A combined morphometric and phylogenetic analysis of an ecomorphological trend: pelagization in Antarctic fishes (Perciformes: Nototheniidae)

The Antarctic fish family Nototheniidae (Perciformes) presumably originated from a benthic ancestor, and several lineages have evolved to live or at least feed in the water column, a trend called pelagization. Here, we use information on phylogeny, allometric growth, and diet composition for an integrated analysis of morphological and ecological diversification in this group, mainly focusing on the subfamilies Trematominae and Pleuragramminae. A phylogenetic analysis of data published in earlier systematic studies produced eight equally parsimonious trees, all indicating that several previously recognized taxa are paraphyletic. These phylogenetic trees all suggest multiple origins of pelagic life styles. Multivariate morphometric analyses including nine species showed that juveniles and adults grow according to a common pattern of ontogenetic allometry. The morphometric differences among species are mosdy the result of lateral transpositions of the growth trajectories, indicating that embryonic and larval development is more important as a determinant of morphological variation than allometric growth as juveniles and adults. We studied patterns of interspecific variation with principal components and the covariation between morphometric variables and food composition with a partial least-squares analysis. Both analyses revealed a gradient from benthic to pelagic foragers. Measurements of structures involved in swimming have a prominent role in these analyses, suggesting adaptive evolution of these traits. Tracing morphometric traits on the phylogenetic trees revealed a considerable amount of evolutionary plasticity, showing that species related phylogenetically need not be morphologically similar, but can diverge considerably, perhaps as a response to natural selection and adaptation to different habitats and foraging modes. In accordance, a test of phylogenetically independent contrasts showed that bursts of increased morphological change accompanied habitat shifts.     

Testing the evolutionary constraints of metamorphosis: The ontogeny of head shape in Triturus newts

In vertebrates with complex, biphasic, life cycles, larvae have a distinct morphology and ecological preferences compared to metamorphosed juveniles and adults. In amphibians, abrupt and rapid metamorphic changes transform aquatic larvae to terrestrial juveniles. The main aim of this study is to test whether, relative to larval stages, metamorphosis (1) resets the pattern of variation between ontogenetic stages and species, (2) constrains intraspecific morphological variability, and (3) similar to the “hour‐glass” model reduces morphological disparity. We explore postembryonic ontogenetic trajectories of head shape (from hatching to completed metamorphosis) of two well‐defined, morphologically distinct Triturus newts species and their F1 hybrids. Variation in head shape is quantified and compared on two levels: dynamic (across ontogenetic stages) and static (at a particular stage). Our results show that the ontogenetic trajectories diverge early during development and continue to diverge throughout larval stages and metamorphosis. The high within‐group variance and the largest disparity level (between‐group variance) characterize the metamorphosed stage. Hence, our results indicate that metamorphosis does not canalize head shape variation generated during larval development and that metamorphosed phenotype is not more constrained relative to larval ones. Therefore, metamorphosis cannot be regarded as a developmental constraint, at least not for salamander head shape.     

Mutualistic mimicry enhances species diversification through spatial segregation and extension of the ecological niche space

Species richness varies among clades, yet the drivers of diversification creating this variation remain poorly understood. While abiotic factors likely drive some of the variation in species richness, ecological interactions may also contribute. Here, we examine one class of potential contributors to species richness variation that is particularly poorly understood: mutualistic interactions. We aim to elucidate large‐scale patterns of diversification mediated by mutualistic interactions using a spatially explicit population‐based model. We focus on mutualistic Müllerian mimicry between conspicuous toxic prey species, where convergence in color patterns emerges from predators' learning process. To investigate the effects of Müllerian mimicry on species diversification, we assume that some speciation events stem from shifts in ecological niches, and can also be associated with shift in mimetic color pattern. Through the emergence of spatial mosaics of mimetic color patterns, Müllerian mimicry constrains the geographical distribution of species and allows different species occupying similar ecological niches to exist simultaneously in different regions. Müllerian mimicry and the resulting spatial segregation of mimetic color patterns thus generate more balanced phylogenetic trees and increase overall species diversity. Our study sheds light on complex effects of Müllerian mimicry on ecological, spatial, and phylogenetic diversification.     

Ontogeny, phylogeny, and morphology in anuran larvae: morphometric analysis of cranial development and evolution in Rana tadpoles (Anura: Ranidae)

Comparative studies of chondrocranial morphology in larval anurans are typically qualitative in nature, focusing primarily on discrete variation or gross differences in the size or shape of individual structures. Detailed data on chondrocranial allometry are currently limited to only two species, Rana sylvatica and Bufo americanus. This study uses geometric morphometric and multivariate statistical analyses to examine interspecific variation in both larval chondrocranial shape and patterns of ontogenetic allometry among six species of Rana. Variation is interpreted within the context of hypothesized phylogenetic relationships among these species. Canonical variates analyses of geometric morphometric datasets indicate that species can be clearly discriminated based on chondrocranial shape, even when whole ontogenies are included in the analysis. Ordinations and cluster analyses based on chondrocranial shape data indicate the presence of three primary groupings (R. sylvatica; R. catesbeiana + R. clamitans; and R. palustris + R. pipiens + R. sphenocephala), and patterns of similarity closely reflect phylogenetic relationships. Analysis of chondrocranial allometry reveals that some patterns are conserved across all species (e.g., most measurements scale with negative allometry, those associated with the posterior palatoquadrate tend to scale with isometry or positive allometry). Ontogenetic scaling along similar allometric trajectories, lateral transpositions of individual trajectories, and variable allometric relationships all contribute to shape differences among species. Overall patterns of similarity among ontogenetic trajectories also strongly reflect phylogenetic relationships. Thus, this study demonstrates a tight link between ontogeny, phylogeny, and morphology, and highlights the importance of including both ontogenetic and phylogenetic data in studies of chondrocranial evolution in larval anurans.     

Where to Live? How Morphology and Evolutionary History Predict Microhabitat Choice by Tropical Tadpoles

Tadpoles have diverse morphologies and occupy diverse habitats. The morphological differences between tadpoles can be represented by linear and geometric measurements and used to explain the organization of tadpole assemblages. However, the effects of evolutionary history must be isolated from the morphological differences before we can determine which patterns result from the use and sharing of common ecological resources. Here, we aimed to determine how morphological similarities and phylogenetic distances affect microhabitat choice by tadpoles. We analyzed the tadpoles of 101 anuran species and classified them according to ecomorphological guild, habitat use, position in the water column, and floor substrate. We used geometric and traditional morphometric approaches to describe the morphological variation among tadpoles and calculated the patristic distance for each species. Afterwards, we used morphometric and phylogenetic matrices as predictors of the variance in the ecological matrix, using a partial redundancy analysis. When we used traditional morphometric data, phylogeny explained a large amount of the ecological variation. By contrast, when we used geometric morphometric data, morphology and phylogeny explained similar amounts of the ecological variation, showing that the technique used to extract morphological variation affects the results. We provide evidence that both morphology, as a surrogate for contemporary factors, and evolutionary inertia are important in determining the behavior of tadpoles. Thus, niche conservatism can be important in modeling the behavior of tadpoles, but does not explain all the preferences of tadpoles.     

Larval development ofNeopisosoma neglectum werding, 1986 (Decapoda: Anomura: Porcellanidae) under laboratory conditions

The complete larval development of the porcellanid crabNeopisosoma negluctum Werding, 1986, was studied under laboratory conditions. At 27°C, the megalopa appeared after 9 days. The development consists of a transitory prezoea, two zoeal stages and a megalopa stage. The larvae exhibit telsonal features which places them in thePetrolisthes-group of porcellanid larvae. Larval morphology gives no additional support for the status ofNeopisosoma as an independent genus.     

A Large-Scale Pattern of Ontogenetic Shape Change in Ray-Finned Fishes

Fishes exhibit a remarkable diversity of body shape as adults; however, it is unknown whether this diversity is reflected in larval stage morphology. Here we investigate the relationship between larval and adult body shape as expressed by body elongation. We surveyed a broad range of ray-finned fish species and compared body shape at larval and adult stages. Analysis shows that the vast majority of fish are more elongate at the larval stage than at the adult stage, and that adults display greater interspecies variation than larvae. We found that the superorder Elompomorpha is unique because many species within the group do not follow the observed elongation trends. These results indicate that much of the diversity observed in adults is achieved in post-larval stages. We suggest that larval morphology is subject to common constraints across the phylogeny.     

The tarsal‐metatarsal complex of caviomorph rodents: Anatomy and functional‐adaptive analysis

Caviomorph rodents represent a major adaptive radiation of Neotropical mammals. They occupy a variety of ecological niches, which is also reflected in their wide array of locomotor behaviors. It is expected that this radiation would be mirrored by an equivalent disparity of tarsal‐metatarsal morphology. Here, the tarsal‐metatarsal complex of Erethizontidae, Cuniculidae, Dasyproctidae, Caviidae, Chinchillidae, Octodontidae, Ctenomyidae, and Echimyidae was examined, in order to evaluate its anatomical variation and functional‐adaptive relevance in relation to locomotor behaviors. A qualitative study in functional morphology and a geometric morphometric analysis were performed. We recognized two distinct tarsal‐metatarsal patterns that represent the extremes of anatomical variation in the foot. The first, typically present in arboreal species, is characterized by features that facilitate movements at different levels of the tarsal‐metatarsal complex. The second pattern, typically present in cursorial caviomorphs, has a set of features that act to stabilize the joints, improve the interlocking of the tarsal bones, and restrict movements to the parasagittal plane. The morphological disparity recognized in this study seems to result from specific locomotor adaptations to climb, dig, run, jump and swim, as well as phylogenetic effects within and among the groups studies.     

The Good,the Bad,and the Ugly: The Influence of Skull Reconstructions and Intraspecific Variability in Studies of Cranial Morphometrics in Theropods and Basal Saurischians

Several studies investigating macroevolutionary skull shape variation in fossil reptiles were published recently, often using skull reconstructions taken from the scientific literature. However, this approach could be potentially problematic, because skull reconstructions might differ notably due to incompleteness and/or deformation of the material. Furthermore, the influence of intraspecific variation has usually not been explored in these studies. Both points could influence the results of morphometric analyses by affecting the relative position of species to each other within the morphospace. The aim of the current study is to investigate the variation in morphometric data between skull reconstructions based on the same specimen, and to compare the results to shape variation occurring in skull reconstructions based on different specimens of the same species (intraspecific variation) and skulls of closely related species (intraspecific variation). Based on the current results, shape variation of different skull reconstructions based on the same specimen seems to have generally little influence on the results of a geometric morphometric analysis, although it cannot be excluded that some erroneous reconstructions of poorly preserved specimens might cause problems occasionally. In contrast, for different specimens of the same species the variation is generally higher than between different reconstructions based on the same specimen. For closely related species, at least with similar ecological preferences in respect to the dietary spectrum, the degree of interspecific variation can overlap with that of intraspecific variation, most probably due to similar biomechanical constraints.     

Form,function and phylogeny: comparative morphometrics of Lake Tanganyika's cichlid tribe Tropheini

Lake Tanganyika's cichlid fishes represent one of the most diverse species assemblages of the world. In this study we focused on the tribe Tropheini which occupies several trophic niches, mostly in rocky habitats. We analysed morphological variation of seventeen closely related species by means of geometric morphometric methods and related these data to ecological characteristics and phylogeny of the study species. It turned out that morphology mostly correlated well with ecological parameters, but not always closely with the degree of the phylogenetic relatedness of the species. Overall, body shapes in the tribe Tropheini are of great evolutionary plasticity, but variation is restricted to particular body parts: the preorbital region once again emerged as a key factor that facilitated their impressive radiation.     

Bat Species Comparisons Based on External Morphology: A Test of Traditional versus Geometric Morphometric Approaches

External morphology is commonly used to identify bats as well as to investigate flight and foraging behavior, typically relying on simple length and area measures or ratios. However, geometric morphometrics is increasingly used in the biological sciences to analyse variation in shape and discriminate among species and populations. Here we compare the ability of traditional versus geometric morphometric methods in discriminating between closely related bat species – in this case European horseshoe bats (Rhinolophidae, Chiroptera) – based on morphology of the wing, body and tail. In addition to comparing morphometric methods, we used geometric morphometrics to detect interspecies differences as shape changes. Geometric morphometrics yielded improved species discrimination relative to traditional methods. The predicted shape for the variation along the between group principal components revealed that the largest differences between species lay in the extent to which the wing reaches in the direction of the head. This strong trend in interspecific shape variation is associated with size, which we interpret as an evolutionary allometry pattern.     

The integrative taxonomic approach reveals host specific species in an encyrtid parasitoid species complex

Integrated taxonomy uses evidence from a number of different character types to delimit species and other natural groupings. While this approach has been advocated recently, and should be of particular utility in the case of diminutive insect parasitoids, there are relatively few examples of its application in these taxa. Here, we use an integrated framework to delimit independent lineages in Encyrtus sasakii (Hymenoptera: Chalcidoidea: Encyrtidae), a parasitoid morphospecies previously considered a host generalist. Sequence variation at the DNA barcode (cytochrome c oxidase I, COI) and nuclear 28S rDNA loci were compared to morphometric recordings and mating compatibility tests, among samples of this species complex collected from its four scale insect hosts, covering a broad geographic range of northern and central China. Our results reveal that Encyrtus sasakii comprises three lineages that, while sharing a similar morphology, are highly divergent at the molecular level. At the barcode locus, the median K2P molecular distance between individuals from three primary populations was found to be 11.3%, well outside the divergence usually observed between Chalcidoidea conspecifics (0.5%). Corroborative evidence that the genetic lineages represent independent species was found from mating tests, where compatibility was observed only within populations, and morphometric analysis, which found that despite apparent morphological homogeneity, populations clustered according to forewing shape. The independent lineages defined by the integrated analysis correspond to the three scale insect hosts, suggesting the presence of host specific cryptic species. The finding of hidden host specificity in this species complex demonstrates the critical role that DNA barcoding will increasingly play in revealing hidden biodiversity in taxa that present difficulties for traditional taxonomic approaches.     

Ecomorphology of a generalist freshwater gastropod: complex relations of shell morphology,habitat, and fecundity

Evolutionary and ecological situations in a species’ native and invasive ranges can be drastically different. This is the case for Potamopyrgus antipodarum Gray (1843) a morphologically highly variable freshwater snail native to New Zealand, where sexual and asexual individuals coexist and experience selective pressure by sterilizing endoparasites. By contrast, only a few asexual lineages have been established in invaded regions around the globe, where parasite infection is extremely rare. We analyzed the ecomorphology of 996 native P. antipodarum in a geometric morphometric framework, using brood size as proxy for fecundity, and mtDNA and nuclear SNPs to account for relatedness and identify reproductive mode. As expected, we found genetic and morphological diversity to be higher in native than in invasive snails investigated previously, but surprisingly no higher morphological diversity in sexual versus asexual individuals. The relationships between shell morphology, habitat, and fecundity were complex. Shape variation was primarily linked to genetic relatedness but specific environmental factors including flow rate induced similar shell shapes. By contrast, shell size was largely explained by environmental factors. Fecundity was correlated with size but showed trade-offs with shape in increasingly extreme conditions. With increasing flow and toward small springs, the trend of shell shape becoming wider was reversed, i.e., snails with narrower shells were brooding more embryos. We concluded that both genetic and environmental contributions to variation in shell morphology in P. antipodarum likely play an important role in the ability of this species to adapt to a wide spectrum of habitats.     

Integrative species delimitation reveals cryptic diversity in the southern Appalachian Antrodiaetus unicolor (Araneae: Antrodiaetidae) species complex

Although species delimitation can be highly contentious, the development of reliable methods to accurately ascertain species boundaries is an imperative step in cataloguing and describing Earth's quickly disappearing biodiversity. Spider species delimitation remains largely based on morphological characters; however, many mygalomorph spider populations are morphologically indistinguishable from each other yet have considerable molecular divergence. The focus of our study, the Antrodiaetus unicolor species complex containing two sympatric species, exhibits this pattern of relative morphological stasis with considerable genetic divergence across its distribution. A past study using two molecular markers, COI and 28S, revealed that A. unicolor is paraphyletic with respect to A. microunicolor. To better investigate species boundaries in the complex, we implement the cohesion species concept and use multiple lines of evidence for testing genetic exchangeability and ecological interchangeability. Our integrative approach includes extensively sampling homologous loci across the genome using a RADseq approach (3RAD), assessing population structure across their geographic range using multiple genetic clustering analyses that include structure , principal components analysis and a recently developed unsupervised machine learning approach (Variational Autoencoder). We evaluate ecological similarity by using large‐scale ecological data for niche‐based distribution modelling. Based on our analyses, we conclude that this complex has at least one additional species as well as confirm species delimitations based on previous less comprehensive approaches. Our study demonstrates the efficacy of genomic‐scale data for recognizing cryptic species, suggesting that species delimitation with one data type, whether one mitochondrial gene or morphology, may underestimate true species diversity in morphologically homogenous taxa with low vagility.     

Caudal vertebral development and morphology in three salamanders with complex life cycles (Ambystoma jeffersonianum, Hemidactylium scutatum, and Desmognathus ocoee)

We describe caudosacral and caudal vertebral morphology across life history stages in three caudate amphibians: Ambystoma jeffersonianum (Ambystomatidae), Desmognathus ocoee (Plethodontidae: Desmognathinae), and Hemidactylium scutatum (Plethodontidae: Plethodontinae). All three species have aquatic larvae, but adults differ in habitat and predator defense strategy. Predator defense includes tail autotomy in D. ocoee and H. scutatum but not A. jeffersonianum. Of the species that autotomize, H. scutatum has a specialized constriction site at the tail base. We investigated whether aquatic larvae exhibit vertebral features similar to those previously described for aquatic adults and examined the effect of metamorphosis, if any, on vertebral morphology and the ontogeny of specialized vertebral features associated with tail autotomy. Interspecific comparisons of cleared-and-stained specimens indicate that vertebral morphology differs dramatically at hatching and that caudosacral and caudal vertebrae undergo continuous ontogenetic change throughout larval, metamorphic, and juvenile periods. Larvae and juveniles of H. scutatum do not exhibit adult vertebral features associated with constricted-base tail autotomy. The pond-type larvae of A. jeffersonianum and H. scutatum have tapering centrum lengths posterior to the sacrum. This pattern is functionally associated with aquatic locomotion. The stream-type larvae of D. ocoee undergo enhanced regional growth in the anterior tail such that the anterior caudal centra become longer than the preceding caudosacral centra. With the exception of the first two caudal vertebrae, a similar growth pattern occurs in H. scutatum adults. We hypothesize that enhanced growth of the anterior caudal segments is associated with tail elongation and autotomy.     

Pattern of differentiation in the annual killifish genus Austrolebias (Cyprinodontiformes: Rivulidae) from a biosphere reserve site in South America: a multidisciplinary approach

The annual killifish genus Austrolebias includes approximately 38 species distributed throughout the Paraná-Plata basin and Patos-Merín system. Within the Austrolebias adloffi species complex, the Uruguayan populations of Austrolebias charrua were considered as an intergradation between A. adloffi and Austrolebias viarius populations. Austrolebias charrua presents an intermediate phenotype between both taxa and high levels of morphological and chromatic variability. In the present study, we incorporate different methodological approaches (molecular, morphology, and gamete ultrastructure) to elucidate the pattern of differentiation among the parapatric taxa ( A. charrua , Austrolebias reicherti , A. viarius ) distributed in a Biosphere Reserve Site. Analyses of cytochrome b sequences show high values of DNA polymorphism, in particular for A. charrua. This is in accordance with both morphological and gametic variation. Using a statistical parsimony network based on these sequences and analysis of morphological data, past fragmentation and range expansion involving perhaps secondary contact between A. charrua and A. reicherti could be proposed. Coloration pattern and morphometric analyses showed an unexpected higher similarity between the most distantly-related taxa, A. viarius and A. charrua . This could be the result of retention of ancestral polymorphisms, especially in A. charrua populations from ponds of higher elevation, or to directional selection acting in similar ecological environments. Because these annual killifish species are considered endangered, our work reinforces the high priority need to include them in a conservation programme.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 620–635.     

Relationships among development, ecology, and morphology in the evolution of Echinoderm larvae and life cycles

The evolution of life cycles involves transitions between discrete states in one or more of the characters that comprise a developmental pattern. In this paper, we examine three of the major life cycle characters and the states for these characters. Using examples from echinoderms, we discuss the evolutionary transitions that have occurred in the type of morphogenesis, developmental habitat, and mode of nutrition during development. We evaluate the functional requirements associated with these transitions to infer the likelihood (frequency or rapidity) of change in a given character and of biases in the polarity of character state transitions. Using comparisons of closely related species, we evaluate the change between states in one character for dependence on the state of, or correlated changes in, other characters. Based on our analysis of congeneric species that differ in developmental habitat, we conclude that the transition between pelagic and benthic development is an ecological change that is independent of changes in morphogenesis and should be reversible. In contrast, the transition from feeding to nonfeeding development has been considered to be irreversible because it involves marked changes in larval morphology. We re-examine the transition between different modes of larval nutrition in light of recent studies that show that there exists a continuum of nutritional strategies between planktotrophy and lecithotrophy. This continuum is largely determined by variation in maternal investment and does not involve alterations in larval morphology. We suggest that the boundary between planktotrophy and lecithotrophy is frequently crossed and that this transition is reversible. Ecological changes represent the crossing of a functional threshold. Only after crossing the threshold, do larvae experience qualitatively different selective pressures that can lead to subsequent changes in morphology and development. Two different changes have occurred in the type of morphogenesis: the simplification of larval morphology that is associated with obligate (nonfeeding) lecithotrophy and the loss of the larval body plan in the evolution from indirect to direct development. It is the modification of morphology independent of the ecological changes that requires alterations in developmental processes, constrains evolutionary options, imposes irreversibility, and establishes the discrete nature of larval patterns in marine invertebrates.     

Genetic constraints on wing pattern variation in Lycaeides butterflies: A case study on mapping complex,multifaceted traits in structured populations

Patterns of phenotypic variation within and among species can be shaped and constrained by trait genetic architecture. This is particularly true for complex traits, such as butterfly wing patterns, that consist of multiple elements. Understanding the genetics of complex trait variation across species boundaries is difficult, as it necessitates mapping in structured populations and can involve many loci with small or variable phenotypic effects. Here, we investigate the genetic architecture of complex wing pattern variation in Lycaeides butterflies as a case study of mapping multivariate traits in wild populations that include multiple nominal species or groups. We identify conserved modules of integrated wing pattern elements within populations and species. We show that trait covariances within modules have a genetic basis and thus represent genetic constraints that can channel evolution. Consistent with this, we find evidence that evolutionary changes in wing patterns among populations and species occur in the directions of genetic covariances within these groups. Thus, we show that genetic constraints affect patterns of biological diversity (wing pattern) in Lycaeides, and we provide an analytical template for similar work in other systems.     

Geographic Cline in the Shape of the Moose Mandible: Indications of an Adaptive Trend

Intra-specific geographic variation is probably one of the most common patterns studied in ungulate morphology. However, the shape of the mandible, a crucial feature with regard to feeding, has been greatly understudied in this context. Here, we utilized a museum collection of moose (Alces alces) mandibles to investigate whether we could detect significant variation in this species, and test for the existence of geographic patterns and associations with population genetic structure. We applied a landmark-based geometric morphometrics approach, analyzing shape data with principal component analysis and linear mixed models. A significant geographic shift in the shape of the moose mandible was revealed. The main pattern was similar in both sexes; however, there was a consistent difference in shape between males and females over the latitudinal scale. The main changes included an enlargement in the attachment surfaces of the muscles controlling biting and mastication, suggesting more effective mastication towards the north, plausibly as an adaptive response to a harder and tougher wintertime diet. Additionally, more subtle, yet statistically significant age-related shape variation was discovered. Interestingly, no or only a weak association between the morphometric variation and the genetic population structure was detected with neutral molecular markers.