Evolution of dentition in salamanders: relative roles of phylogeny and diet

Despite being widely regarded as generalist predators, amphibians exhibit a diversity of tooth shapes and dentition patterns, which may indicate the influence of dietary specialization on the evolution of tooth morphology. Very few studies have analysed the relationship between tooth morphology and diet (i.e., prey items) in amphibians, and those existing studies are highly speculative. We investigated the evolution of salamander teeth and the relationship between tooth morphology and diet in a phylogenetically independent fashion. We used a phylogeny of 23 species of salamander representing three families (Ambystomatidae, Plethodontidae, and Salamandridae) to, first, analyse the divergence of tooth morphology and its relationship to phylogeny and, second, to analyse the relationship between tooth morphology and diet diversity. We used electron scanning microscopy and a statistical comparative approach using Spatial Evolutionary and Ecological Analysis (SEEVA) and phylogenetic generalized least‐squares regression in R. Our results indicated significant divergence in tooth morphology at major phylogenetic splits. Moreover, there was a significant, phylogenetically independent relationship between tooth morphology and diet diversity. The relationship between diet and tooth morphology indicates not only a reflection of phylogenetic history, but also a degree of dietary specialization, indicating that evolution in tooth morphology has had an adaptive aspect in relation to salamander diet.     

Chewing on the trees: Constraints and adaptation in the evolution of the primate mandible

Chewing on different food types is a demanding biological function. The classic assumption in studying the shape of feeding apparatuses is that animals are what they eat, meaning that adaptation to different food items accounts for most of their interspecific variation. Yet, a growing body of evidence points against this concept. We use the primate mandible as a model structure to investigate the complex interplay among shape, size, diet, and phylogeny. We find a weak but significant impact of diet on mandible shape variation in primates as a whole but not in anthropoids and catarrhines as tested in isolation. These clades mainly exhibit allometric shape changes, which are unrelated to diet. Diet is an important factor in the diversification of strepsirrhines and platyrrhines and a phylogenetic signal is detected in all primate clades. Peaks in morphological disparity occur during the Oligocene (between 37 and 25 Ma) supporting the notion that an adaptive radiation characterized the evolution of South American monkeys. In all primate clades, the evolution of mandible size is faster than its shape pointing to a strong effect of allometry on ecomorphological diversification in this group.     

Mandible shape in marsupial and placental carnivorous mammals: a morphological comparative study using geometric morphometrics

We analysed mandible shape of the orders Dasyuromorpha, Didelphimorphia, and Carnivora using two‐dimensional geometric morphometrics, in order to explore the relationship between shape, size, and phylogeny. We studied 541 specimens, covering most of the genera of the terrestrial Carnivora (115 species) and a wide sample of marsupials (36 species). The observed shape variation had an ecological component. As an example, omnivorous carnivores have thick mandibles and large talonids in the carnassials, while hypercarnivores possess short mandibles and reduced talonids. There is also a discrimination between different taxonomic groups (i.e. marsupials and Carnivora), indicating some kind of constraint. Size explains a large percentage of total variance (large species had shorter and stronger mandibles, with anteriorly displaced carnassials), was significant when phylogeny was taken into account with a comparative method, but not when size and shape were optimized on the phylogeny. Carnivora presents a larger disparity and variation in body size, which could be related to the difference in teeth replacement. The optimization of mandible shape on the phylogenetic tree indicates that functional aspects, such as diet, are a key factor in the evolution of the carnivore mandible, but also that there is a phylogenetic pattern that cannot be explained by differences in diet alone. © 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2012, 164 , 836–855.     

Differential correlates of diet and phylogeny on the shape of the premaxilla and anterior tooth in sparid fishes (Perciformes: Sparidae)

We explore the correlational patterns of diet and phylogeny on the shape of the premaxilla and anterior tooth in sparid fishes (Perciformes: Sparidae) from the western Mediterranean Sea. The premaxilla is less variable, and in spite of the presence of species-specific features, a common structural pattern is easily recognizable in all species (i.e. the ascending and the articular processes are fused in a single branch, as in many percoid fishes). In contrast, tooth shape is more variable, and different structural types can be recognized (e.g. canine-like or incisive). Coupling geometric morphometric and comparative methods we found that the relationship between shape, diet and phylogeny also differs between premaxilla and tooth. Thus, the shape of the premaxilla is significantly correlated with food type, whereas the shape of the teeth is not correlated with diet, and probably reflects the species phylogenetic relationships. Two biological roles, resistance against compressive forces generated in the buccal cavity and the size of the oral gape, would explain the ecomorphological patterns of the premaxilla. The premaxilla and anterior tooth appear to evolve at different rates (mosaic evolution) and represent an example of morphological traits belonging to the same functional unit but following uncoupled evolutionary pathways.     

Morphometric convergence among European sand gobies in freshwater (Gobiiformes: Gobionellidae)

The five genera of sand gobies inhabit the seas and freshwaters of Europe and western Asia and occupy habitats ranging from fully marine to exclusively freshwater. In this study, we use geometric morphometrics to quantify body shape among sand gobies, in order to investigate how shape has evolved and how it is related to habitat. We also compare body shape between preserved museum specimens and fresh specimens, to determine whether or not fixation and storage in ethanol introduce detectable bias. We confirm that the fixed specimens exhibit significant shape changes as compared to fresh specimens, and so, we perform the bulk of our analyses exclusively on fixed specimens. We find that Economidichthys, Orsinigobius, and Pomatoschistus occupy distinct regions of morphospace. Knipowitschia and Ninnigobius have intermediate forms that overlap with Pomatoschistus and Orsinigobius, but not Economidichthys. This pattern is also in rough accordance with their habitats: Pomatoschistus is fully marine, Economidichthys fully freshwater, and the others fresh with some brackish tolerance. We augment a recent phylogeny of sand gobies with data for P. quagga and interpret morphometric shape change on that tree. We then evaluate convergence in form among disparate lineages of freshwater species by constructing a phylomorphospace and applying pattern‐based (convevol) measures of convergence. We find that freshwater taxa occupy a mostly separate region of morphospace from marine taxa and exhibit significant convergence in form. Freshwater taxa are characterized by relatively larger heads and stockier bodies than their marine relatives, potentially due to a common pattern of heterochronic size reduction.     

Environment and space as drivers of variation in skull shape in two widely distributed South‐American Tayassuidae,Pecari tajacu and Tayassu pecari (Mammalia: Cetartiodactyla)

The influence of the environment on the geographical variation of morphological traits has been recognized in a number of taxa. Pecari tajacu and Tayassu pecari are ideal models to investigate intraspecific geographic variation in skull because of their wide and heterogeneous geographical distribution in South America. We used geometric morphometric procedures to examine the geographical variation in skull shape of 294 adult specimens of these species from 134 localities. We quantified to what extent skull shape variation was explained by environment, skull size and geographical space using variation partitioning analysis. We detected a strong pattern of geographic variation for P. tajacu skull shape, but not for T. pecari. The environment seems to be the major selective force that drives skull shape variation in both species. Nevertheless, other spatially structured processes (e.g. genetic drift, gene flow) might also have affected variation in the skull shape of the more widespread species P. tajacu. Allometric relationships might reflect the biomechanical constraints that are thought to be strong enough to limit size‐related changes in T. pecari skull shape.     

Geometric morphometric analysis of the effect of temperature on wing size and shape in Aedes albopictus

Wing geometry helps to identify mosquito species, even cryptic ones. On the other hand, temperature has a well‐known effect on insect metric properties. Can such effects blur the taxonomic signal embedded in the wing? Two strains of Aedes albopictus (laboratory and field strain) were examined under three different rearing temperatures (26, 30 and 33 °C) using landmark‐ and outline‐based morphometric approaches. The wings of each experimental line were compared with Aedes aegypti. Both approaches indicated similar associations between wing size and temperature. For the laboratory strain, the wing size significantly decreased as the temperature increased. For the field strain, the largest wings were observed at the intermediate temperature. The two morphometric approaches describing shape showed different sensibilities to temperature. For both strains and sexes, the landmark‐based approach disclosed significant wing shape changes with temperature changes. The outline‐based approach showed lesser effects, detecting significant changes only in laboratory females and in field males. Despite the size and shape changes induced by temperature, the two strains of Ae. albopictus were always distinguished from Ae. aegypti. The present study confirms the lability of size. However, it also suggests that, despite environmentally‐induced variation, the architecture of the wing still provides a strong taxonomic signal.     

Ontogenetic allometry constrains cranial shape of the head‐first burrowing worm lizard Cynisca leucura (Squamata: Amphisbaenidae)

Amphisbaenians are fossorial, predominantly limbless squamate reptiles with distinct cranial shapes corresponding to specific burrowing behaviors. Due to their cryptic lifestyles and the scarcity of museum specimens, little is known of their intraspecific variation, particularly regarding cranial osteology. This represents a critical lack of information, because the majority of morphological investigations of squamate relationships are based on cranial characters. We investigated cranial variation in the West African Coast Worm Lizard Cynisca leucura, a round‐headed member of the Amphisbaenidae. Using geometric morphometric analyses of three‐dimensional computed tomographic scans, we found that cranial osteology of C. leucura is highly conserved, with the majority of shape changes occurring during growth as the cranium becomes more slender and elongate, accompanied by increasing interdigitation among the dermal roofing bones. Elements of the ventral portion of the cranium remain loosely connected in adults, possibly as a protective mechanism against repeated compression and torsion during burrow excavation. Intraspecific variation was strongly correlated with size change from juveniles to adults, indicating a dominant role of ontogenetic allometry in determining cranial shape. We found no evidence of sexual dimorphism, either during growth or among adults. Given the fossorial habits of C. leucura, we hypothesize that cranial allometry is under strong stabilizing selection to maintain adequate proportions for head‐first digging, thereby constraining the ability of individuals to respond to differing selection pressures, including sexual selection and variation in diet or microhabitat. For species in which digging imposes less mechanical stress (e.g., in softer sand), allometric associations during growth may be weakened, allowing changes to the ontogenetic trajectory and subsequent morphological traits. Such developmental dissociation between size and shape, known as heterochrony, may also be implicit in the evolution of the other amphisbaenian cranial shapes (shovel, spade, and keel), which may themselves be functionally adapted for their respective burrowing techniques. J. Morphol. 277:1159–1167, 2016. © 2016 Wiley Periodicals, Inc.     

Lower molar shape and size in prosimian and platyrrhine primates

The goal of this research is to evaluate the relative strength of the influences of diet, size, and phylogenetic signal on dental geometric shape. Accurate comprehension of these factors and their interaction is important for reconstructing diet and deriving characters for a cladistic analysis in fossil primates. Geometric morphometric analysis is used to identify axes of shape variation in the lower second molars of (a) prosimian primates and (b) platyrrhines. Landmarks were placed on µCT‐generated surface renderings. Landmark configurations were aligned using generalized Procrustes analysis. Principal components analysis and phylogenetic principal components analysis (pPCA) were performed on species average landmark co‐ordinates. pPCs were examined with phylogenetic generalized least squares analysis for association with size and with diet. PCs from both phylogenetic and non‐phylogenetic analyses were sufficient to separate species by broad dietary categories, including insectivores and folivores. In neither analysis was pPC1 correlated with tooth size, but some other pPCs were significantly correlated with size. The pattern of association between pPCs and size altered when centroid size and dietary variables were combined in the model; effects of diet factors typically exceeded effects of size. These results indicate a dominant phylogenetic and dietary signal in molar shape but also show some shape change correlated with size in the absence of obvious dietary associations. Geometric morphometric analysis appears to be useful for tracking functional traits in molars, particularly in tracking differences between folivorous and insectivorous species.     

Discrete and morphometric traits reveal contrasting patterns and processes in the macroevolutionary history of a clade of scorpions

Many palaeontological studies have investigated the evolution of entire body plans, generally relying on discrete character‐taxon matrices. In contrast, macroevolutionary studies performed by neontologists have mostly focused on morphometric traits. Although these data types are very different, some studies have suggested that they capture common patterns. Nonetheless, the tests employed to support this claim have not explicitly incorporated a phylogenetic framework and may therefore be susceptible to confounding effects due to the presence of common phylogenetic structure. We address this question using the scorpion genus Brachistosternus Pocock 1893 as case study. We make use of a time‐calibrated multilocus molecular phylogeny, and compile discrete and traditional morphometric data sets, both capturing the overall morphology of the organisms. We find that morphospaces derived from these matrices are significantly different, and that the degree of discordance cannot be replicated by simulations of random character evolution. Moreover, we find strong support for contrasting modes of evolution, with discrete characters being congruent with an ‘early burst’ scenario whereas morphometric traits suggest species‐specific adaptations to have driven morphological evolution. The inferred macroevolutionary dynamics are therefore contingent on the choice of character type. Finally, we confirm that metrics of correlation fail to detect these profound differences given common phylogenetic structure in both data sets, and that methods incorporating a phylogenetic framework and accounting for expected covariance should be favoured.     

Adaptive processes drive ecomorphological convergent evolution in antwrens (Thamnophilidae)

Phylogenetic niche conservatism (PNC) and convergence are contrasting evolutionary patterns that describe phenotypic similarity across independent lineages. Assessing whether and how adaptive processes give origin to these patterns represent a fundamental step toward understanding phenotypic evolution. Phylogenetic model‐based approaches offer the opportunity not only to distinguish between PNC and convergence, but also to determine the extent that adaptive processes explain phenotypic similarity. The Myrmotherula complex in the Neotropical family Thamnophilidae is a polyphyletic group of sexually dimorphic small insectivorous forest birds that are relatively homogeneous in size and shape. Here, we integrate a comprehensive species‐level molecular phylogeny of the Myrmotherula complex with morphometric and ecological data within a comparative framework to test whether phenotypic similarity is described by a pattern of PNC or convergence, and to identify evolutionary mechanisms underlying body size and shape evolution. We show that antwrens in the Myrmotherula complex represent distantly related clades that exhibit adaptive convergent evolution in body size and divergent evolution in body shape. Phenotypic similarity in the group is primarily driven by their tendency to converge toward smaller body sizes. Differences in body size and shape across lineages are associated to ecological and behavioral factors.     

Diet of Adenomera thomei (Almeida and Angulo, 2006) (Anura: Leptodactylidae) from a rubber tree plantation in southern Bahia,Brazil

This work describes the diet of a population of Adenomera thomei from a rubber tree plantation within the Atlantic Rainforest of Brazil. Individuals were measured and treated with a stomach flushing method. We assessed the correlation between morphometric aspects and stomach contents and compared electivity with the available invertebrate fauna in the leaf litter. The most important item in the diet was Formicidae. We found 2.48 prey items per stomach. Electivity was highest for isopods. We conclude that A. thomei is a sit-and-wait forager that, despite feeding mainly on ants, cannot be considered an ant specialist because it selects other prey items present in their environment.     

Evolutionary allometry of lumbar shape in Felidae and Bovidae

As body size increases, so do the biomechanical challenges of terrestrial locomotion. In the appendicular skeleton, increasing size is met with allometry of limb posture and structure, but much less is known about adaptations of the axial skeleton. It has been hypothesized that stabilization of the lumbar region against sagittal bending may be a response to increasing size in running mammals. However, empirical data on lumbar allometry in running mammals are scarce. This study presents quantitative data on allometry of the penultimate lumbar vertebra in two mammal families: Bovidae and Felidae. One hundred and twenty 3D landmarks were collected on the penultimate lumbar vertebra of 34 bovid (N = 123) and 23 felid (N = 93) species. Multivariate phylogenetically informed regressions were computed, and the shape variation associated with increasing size calculated. The influence of locomotor and habitat variables on size‐corrected lumbar shape was tested using phylogenetic multivariate analysis of variance (MANOVAs). Results demonstrate that the scaling patterns in both groups are consistent with the hypothesis of allometric stabilization of the lumbar region, and suggest convergent evolution of allometric responses in distantly related lineages of mammals. However, there was a relatively smaller effect of size in felids than bovids, even when size range disparities were accounted for, suggesting a trade‐off between size and running behaviour. Despite the strong influence of size and phylogeny on lumbar shape, there was no correlation with either habitat or diet within families, though certain specialized taxa (i.e., cheetah) did have divergent morphology.     

Constrained body shape among highly genetically divergent allopatric lineages of the supralittoral isopod Ligia occidentalis (Oniscidea)

Multiple highly divergent lineages have been identified within Ligia occidentalis sensu lato, a rocky supralittoral isopod distributed along a ~3000 km latitudinal gradient that encompasses several proposed marine biogeographic provinces and ecoregions in the eastern Pacific. Highly divergent lineages have nonoverlapping geographic distributions, with distributional limits that generally correspond with sharp environmental changes. Crossbreeding experiments suggest postmating reproductive barriers exist among some of them, and surveys of mitochondrial and nuclear gene markers do not show evidence of hybridization. Populations are highly isolated, some of which appear to be very small; thus, the effects of drift are expected to reduce the efficiency of selection. Large genetic divergences among lineages, marked environmental differences in their ranges, reproductive isolation, and/or high isolation of populations may have resulted in morphological differences in L. occidentalis, not detected yet by traditional taxonomy. We used landmark‐based geometric morphometric analyses to test for differences in body shape among highly divergent lineages of L. occidentalis, and among populations within these lineages. We analyzed a total of 492 individuals from 53 coastal localities from the southern California Bight to Central Mexico, including the Gulf of California. We conducted discriminant function analyses (DFAs) on body shape morphometrics to assess morphological variation among genetically differentiated lineages and their populations. We also tested for associations between phylogeny and morphological variation, and whether genetic divergence is correlated to multivariate morphological divergence. We detected significant differences in body shape among highly divergent lineages, and among populations within these lineages. Nonetheless, neither lineages nor populations can be discriminated on the basis of body shape, because correct classification rates of cross‐validated DFAs were low. Genetic distance and phylogeny had weak to no effect on body shape variation. The supralittoral environment appears to exert strong stabilizing selection and/or strong functional constraints on body shape in L. occidentalis, thereby leading to morphological stasis in this isopod.     

Distinct evolutionary patterns of morphometric sperm traits in passerine birds

The striking diversity of sperm shape across the animal kingdom is still poorly understood. Postcopulatory sexual selection is an important factor driving the evolution of sperm size and shape. Interestingly, morphometric sperm traits, such as the length of the head, midpiece and flagellum, exhibit a strong positive phenotypic correlation across species. Here we used recently developed comparative methods to investigate how such phenotypic correlations between morphometric sperm traits may evolve. We compare allometric relationships and evolutionary trajectories of three morphometric sperm traits (length of head, midpiece and flagellum) in passerine birds. We show that these traits exhibit strong phenotypic correlations but that allometry varies across families. In addition, the evolutionary trajectories of the midpiece and flagellum are similar while the trajectory for head length differs. We discuss our findings in the light of three scenarios accounting for correlated trait evolution: (i) genetic correlation; (ii) concerted response to selection acting simultaneously on different traits; and (iii) phenotypic correlation between traits driven by mechanistic constraints owing to selection on sperm performance. Our results suggest that concerted response to selection is the most likely explanation for the phenotypic correlation between morphometric sperm traits.     

A complete survey of normal pores on a smooth shell ostracod (Crustacea): Landmark‐based versus outline geometric morphometrics

Pores and sensilla on ostracod shell have often been used in studies of ontogeny, taxonomy, and phylogeny of the group. However, an analysis of sexual dimorphism and variation between valves in the number and distribution of pores is lacking. Also, such studies have never been done on a widely distributed, morphologically variable, and weakly ornamented freshwater ostracod. Here, we survey pores in one such species, Physocypria kraepelini . We choose 27 homologous pores as landmarks for 2D‐geometric morphometric analysis, with the aim to assess intersexual and between valves variation in size and shape relative to the Fourier outline analysis. This species has only simple (Type A) pores with and without a lip, and each pore carries an undivided sensory seta. Our results show that the total number of pores varies (from 270 to 296), but this is not associated with a specific valve. Males carry fewer pores than females, however no sex specific pores are found. Small intrapopulation divergence of the Cyt b molecular marker (1%) indicates that morphological variability is not species related. We found that P. kraepelini exhibits directional asymmetry of size and shape, sexual size dimorphism (SSD) but lacks sexual shape dimorphism (SShD). Two geometric morphometrics methods were congruent in the estimation of SSD, SShD, and directional asymmetry of shape but differ in the statistical evaluation of directional asymmetry of size. Contrary to other animal groups, our study suggests that ostracods have more pronounced directional asymmetry of shape compared to directional asymmetry of size.     

Evolution of ontogenetic allometry shaping giant species: a case study from the damselfish genus Dascyllus (Pomacentridae)

The evolution of body size, the paired phenomena of giantism and dwarfism, has long been studied by biologists and paleontologists. However, detailed investigations devoted to the study of the evolution of ontogenetic patterns shaping giant species are scarce. The damselfishes of the genus Dascyllus appear as an excellent model for such a study. Their well understood phylogeny reveals that large‐bodied species have evolved in two different clades. Geometric morphometric methods were used to compare the ontogenetic trajectories of the neurocranium and the mandible in both small‐bodied (Dascyllus aruanus and Dascyllus carneus; maximum size: 50–65 mm standard length) and giant (Dascyllus trimaculatus and Dascyllus flavicaudus; maximum size: 90–110 mm standard length) Dascyllus species. At their respective maximum body size, the neurocranium of the giant species is significantly shorter and have a higher supraoccipital crest relative to the small‐bodied species, whereas mandible shape variation is more limited and is not related to the ‘giant’ trait. The hypothesis of ontogenetic scaling whereby the giant species evolved by extending the allometric trajectory of the small‐bodied ones (i.e. hypermorphosis) is rejected. Instead, the allometric trajectories vary among species by lateral transpositions. The rate of shape changes and the type of lateral transposition also differ according to the skeletal unit among Dascyllus species. Differences seen between the two giant species in the present study demonstrate that giant species may appear by varied alterations of the ancestor allometric pattern. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 99–117.     

Testing evolutionary stasis and trends in first lower molar shape of extinct Italian populations of Terricola savii (Arvicolidae,Rodentia) by means of geometric morphometrics

Extinct populations of Terricola savii have been investigated in order to analyse evolutionary stasis and correlation of first lower molar shape with climatic proxies by means of geometric morphometrics. Evolutionary stasis, its recognition and explanation are central topics in evolutionary paleobiology. In this study, tooth shape variation of the arvicolid T. savii has been analysed through time. In addition to explicit multivariate tests of stasis based on landmark and semi‐landmark geometric morphometrics, first lower molar M₁ shape has been decomposed in orthogonal axes of variation and tested for correlation with climate changes. Multivariate tests were consistent with evolutionary stasis. Yet, according to univariate tests, the dominant dimension of shape variation shows a temporal trend well correlated with a climatic proxy, i.e. δ¹⁸O. The remaining variation does not show any trend. Adaptation to current climatic condition might occur even without affecting shape as a whole. Phenotypic plasticity of this species could be invoked to explain evolutionary stasis, as a long time pattern.     

Morphological diversity of Old World rats and mice (Rodentia, Muridae) mandible in relation with phylogeny and adaptation

The respective roles of the phylogenetic and ecological components in an adaptive radiation are tested on a sample of Old World rats and mice (Muridae, Murinae). Phylogeny was established on nuclear and mitochondrial genes and reconstructed by maximum likelihood and Bayesian methods. This phylogeny is congruent with previous larger scale ones recently published, but includes some new results: Bandicota and Nesokia are sister taxa and Micromys would be closely related to the Rattus group. The ecological diversification is investigated through one factor, the diet, and the mandible outline provides the morphological marker. Elliptic and radial Fourier transforms are used for quantifying size and shape differences among species. Univariate size and shape parameters indicate that phylogeny is more influential on size than diet, and the reverse occurs for shape and robust patterns are recognized by multivariate analyses of the data sets provided by the Fourier methods. Omnivorous and herbivorous groups are well separated despite some overlapping, as well as are other Murinae with a specialized diet (insects, seeds). Phylogeny is also influential as shown by the segregation of several groups (Praomys, Arvicanthini, Rattus, Apodemus). Allometric shape variation was investigated, and although present it does not overwhelm effects of either phylogeny or diet. Massive mandibles characterize herbivorous Murinae and slender mandibles, the insectivorous ones. A strong angular process relative to the coronoid process characterizes seedeaters, and the reverse characterized Murinae with a diet based largely on animal matter. Such changes in morphology are clearly in relation with the functioning of the mandible, and with the forces required by the nature of the food: the need of a stronger occlusal force in herbivorous species would explain massive mandibles, and an increase of the grasping and piercing function of incisors in insectivorous species would explain slender mandibles.