by transitions into the strategy. The ability to specialize and subdivide the trophic niche allowed herbivores and carnivores to evolve greater diversity than omnivores.

The evolution of pharyngognathy: a phylogenetic and functional appraisal of the pharyngeal jaw key innovation in labroid fishes and beyond.

The perciform group Labroidei includes approximately 2600 species and comprises some of the most diverse and successful lineages of teleost fishes. Composed of four major clades, Cichlidae, Labridae (wrasses, parrotfishes, and weed whitings), Pomacentridae (damselfishes), and Embiotocidae (surfperches); labroids have been an icon for studies of biodiversity, adaptive radiation, and sexual selection. The success and diversification of labroids have been largely attributed to the presence of a major innovation in the pharyngeal jaw apparatus, pharyngognathy, which is hypothesized to increase feeding capacity and versatility. We present results of large-scale phylogenetic analyses and a survey of pharyngeal jaw functional morphology that allow us to examine the evolution of pharyngognathy in a historical context. Phylogenetic analyses were based on a sample of 188 acanthomorph (spiny-rayed fish) species, primarily percomorphs (perch-like fishes), and DNA sequence data collected from 10 nuclear loci that have been previously used to resolve higher level ray-finned fish relationships. Phylogenies inferred from this dataset using maximum likelihood, Bayesian, and species tree analyses indicate polyphyly of the traditional Labroidei and clearly separate Labridae from the remainder of the traditional labroid lineages (Cichlidae, Embiotocidae, and Pomacentridae). These three "chromide" families grouped within a newly discovered clade of 40 families and more than 4800 species (>27% of percomorphs and >16% of all ray-finned fishes), which we name Ovalentaria for its characteristic demersal, adhesive eggs with chorionic filaments. This fantastically diverse clade includes some of the most species-rich lineages of marine and freshwater fishes, including all representatives of the Cichlidae, Embiotocidae, Pomacentridae, Ambassidae, Gobiesocidae, Grammatidae, Mugilidae, Opistognathidae, Pholidichthyidae, Plesiopidae (including Notograptus), Polycentridae, Pseudochromidae, Atherinomorpha, and Blennioidei. Beyond the discovery of Ovalentaria, this study provides a surprising, but well-supported, hypothesis for a convict-blenny (Pholidichthys) sister group to the charismatic cichlids and new insights into the evolution of pharyngognathy. Bayesian stochastic mapping ancestral state reconstructions indicate that pharyngognathy has evolved at least six times in percomorphs, including four separate origins in members of the former Labroidei, one origin in the Centrogenyidae, and one origin within Beloniformes. Our analyses indicate that all pharyngognathous fishes have a mechanically efficient biting mechanism enabled by the muscular sling and a single lower jaw element. However, a major distinction exists between Labridae, which lacks the widespread, generalized percomorph pharyngeal biting mechanism, and all other pharyngognathous clades, which possess this generalized biting mechanism in addition to pharyngognathy. Our results reveal a remarkable history of pharyngognathy: far from a single origin, it appears to have evolved at least six times, and its status as a major evolutionary innovation is reinforced by it being a synapomorphy for several independent major radiations, including some of the most species rich and ecologically diverse percomorph clades of coral reef and tropical freshwater fishes, Labridae and Cichlidae. [Acanthomorpha; Beloniformes; Centrogenyidae; key innovation; Labroidei; Ovalentaria; pharyngeal jaws; Perciformes.].

The delayed rise of present-day mammals.

Did the end-Cretaceous mass extinction event, by eliminating non-avian dinosaurs and most of the existing fauna, trigger the evolutionary radiation of present-day mammals? Here we construct, date and analyse a species-level phylogeny of nearly all extant Mammalia to bring a new perspective to this question. Our analyses of how extant lineages accumulated through time show that net per-lineage diversification rates barely changed across the Cretaceous/Tertiary boundary. Instead, these rates spiked significantly with the origins of the currently recognized placental superorders and orders approximately 93 million years ago, before falling and remaining low until accelerating again throughout the Eocene and Oligocene epochs. Our results show that the phylogenetic 'fuses' leading to the explosion of extant placental orders are not only very much longer than suspected previously, but also challenge the hypothesis that the end-Cretaceous mass extinction event had a major, direct influence on the diversification of today's mammals.

Biomechanical trade-offs bias rates of evolution in the feeding apparatus of fishes.

Morphological diversification does not proceed evenly across the organism. Some body parts tend to evolve at higher rates than others, and these rate biases are often attributed to sexual and natural selection or to genetic constraints. We hypothesized that variation in the rates of morphological evolution among body parts could also be related to the performance consequences of the functional systems that make up the body. Specifically, we tested the widely held expectation that the rate of evolution for a trait is negatively correlated with the strength of biomechanical trade-offs to which it is exposed. We quantified the magnitude of trade-offs acting on the morphological components of three feeding-related functional systems in four radiations of teleost fishes. After accounting for differences in the rates of morphological evolution between radiations, we found that traits that contribute more to performance trade-offs tend to evolve more rapidly, contrary to the prediction. While ecological and genetic factors are known to have strong effects on rates of phenotypic evolution, this study highlights the role of the biomechanical architecture of functional systems in biasing the rates and direction of trait evolution.

Biotic Interactions and the Future of Fishes on Coral Reefs: The Importance of Trait-Based Approaches.

Biotic interactions govern the structure and function of coral reef ecosystems. As environmental conditions change, reef-associated fish populations can persist by tracking their preferred niche or adapting to new conditions. Biotic interactions will affect how these responses proceed and whether they are successful. Yet, our understanding of these effects is currently limited. Ecological and evolutionary theories make explicit predictions about the effects of biotic interactions, but many remain untested. Here, we argue that large-scale functional trait datasets enable us to investigate how biotic interactions have shaped the assembly of contemporary reef fish communities and the evolution of species within them, thus improving our ability to predict future changes. Importantly, the effects of biotic interactions on these processes have occurred simultaneously within dynamic environments. Functional traits provide a means to integrate the effects of both ecological and evolutionary processes, as well as a way to overcome some of the challenges of studying biotic interactions. Moreover, functional trait data can enhance predictive modeling of future reef fish distributions and evolvability. We hope that our vision for an integrative approach, focused on quantifying functionally relevant traits and how they mediate biotic interactions in different environmental contexts, will catalyze new research on the future of reef fishes in a changing environment.

Prolonged morphological expansion of spiny-rayed fishes following the end-Cretaceous.

Spiny-rayed fishes (Acanthomorpha) dominate modern marine habitats and account for more than a quarter of all living vertebrate species. Previous time-calibrated phylogenies and patterns from the fossil record explain this dominance by correlating the origin of major acanthomorph lineages with the Cretaceous-Palaeogene mass extinction. Here we infer a time-calibrated phylogeny using ultraconserved elements that samples 91.4% of all acanthomorph families and investigate patterns of body shape disparity. Our results show that acanthomorph lineages steadily accumulated throughout the Cenozoic and underwent a significant expansion of among-clade morphological disparity several million years after the end-Cretaceous. These acanthomorph lineages radiated into and diversified within distinct regions of morphospace that characterize iconic lineages, including fast-swimming open-ocean predators, laterally compressed reef fishes, bottom-dwelling flatfishes, seahorses and pufferfishes. The evolutionary success of spiny-rayed fishes is the culmination of multiple species-rich and phenotypically disparate lineages independently diversifying across the globe under a wide range of ecological conditions.

FishShapes v1: Functionally relevant measurements of teleost shape and size on three dimensions.

Teleost fishes account for 96% of all fish species and exhibit a spectacular variety of body forms. Teleost lineages range from deep bodied to elongate (e.g., eels, needlefish), laterally compressed (e.g., ribbonfish) to globular (e.g., pufferfish), and include uniquely shaped lineages such as seahorses, flatfishes, and ocean sunfishes. Adaptive body shape convergence within fishes has long been hypothesized but the nature of the relationships between fish form and ecological and environmental variables remain largely unknown at the macroevolutionary scale. To facilitate the investigation of the interacting factors influencing teleost body shape evolution we measured eight functionally relevant linear traits on adult-sized specimens along with specimen mass. Linear measurements of standard length, maximum body depth, maximum fish width, lower jaw length, mouth width, head depth, minimum caudal peduncle depth, and minimum caudal peduncle width were taken in millimeters with calipers, or tape measures for oversized specimens. We measured these traits on a total of 16,523 specimens (1-3 specimens per species) at the Smithsonian National Museum of Natural History and took approximately 7000 person hours of data collection to complete. The data went through a three-step error-checking process to clean and validate the data and then species averages were calculated. We present the complete specimen data set, which encompasses approximately one-fifth of extant teleost species diversity, spanning ~90% of teleost families and ~96% of orders. The species and family names are compatible with the taxonomy used by FishBase and the order information with the phylogenetically informed taxonomy of Betancur-R and colleagues published in 2014. This dataset is licensed under Creative Commons CC0 1.0 Universal (CC0 1.0) but please cite this paper when using the data or a subset of it.

The Effect of Locomotion Mode on Body Shape Evolution in Teleost Fishes.

Teleost fishes vary in their reliance on median and paired fins (MPF) or undulation of the body (BCF) to generate thrust during straight-line, steady swimming. Previous work indicates that swimming mode is associated with different body shapes, though this has never been empirically demonstrated across the diversity of fishes. As the body does not play as active a mechanical role in steady swimming by MPF swimmers, this may relax constraints and spur higher rates of body shape diversification. We test these predictions by measuring the impact of the dominant steady swimming mode on the evolution of body shape across 2295 marine teleost fishes. Aligning with historical expectations, BCF swimmers exhibit a more elongate, slender body shape, while MPF propulsion is associated with deeper and wider body shapes. However, in contrast to expectations, we find that BCF propulsion is associated with higher morphological diversity and greater variance around trait optima. This surprising result is consistent with the interpretation that stronger functional trade-offs stimulate phenotypic evolution, rather than constrain it.

Diversity versus disparity and the radiation of modern cetaceans.

Modern whales are frequently described as an adaptive radiation spurred by either the evolution of various key innovations (such as baleen or echolocation) or ecological opportunity following the demise of archaic whales. Recent analyses of diversification rate shifts on molecular phylogenies raise doubts about this interpretation since they find no evidence of increased speciation rates during the early evolution of modern taxa. However, one of the central predictions of ecological adaptive radiation is rapid phenotypic diversification, and the tempo of phenotypic evolution has yet to be quantified in cetaceans. Using a time-calibrated molecular phylogeny of extant cetaceans and a morphological dataset on size, we find evidence that cetacean lineages partitioned size niches early in the evolutionary history of neocetes and that changes in cetacean size are consistent with shifts in dietary strategy. We conclude that the signature of adaptive radiations may be retained within morphological traits even after equilibrium diversity has been reached and high extinction or fluctuations in net diversification have erased any signature of an early burst of diversification in the structure of the phylogeny.

Do key innovations unlock diversification? A case-study on the morphological and ecological impact of pharyngognathy in acanthomorph fishes.

Key innovations may allow lineages access to new resources and facilitate the invasion of new adaptive zones, potentially influencing diversification patterns. Many studies have focused on the impact of key innovations on speciation rates, but far less is known about how they influence phenotypic rates and patterns of ecomorphological diversification. We use the repeated evolution of pharyngognathy within acanthomorph fishes, a commonly cited key innovation, as a case study to explore the predictions of key innovation theory. Specifically, we investigate whether transitions to pharyngognathy led to shifts in the rate of phenotypic evolution, as well as shifts and/or expansion in the occupation of morphological and dietary space, using a dataset of 8 morphological traits measured across 3,853 species of Acanthomorpha. Analyzing the 6 evolutionarily independent pharyngognathous clades together, we found no evidence to support pharyngognathy as a key innovation; however, comparisons between individual pharyngognathous lineages and their sister clades did reveal some consistent patterns. In morphospace, most pharyngognathous clades cluster in areas that correspond to deeper-bodied morphologies relative to their sister clades, whereas occupying greater areas in dietary space that reflects a more diversified diet. Additionally, both Cichlidae and Labridae exhibited higher univariate rates of phenotypic evolution compared with their closest relatives. However, few of these results were exceptional relative to our null models. Our results suggest that transitions to pharyngognathy may only be advantageous when combined with additional ecological or intrinsic factors, illustrating the importance of accounting for lineage-specific effects when testing key innovation hypotheses. Moreover, the challenges we experienced formulating informative comparisons, despite the ideal evolutionary scenario of multiple independent evolutionary origins of pharyngognathous clades, illustrates the complexities involved in quantifying the impact of key innovations. Given the issues of lineage specific effects and rate heterogeneity at macroevolutionary scales we observed, we suggest a reassessment of the expected impacts of key innovations may be warranted.

The Future is Bright for Evolutionary Morphology and Biomechanics in the Era of Big Data.

In recent years, the fields of evolutionary biomechanics and morphology have developed into a deeply quantitative and integrative science, resulting in a much richer understanding of how structural relationships shape macroevolutionary patterns. This issue highlights new research at the conceptual and experimental cutting edge, with a special focus on applying big data approaches to classic questions in form-function evolution. As this issue illustrates, new technologies and analytical tools are facilitating the integration of biomechanics, functional morphology, and phylogenetic comparative methods to catalyze a new, more integrative discipline. Although we are at the cusp of the big data generation of organismal biology, the field is nonetheless still data-limited. This data bottleneck is primarily due to the rate-limiting steps of digitizing specimens, recording and tracking organismal movements, and extracting patterns from massive datasets. Automation and machine-learning approaches hold great promise to help data generation keep pace with ideas. As a final and important note, almost all the research presented in this issue relied on specimens-totaling the tens of thousands-provided by museum collections. Without collection, curation, and conservation of museum specimens, the future of the field is much less bright.

The influence of size on body shape diversification across Indo-Pacific shore fishes.

Understanding the causes of body shape variability across the tree of life is one of the central issues surrounding the origins of biodiversity. One potential mechanism driving observed patterns of shape disparity is a strongly conserved relationship between size and shape. Conserved allometry has been shown to account for as much as 80% of shape variation in some vertebrate groups. Here, we quantify the amount of body shape disparity attributable to changes in body size across nearly 800 species of Indo-Pacific shore fishes using a phylogenetic framework to analyze 17 geometric landmarks positioned to capture general body shape and functionally significant features. In marked contrast to other vertebrate lineages, we find that changes in body size only explain 2.9% of the body shape variation across fishes, ranging from 3% to 50% within our 11 sampled families. We also find a slight but significant trend of decreasing rates of shape evolution with increasing size. Our results suggest that the influence of size on fish shape has largely been overwhelmed by lineage-specific patterns of diversification that have produced the modern landscape of highly diverse forms that we currently observe in nature.

Hunting to extinction: biology and regional economy influence extinction risk and the impact of hunting in artiodactyls.

Half of all artiodactyls (even-toed hoofed mammals) are threatened with extinction, around double the mammalian average. Here, using a complete species-level phylogeny, we construct a multivariate model to assess for the first time which intrinsic (biological) and extrinsic (anthropogenic and environmental) factors influence variation in extinction risk in artiodactyls. Globally artiodactyls at greatest risk live in economically less developed areas, have older weaning ages and smaller geographical ranges. Our findings suggest that identifying predictors of threat is complicated by interactions between both biological and anthropogenic factors, resulting in differential responses to threatening processes. Artiodactyl species that experience unregulated hunting live in significantly less economically developed areas than those that are not hunted; however, hunted species are more susceptible to extinction if they have slower reproductive rates (older weaning ages). In contrast, risk in non-hunted artiodactyls is unrelated to reproductive rate and more closely associated with the economic development of the region in which they live.

The Impact of Organismal Innovation on Functional and Ecological Diversification.

Innovations in organismal functional morphology are thought to be a major force in shaping evolutionary patterns, with the potential to drive adaptive radiation and influence the evolutionary prospects for lineages. But the evolutionary consequences of innovation are diverse and usually do not result in adaptive radiation. What factors shape the macroevolutionary impact of innovations? We assert that little is known in general about the macroevolutionary outcomes associated with functional innovations and we discuss a framework for studying biological innovations in an evolutionary context. Innovations are novel functional mechanisms that enhance organismal performance. The ubiquity of trade-offs in functional systems means that enhanced performance on one axis often occurs at the expense of performance on another axis, such that many innovations result in an exchange of performance capabilities, rather than an expansion. Innovations may open up new resources for exploitation but their consequences for functional and ecological diversification depend heavily on the adaptive landscape around these novel resources. As an example of a broader program that we imagine, we survey five feeding innovations in labrid fishes, an exceptionally successful and ecologically diverse group of reef fishes, and explore their impact on the rate of evolution of jaw functional morphology. All of the innovations provide performance enhancements and result in changes in patterns of resource use, but most are not associated with subsequent functional diversification or substantial ecological diversification. Because selection acts on a specific performance enhancement and not on the evolutionary potential of an innovation, the enhancement of diversity may be highly serendipitous. The macroevolutionary potential of innovations depends critically on the interaction between the performance enhancement and the ecological opportunity that is exposed.