Feeding kinematics of a surgeonfish reveal novel functions and relationships to reef substrata.

Biting to obtain attached benthic prey characterizes a large number of fish species on coral reefs, and is a feeding mode that contributes to important ecosystem functions. We use high-speed video to reveal the mechanisms used by a surgeonfish, Acanthurus leucosternon, to detach algae. After gripping algae in its jaws, the species pulls it by ventrally rotating both the head and the closed jaws, in a novel use of the intra-mandibular joint. These motions remain in the plane of the fish, reducing the use of a lateral head flick to detach the algae. The novel ability to bite and pull algae off the substrate without bending the body laterally minimizes exposure to high water flows, and may be an adaptation to feeding in challenging reef habitats such as the crest and flat. Therefore, our results could potentially represent a key milestone in the evolutionary history of coral reef trophodynamics.

The cichlid pharyngeal jaw novelty enhances evolutionary integration in the feeding apparatus.

The modified pharyngeal jaw system of cichlid fishes is widely viewed as a key innovation that substantially facilitated the evolutionary exuberance of this iconic evolutionary radiation. We conduct comparative phylogenetic analyses of integration, disparity, and rate of evolution among feeding-related, skeletal structures in Neotropical cichlids and North American centrarchids, which lack the specialized pharyngeal jaw. Contrasting evolutionary patterns in these two continental radiations, we test a classic decoupling hypothesis. Specifically, we ask whether the modified pharyngeal jaw in cichlids resulted in enhanced evolutionary independence of the oral and pharyngeal jaws, leading to increased diversity of trophic structures. Contrary to this prediction, we find significantly stronger evolutionary integration between the oral and pharyngeal jaws in cichlids compared to centrarchids, although the two groups do not differ in patterns of integration within each jaw system. Further, though we find no significant differences in disparity, centrarchids show faster rates of morphological evolution. Our results suggest that the modified pharyngeal jaw resulted in less evolutionary independence and slower rates of evolution within the feeding system. Thus, we raise the possibility that the cichlid novelty enhances feeding performance, but does not prompt increased morphological diversification within the feeding apparatus, as has long been thought.

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.

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.

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.

A novel intramandibular joint facilitates feeding versatility in the sixbar distichodus.

The intramandibular joint (IMJ) is a secondary point of movement between the two major bones of the lower jaw. It has independently evolved in several groups of teleost fishes, each time representing a departure from related species in which the mandible functions as a single structure rotating only at the quadratomandibular joint (QMJ). In this study, we examine kinematic consequences of the IMJ novelty in a freshwater characiform fish, the herbivorous Distichodus sexfasciatus. We combine traditional kinematic approaches with trajectory-based analysis of motion shapes to compare patterns of prey capture movements during substrate biting, the fish's native feeding mode, and suction of prey from the water column. We find that the IMJ enables complex jaw motions and contributes to feeding versatility by allowing the fish to modulate its kinematics in response to different prey and to various scenarios of jaw-substrate interaction. Implications of the IMJ include context-dependent movements of lower versus upper jaws, enhanced lower jaw protrusion, and the ability to maintain contact between the teeth and substrate throughout the jaw closing or biting phase of the motion. The IMJ in D. sexfasciatus appears to be an adaptation for removing attached benthic prey, consistent with its function in other groups that have evolved the joint. This study builds on our understanding of the role of the IMJ during prey capture and provides insights into broader implications of the innovative trait.

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.

Reevaluating claims of ecological speciation in Halichoeres bivittatus.

Allopatry has traditionally been viewed as the primary driver of speciation in marine taxa, but the geography of the marine environment and the larval dispersal capabilities of many marine organisms render this view somewhat questionable. In marine fishes, one of the earliest and most highly cited empirical examples of ecological speciation with gene flow is the slippery dick wrasse, Halichoeres bivittatus. Evidence for this cryptic or incipient speciation event was primarily in the form of a deep divergence in a single mitochondrial locus between the northern and southern Gulf of Mexico, combined with a finding that these two haplotypes were associated with different habitat types ("tropical" vs. "subtropical") in the Florida Keys and Bermuda, where they overlap. Here, we examine habitat assortment in the Florida Keys using a broader sampling of populations and habitat types than were available for the original study. We find no evidence to support the claim that haplotype frequencies differ between habitat types, and little evidence to support any differences between populations in the Keys. These results undermine claims of ecological speciation with gene flow in Halichoeres bivittatus. Future claims of this type should be supported by multiple lines of evidence that illuminate potential mechanisms and allow researchers to rule out alternative explanations for spatial patterns of genetic differences.

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.

A Multifunction Trade-Off has Contrasting Effects on the Evolution of Form and Function.

Trade-offs caused by the use of an anatomical apparatus for more than one function are thought to be an important constraint on evolution. However, whether multifunctionality suppresses diversification of biomechanical systems is challenged by recent literature showing that traits more closely tied to trade-offs evolve more rapidly. We contrast the evolutionary dynamics of feeding mechanics and morphology between fishes that exclusively capture prey with suction and multifunctional species that augment this mechanism with biting behaviors to remove attached benthic prey. Diversification of feeding kinematic traits was, on average, over 13.5 times faster in suction feeders, consistent with constraint on biters due to mechanical trade-offs between biting and suction performance. Surprisingly, we found that the evolution of morphology contrasts directly with these differences in kinematic evolution, with significantly faster rates of evolution of head shape in biters. This system provides clear support for an often postulated, but rarely confirmed prediction that multifunctionality stifles functional diversification, while also illustrating the sometimes weak relationship between form and function. [Form-function evolution; geometric morphometrics; kinematic evolution; macroevolution; Ornstein-Uhlenbeck; RevBayes; suction feeding].

Anatomical basis of diverse jaw protrusion directionality in ponyfishes (Family Leiognathidae).

Protrusion of the oral jaws is a key morphological innovation that enhances feeding performance in fishes. The mechanisms of protrusion and the basis of variation in its magnitude are well studied, but little attention has been paid to the functional morphology of protrusion directionality, despite wide variation among teleost species from slightly dorsal to strongly ventral. Ponyfishes (Leiognathidae) comprise a group of 52 species that exhibit striking diversity in the directionality of jaw protrusion, providing a promising system for exploring its underlying basis in a single clade. We examined the anatomical basis of protrusion directionality by measuring eight traits associated with the size and positioning of oral jaw bones. Measurements were made on cleared and stained specimens of 20 ponyfish species, representing every major lineage within the family. Species fell into three nonoverlapping clusters with respect to directionality including dorsal, rostral, and ventral protruders. A key correlate of protrusion direction is the anterior-posterior position of the articular-quadrate jaw joint. As the joint position moves from a posterior to a more anterior location, the orientation of the relaxed mandible rotates from an almost horizontal resting position to an upright vertical posture. Abduction of the mandible from the horizontal position results in ventrally directed protrusion, while the more upright mandible rotates to a position that maintains dorsal orientation. The resting orientation of the premaxilla and maxilla, thus, vary consistently with protrusion direction. Mouth size, represented by length of the mandible and maxilla, is a second major axis of variation in ponyfishes that is independent of variation in protrusion directionality.

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.

Correlated Evolution of Sex Allocation and Mating System in Wrasses and Parrotfishes.

In accordance with predictions of the size-advantage model, comparative evidence confirms that protogynous sex change is lost when mating behavior is characterized by weak size advantage. However, we lack comparative evidence supporting the adaptive significance of sex change. Specifically, it remains unclear whether increasing male size advantage induces transitions to protogynous sex change across species, as it can within species. We show that in wrasses and parrotfishes (Labridae) the evolution of protogynous sex change is correlated with polygynous mating and that the degree of male size advantage expressed by polygynous species influences transitions between different types of protogynous sex change. Phylogenetic reconstructions reveal strikingly similar patterns of sex allocation and mating system evolution with comparable lability. Despite the plasticity of sex-determination mechanisms in labrids, transitions trend toward monandry (all males derived from sex-changed females), with all observed losses of protogyny accounted for by shifts in the timing of sex change to prematuration. Likewise, transitions in mating system trend from the ancestral condition of lek-like polygyny toward greater male size advantage, characteristic of haremic polygyny. The results of our comparative analyses are among the first to confirm the adaptive significance of sex change as described by the size-advantage model.

Decoupled jaws promote trophic diversity in cichlid fishes.

Functional decoupling of oral and pharyngeal jaws is widely considered to have expanded the ecological repertoire of cichlid fishes. But, the degree to which the evolution of these jaw systems is decoupled and whether decoupling has impacted trophic diversification remains unknown. Focusing on the large Neotropical radiation of cichlids, we ask whether oral and pharyngeal jaw evolution is correlated and how their evolutionary rates respond to feeding ecology. In support of decoupling, we find relaxed evolutionary integration between the two jaw systems, resulting in novel trait combinations that potentially facilitate feeding mode diversification. These outcomes are made possible by escaping the mechanical trade-off between force transmission and mobility, which characterizes a single jaw system that functions in isolation. In spite of the structural independence of the two jaw systems, results using a Bayesian, state-dependent, relaxed-clock model of multivariate Brownian motion indicate strongly aligned evolutionary responses to feeding ecology. So, although decoupling of prey capture and processing functions released constraints on jaw evolution and promoted trophic diversity in cichlids, the natural diversity of consumed prey has also induced a moderate degree of evolutionary integration between the jaw systems, reminiscent of the original mechanical trade-off between force and mobility.

Head Shape Modulates Diversification of a Classic Cichlid Pharyngeal Jaw Innovation.

Functional innovations are often invoked to explain the uneven distribution of ecological diversity. Innovations may provide access to new adaptive zones by expanding available ecological opportunities and may serve as catalysts of adaptive radiation. However, diversity is often unevenly distributed within clades that share a key innovation, highlighting the possibility that the impact of the innovation is mediated by other traits. Pharyngognathy is a widely recognized innovation of the pharyngeal jaws that enhances the ability to process hard and tough prey in several major radiations of fishes, including marine wrasses and freshwater cichlids. We explored diversification of lower pharyngeal jaw shape, a key feature of pharyngognathy, and the extent to which it is influenced by head shape in Neotropical cichlids. While pharyngeal jaw shape was unaffected by either head length or head depth, its disparity declined dramatically with increasing head width. Head width also predicted the rate of pharyngeal jaw evolution such that higher rates were associated with narrow heads. Wide heads are associated with exploiting prey that require intense processing by pharyngeal jaws that have expanded surfaces for the attachment of enlarged muscles. However, we show that a wide head constrains access to adaptive peaks associated with several trophic roles. A constraint on the independent evolution of pharyngeal jaw and head shape may explain the uneven distribution of ecological diversity within a clade that shares a major functional innovation.

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.

Geography of speciation affects rate of trait divergence in haemulid fishes.

Speciation and the interactions between recently diverged species are thought to be major causes of ecological and morphological divergence in evolutionary radiations. Here, we explore the extent to which geographical overlap and time since speciation may promote divergence in marine species, which represent a small fraction of currently published studies about the patterns and processes of speciation. A time-calibrated molecular phylogeny of New World haemulid fishes, a major radiation of reef and shore fishes in the tropical West Atlantic and East Pacific, reveals 21 sister species pairs, of which eight are fully sympatric and 13 are allopatric. Sister species comparisons show a non-significant relation between most of the phenotypic traits and time since divergence in allopatric taxa. Additionally, we find no difference between sympatric and allopatric pairs in the rate of divergence in colour pattern, overall body shape, or functional morphological traits associated with locomotion or feeding. However, sympatric pairs show a significant decrease in the rate of divergence in all of these traits with increasing time since their divergence, suggesting an elevated rate of divergence at the time of speciation, the effect of which attenuates as divergence time increases. Our results are consistent with an important role for geographical overlap driving phenotypic divergence early in the speciation process, but the lack of difference in rates between sympatric and allopatric pairs indicates that the interactions between closely related species are not dominant drivers of this divergence.

Reef fish functional traits evolve fastest at trophic extremes.

Trophic ecology is thought to exert a profound influence on biodiversity, but the specifics of the process are rarely examined at large spatial and evolutionary scales. We investigate how trophic position and diet breadth influence functional trait evolution in one of the most species-rich and complex vertebrate assemblages, coral reef fishes, within a large-scale phylogenetic framework. We show that, in contrast with established theory, functional traits evolve fastest in trophic specialists with narrow diet breadths at both very low and high trophic positions. Top trophic level specialists exhibit the most functional diversity, while omnivorous taxa with intermediate trophic positions and wide diet breadth have the least functional diversity. Our results reveal the importance of trophic position in shaping evolutionary dynamics while simultaneously highlighting the incredible trophic and functional diversity present in coral reef fish assemblages.

Adaptive radiation in labrid fishes: A central role for functional innovations during 65 My of relentless diversification.

Early burst patterns of diversification have become closely linked with concepts of adaptive radiation, reflecting interest in the role of ecological opportunity in modulating diversification. But, this model has not been widely explored on coral reefs, where biodiversity is exceptional, but many lineages have high dispersal capabilities and a pan-tropical distribution. We analyze adaptive radiation in labrid fishes, arguably the most ecologically dominant and diverse radiation of fishes on coral reefs. We test for time-dependent speciation, trophic diversification, and origination of 15 functional innovations, and early bursts in a series of functional morphological traits associated with feeding and locomotion. We find no evidence of time-dependent or early burst evolution. Instead, the pace of speciation, ecological diversification, and trait evolution has been relatively constant. The origination of functional innovations has slowed over time, although few arose early. The labrid radiation seems to have occurred in response to extensive and still increasing ecological opportunity, but within a rich community of antagonists that may have prevented abrupt diversification. Labrid diversification is closely tied to a series of substantial functional innovations that individually broadened ecological diversity, ultimately allowing them to invade virtually every trophic niche held by fishes on coral reefs.