Beaks promote rapid morphological diversification along distinct evolutionary trajectories in labrid fishes (Eupercaria: Labridae).

The upper and lower jaws of some wrasses (Eupercaria: Labridae) possess teeth that have been coalesced into a strong durable beak that they use to graze on hard coral skeletons, hard-shelled prey, and algae, allowing many of these species to function as important ecosystem engineers in their respective marine habitats. While the ecological impact of the beak is well understood, questions remain about its evolutionary history and the effects of this innovation on the downstream patterns of morphological evolution. Here we analyze 3D cranial shape data in a phylogenetic comparative framework and use paleoclimate modeling to reconstruct the evolution of the labrid beak across 205 species. We find that wrasses evolved beaks three times independently, once within odacines and twice within parrotfishes in the Pacific and Atlantic Oceans. We find an increase in the rate of shape evolution in the Scarus+Chlorurus+Hipposcarus (SCH) clade of parrotfishes likely driven by the evolution of the intramandibular joint. Paleoclimate modeling shows that the SCH clade of parrotfishes rapidly morphologically diversified during the middle Miocene. We hypothesize that possession of a beak in the SCH clade coupled with favorable environmental conditions allowed these species to rapidly morphologically diversify.

How to tuna fish: constraint, convergence, and integration in the neurocranium of pelagiarian fishes.

Morphological evolution of the vertebrate skull has been explored across a wide range of tetrapod clades using geometric morphometrics, but the application of these methods to teleost fishes, accounting for roughly half of all vertebrate species, has been limited. Here we present the results of a study investigating 3D morphological evolution of the neurocranium across 114 species of Pelagiaria, a diverse clade of open-ocean teleost fishes that includes tuna and mackerel. Despite showing high shape disparity overall, taxa from all families fall into three distinct morphological clusters. Convergence in shape within clusters is high, and phylogenetic signal in shape data is significant but low. Neurocranium shape is significantly correlated with body elongation and significantly but weakly correlated with size. Diet and habitat depth are weakly correlated with shape, and nonsignificant after accounting for phylogeny. Evolutionary integration in the neurocranium is high, suggesting that convergence in skull shape and the evolution of extreme morphologies are associated with the correlated evolution of neurocranial elements. These results suggest that shape evolution in the pelagiarian neurocranium reflects the extremes in elongation found in body shape but is constrained along relatively few axes of variation, resulting in repeated evolution toward a restricted range of morphologies.

Untangling the relationship between developmental and evolutionary integration.

Patterns of integration and modularity among organismal traits are prevalent across the tree of life, and at multiple scales of biological organization. Over the past several decades, researchers have studied these patterns at the developmental, and evolutionary levels. While their work has identified the potential drivers of these patterns at different scales, there appears to be a lack of consensus on the relationship between developmental and evolutionary integration. Here, we review and summarize key studies and build a framework to describe the conceptual relationship between these patterns across organismal scales and illustrate how, and why some of these studies may have yielded seemingly conflicting outcomes. We find that among studies that analyze patterns of integration and modularity using morphological data, the lack of consensus may stem in part from the difficulty of fully disentangling the developmental and functional causes of integration. Nonetheless, in some empirical systems, patterns of evolutionary modularity have been found to coincide with expectations based on developmental processes, suggesting that in some circumstances, developmental modularity may translate to evolutionary modularity. We also advance an extension to Hallgrímsson et al.'s palimpsest model to describe how patterns of trait modularity may shift across different evolutionary scales. Finally, we also propose some directions for future research which will hopefully be useful for investigators interested in these issues.

Mosaic Evolution of the Skull in Labrid Fishes Involves Differences in Both Tempo and Mode of Morphological Change.

Modularity is a ubiquitous feature of organismal design that plays an important role in structuring patterns of morphological diversification. Modularity can facilitate evolutionary changes by allowing subsets of traits to coevolve as integrated units and follow quasi-independent evolutionary trajectories, a pattern that may be particularly consequential in the case of highly complex morphological structures. Here we examine modularity in a complex and highly kinetic structure, the teleost skull, and ask if a modular organization of the skull has influenced the diversification dynamics of the shapes of its osteological components across the labrid phylogeny. We compiled one of the largest 3D morphological data sets of fishes to date and used geometric morphometrics to quantify patterns of cranial shape evolution across 184 species of wrasses (Labridae). We then tested several hypotheses of modularity inspired by functional and developmental relationships between cranial bones and compared phenotypic rates among modules. We also compared the fit of models of trait evolution for the entire skull and the various articulated bones that it comprises. Our analyses indicated strong support for a 2-module hypothesis, one that encompasses the oral and pharyngeal jaws and another module comprised of the neurocranium, hyoid apparatus, and operculum. This functional hypothesis yielded one of the highest significant rate differentials across modules, yet we also found that the best-fitting models of trait evolution differed among skull bones. These results suggest that modularity can influence morphological diversification in complex biological structures via differences in both the tempo and mode of evolutionary change. [3D geometric morphometrics, cranial morphology, evolutionary modularity, Labridae, phenotypic rates, structural complexity.].

Burrowing constrains patterns of skull shape evolution in wrasses.

The evolution of behavioral and ecological specialization can have marked effects on the tempo and mode of phenotypic evolution. Head-first burrowing has been shown to exert powerful selective pressures on the head and body shapes of many vertebrate and invertebrate taxa. In wrasses, burrowing behaviors have evolved multiple times independently, and are commonly used in foraging and predator avoidance behaviors. While recent studies have examined the kinematics and body shape morphology associated with this behavior, no study to-date has examined the macroevolutionary implications of burrowing on patterns of phenotypic diversification in this clade. Here, we use three-dimensional geometric morphometrics and phylogenetic comparative methods to study the evolution of skull shape in fossorial wrasses and their relatives. We test for skull shape differences between burrowing and non burrowing wrasses and evaluate hypotheses of shape convergence among the burrowing wrasses. We also quantify rates of skull shape evolution between burrowing and non burrowing wrasses to test for whether burrowing constrains or accelerates rates of skull shape evolution in this clade. We find that while burrowing and non burrowing wrasses exhibit similar degrees of morphological disparity, for burrowing wrasses, it took nearly twice as long to amass this disparity. Furthermore, while the disparities between groups are evenly matched, we find that most burrowing species are confined to a particular region of shape space with most species exhibiting narrower heads than many non-burrowing species. These results suggest head-first burrowing constrains patterns of skull shape diversification in wrasses by potentially restricting the range of phenotypes that can perform this behavior.

Tooth replacement and attachment morphology in the Pacific Leaping Blenny, Alticus arnoldorum (Blenniiformes: Blenniidae: Salariini) with a discussion on tooth function.

Modes of teleost tooth replacement and attachment have historically been described using discrete classification systems that categorize major patterns across taxa. While useful, these discrete classification schemes understate teleost tooth diversity. The "unattached" dentition of salariin combtooth blennies (Blenniiformes: Blenniidae: Salariini) is frequently overlooked due to its perceived complexity, so we examined the Pacific Leaping Blenny, Alticus arnoldorum, to describe this complex morphology. Using a range of methods including histology, SEM, microCT scanning, and clearing and staining, we establish a descriptive model of tooth replacement for A. arnoldorum. We then use our descriptive model of tooth replacement to propose a hypothesis of tooth function in salariin blennies. Our results show that A. arnoldorum exhibits grouped, extraosseous replacement of feeding teeth upon a discontinuous, permanent dental lamina. We also find that tooth replacement occurs within lip tissue that is laterally displaced from the distal margins of the jaw bones, a process previously undocumented in teleost fish. Feeding teeth attach to the dentigerous bone via a primary attachment mode consisting of a continuous collagen band at the posterior base of the teeth, and a secondary attachment mode consisting of epithelial cells. Alticus arnoldorum presents novel modes of tooth replacement and attachment that challenge historical classification modes of teleost dentition. Our descriptive tooth replacement model also provides a reliable framework to propose hypotheses of tooth function that can be applied in future comparative studies on salariin blennies and other long-toothed teleosts to further elucidate the functional role of long-toothed fishes in aquatic ecosystems.

Integration drives rapid phenotypic evolution in flatfishes.

Evolutionary innovations are scattered throughout the tree of life, and have allowed the organisms that possess them to occupy novel adaptive zones. While the impacts of these innovations are well documented, much less is known about how these innovations arise in the first place. Patterns of covariation among traits across macroevolutionary time can offer insights into the generation of innovation. However, to date, there is no consensus on the role that trait covariation plays in this process. The evolution of cranial asymmetry in flatfishes (Pleuronectiformes) from within Carangaria was a rapid evolutionary innovation that preceded the colonization of benthic aquatic habitats by this clade, and resulted in one of the most bizarre body plans observed among extant vertebrates. Here, we use three-dimensional geometric morphometrics and a phylogenetic comparative toolkit to reconstruct the evolution of skull shape in carangarians, and quantify patterns of integration and modularity across the skull. We find that the evolution of asymmetry in flatfishes was a rapid process, resulting in the colonization of novel trait space, that was aided by strong integration that coordinated shape changes across the skull. Our findings suggest that integration plays a major role in the evolution of innovation by synchronizing responses to selective pressures across the organism.

A redescription of deep-channel ghost knifefish, Sternarchogiton preto (Gymnotiformes: Apteronotidae), with assignment to a new genus

From a study of morphological and molecular datasets we determine that a species originally described as Sternarchogiton preto does not form a monophyletic group with the other valid species of Sternarchogiton including the type species, S. nattereri. Previously-published phylogenetic analyses indicate that this species is sister to a diverse clade comprised of six described apteronotid genera. We therefore place it into a new genus diagnosed by the presence of three cranial fontanels, first and second infraorbital bones independent (not fused), the absence of an ascending process on the endopterygoid, and dark brown to black pigments over the body surface and fins membranes. We additionally provide a redescription of this enigmatic species with an emphasis on its osteology, and provide the first documentation of secondary sexual dimorphism in this species.(AU)

RESUMO Através de um estudo com dados morfológicos e moleculares, nós propomos que a espécie originalmente descrita como Sternarchogiton preto não forma um grupo monofilético com outras espécies válidas de Sternarchogiton incluindo a espécie-tipo, S. nattereri. Análises filogenéticas anteriormente publicadas indicam que essa espécie é irmã de um clado diverso contendo seis gêneros descritos de Apteronotidae. Nós então a alocamos em um novo gênero diagnosticado pela presença de três fontanelas craniais, primeiro e segundo ossos infraorbitais independentes (não fusionados), ausência de um processo ascendente do endopterigoide e pigmentação marrom-escura à negra sobre a superfície do corpo e membranas das nadadeiras. Adicionalmente, nós realizamos a redescrição dessa enigmática espécie com ênfase na sua osteologia, e fazemos o primeiro registro de dimorfismo sexual secundário nessa espécie.(AU)

Do Coral Reefs Promote Morphological Diversification? Exploration of Habitat Effects on Labrid Pharyngeal Jaw Evolution in the Era of Big Data.

Coral reefs are complex marine habitats that have been hypothesized to facilitate functional specialization and increased rates of functional and morphological evolution. Wrasses (Labridae: Percomorpha) in particular, have diversified extensively in these coral reef environments and have evolved adaptations to further exploit reef-specific resources. Prior studies have found that reef-dwelling wrasses exhibit higher rates of functional evolution, leading to higher functional variation than in non-reef dwelling wrasses. Here, we examine this hypothesis in the lower pharyngeal tooth plate of 134 species of reef and non-reef-associated labrid fishes using high-resolution morphological data in the form of micro-computed tomography scans and employing three-dimensional geometric morphometrics to quantify shape differences. We find that reef-dwelling wrasses do not differ from non-reef-associated wrasses in morphological disparity or rates of shape evolution. However, we find that some reef-associated species (e.g., parrotfishes and tubelips) exhibit elevated rates of pharyngeal jaw shape evolution and have colonized unique regions of morphospace. These results suggest that while coral reef association may provide the opportunity for specialization and morphological diversification, species must still be able to capitalize on the ecological opportunities to invade novel niche space, and that these novel invasions may prompt rapid rates of morphological evolution in the associated traits that allow them to capitalize on new resources.

Bony Patchwork: Mosaic Patterns of Evolution in the Skull of Electric Fishes (Apteronotidae: Gymnotiformes).

Mosaic evolution refers to the pattern whereby different organismal traits exhibit differential rates of evolution typically due to reduced levels of trait covariation through deep time (i.e., modularity). These differences in rates can be attributed to variation in responses to selective pressures between individual traits. Differential responses to selective pressures also have the potential to facilitate functional specialization, allowing certain traits to track environmental stimuli more closely than others. The teleost skull is a multifunctional structure comprising a complex network of bones and thus an excellent system for which to study mosaic evolution. Here we construct an ultrametric phylogeny for a clade of Neotropical electric fishes (Apteronotidae: Gymnotiformes) and use three-dimensional geometric morphometrics to investigate patterns of mosaic evolution in the skull and jaws. We find strong support for a developmental, three-module hypothesis that consists of the face, braincase, and mandible, and we find that the mandible has evolved four times faster than its neighboring modules. We hypothesize that the functional specialization of the mandible in this group of fishes has allowed it to outpace the face and braincase and evolve in a more decoupled manner. We also hypothesize that this pattern of mosaicism may be widespread across other clades of teleost fishes.

Why the short face? Developmental disintegration of the neurocranium drives convergent evolution in neotropical electric fishes.

Convergent evolution is widely viewed as strong evidence for the influence of natural selection on the origin of phenotypic design. However, the emerging evo-devo synthesis has highlighted other processes that may bias and direct phenotypic evolution in the presence of environmental and genetic variation. Developmental biases on the production of phenotypic variation may channel the evolution of convergent forms by limiting the range of phenotypes produced during ontogeny. Here, we study the evolution and convergence of brachycephalic and dolichocephalic skull shapes among 133 species of Neotropical electric fishes (Gymnotiformes: Teleostei) and identify potential developmental biases on phenotypic evolution. We plot the ontogenetic trajectories of neurocranial phenotypes in 17 species and document developmental modularity between the face and braincase regions of the skull. We recover a significant relationship between developmental covariation and relative skull length and a significant relationship between developmental covariation and ontogenetic disparity. We demonstrate that modularity and integration bias the production of phenotypes along the brachycephalic and dolichocephalic skull axis and contribute to multiple, independent evolutionary transformations to highly brachycephalic and dolichocephalic skull morphologies.

Fluctuations in Evolutionary Integration Allow for Big Brains and Disparate Faces.

In theory, evolutionary modularity allows anatomical structures to respond differently to selective regimes, thus promoting morphological diversification. These differences can then influence the rate and direction of phenotypic evolution among structures. Here we use geometric morphometrics and phenotypic matrix statistics to compare rates of craniofacial evolution and estimate evolvability in the face and braincase modules of a clade of teleost fishes (Gymnotiformes) and a clade of mammals (Carnivora), both of which exhibit substantial craniofacial diversity. We find that the face and braincase regions of both clades display different degrees of integration. We find that the face and braincase evolve at similar rates in Gymnotiformes and the reverse in Carnivora with the braincase evolving twice as fast as the face. Estimates of evolvability and constraints in these modules suggest differential responses to selection arising from fluctuations in phylogenetic integration, thus influencing differential rates of skull-shape evolution in these two clades.

Taxonomic revision of the deep channel electric fish genus Sternarchella (Teleostei: Gymnotiformes: Apteronotidae), with descriptions of two new species

This paper provides a taxonomic revision of the Neotropical electric fish genus Sternarchella, with redescriptions of seven valid species and descriptions of two new species. A maximum parsimony analysis of 76 morphological characters from seven ingroup and seven outgroup taxa recovered a non-monophyletic Sternarchella, in which a clade comprising two species with a ventral mouth (S. orinoco + S. sima) is the sister group to a clade comprising seven species that possess a terminal or superior mouth. Nested within this higher-diversity clade is the genus Magosternarchus (recognized herein as a junior synonym of Sternarchella) comprising M. duccis and M. raptor. The Magosternarchus clade forms a polytomy with S. orthos and S. schotti. Sternarchella calhamazon + a new species from the upper Río Madeira (sister species to S. calhamazon), and a new larger-bodied species from the central and upper Río Amazonas also form a clade. Sternarchella orthos is distributed in both the Amazon and Orinoco basins, where it exhibits considerable phenotypic diversity. Sternarchella orthos includes most specimens from the Amazon formerly assigned to the nominal species S. terminalis (recognized herein as a junior synonym of S. schotti).(AU)

Este artigo propõe uma revisão taxonômica do gênero Neotropical de peixe-elétrico Sternarchella, incluindo a redescrição de sete espécies válidas e duas novas espécies. Análise de máxima parcimônia com 76 caracteres morfológicos e amostragem de sete grupos internos e sete grupos externos indica que Sternarchella não constitui grupo monofilético, sendo um clado composto por duas espécies com bocas ventrais (S. orinoco + S. sima) e outro com sete espécies com bocas terminais ou superiores. Dentro deste último clado estão as espécies do gênero Magosternarchus (reconhecido aqui como um sinônimo júnior de Sternarchella): M. duccis e M. raptor. O clado de Magosternarchus forma uma politomia com S. orthos e S. schotti. Sternarchella calhamazon + uma nova espécie do alto rio Madeira (espécie irmã de S. calhamazon) e uma nova espécie de corpo maior do rio Amazonas central e superior também formam um clado. Sternarchella orthos está distribuída nos rios amazônicos e no Orinoco, onde apresenta elevada diversidade fenotípica. Sternarchella orthos inclui a maioria dos espécimes do rio Amazonas anteriormente atribuídos à S. terminalis (considerada neste estudo como sinônimo júnior de S. schotti).(AU)