The evolution of ecological specialization across the range of a broadly distributed marine species

Ecological specialization is an important engine of evolutionary change and adaptive radiation, but empirical evidence of local adaptation in marine environments is rare, a pattern that has been attributed to the high dispersal ability of marine taxa and limited geographic barriers to gene flow. The broad-nosed pipefish, Syngnathus typhle, is one of the most broadly distributed syngnathid species and shows pronounced variation in cranial morphology across its range, a factor that may contribute to its success in colonizing new environments. We quantified variation in cranial morphology across the species range using geometric morphometrics, and tested for evidence of trophic specialization by comparing individual-level dietary composition with the community of prey available at each site. Although the diets of juvenile pipefish from each site were qualitatively similar, ontogenetic shifts in dietary composition resulted in adult populations with distinctive diets consistent with their divergent cranial morphology. Morphological differences found in nature are maintained under common garden conditions, indicating that trophic specialization in S. typhle is a heritable trait subject to selection. Our data highlight the potential for ecological specialization in response to spatially variable selection pressures in broadly distributed marine species.     

Postcranial element shape and function: assessing locomotor mode in extant and extinct mustelid carnivorans

Assessment of locomotor modes in fossil taxa must often be made on the basis of heavily fragmented postcranial material. Previous authors have used quantitative methods to determine locomotor function from whole postcranial elements. The goals of this project were to assess the ability of element shape to discern between locomotor modes through landmark analysis, and to apply the results to assessment of fossils. Results suggest that element shape is a good predictor of function, but that different elements have different predictive capacities for each locomotor mode. Additionally, a relationship between size and shape exists that appears to drive morphological differentiation in the group. Finally, data from the extant sample were applied to fossil material of the extinct Plio-Pleistocene taxon Trigonictis . The results suggest that the locomotor mode of Trigonictis was generalized and probably an intermediate between the half-bound locomotion found in weasels and ferrets and the scansorial locomotion of martens and fishers.  © 2007 The Linnean Society of London, Zoological Journal of the Linnean Society , 2007, 150 , 895–914.     

A unique feeding strategy of the extinct marine mammal Kolponomos: convergence on sabretooths and sea otters

Mammalian molluscivores feed mainly by shell-crushing or suction-feeding. The extinct marine arctoid, Kolponomos, has been interpreted as an otter-like shell-crusher based on similar dentitions. However, neither the masticatory biomechanics of the shell-crushing adaptation nor the way Kolponomos may have captured hard-shelled prey have been tested. Based on mandibular symphyseal morphology shared by Kolponomos and sabre-toothed carnivores, we hypothesize a sabretooth-like mechanism for Kolponomos prey-capture, whereby the mandible functioned as an anchor. Torque generated from jaw closure and head flexion was used to dislodge prey by prying, with prey then crushed using cheek teeth. We test this hypothesized feeding sequence using phylogenetically informed biomechanical simulations and shape analyses, and find a strongly supported, shared high mandibular stiffness in simulated prey-capture bites and mandibular shape in Kolponomos and the sabre-toothed cat Smilodon. These two distantly related taxa converged on using mandibles to anchor cranial torqueing forces when prying substrate-bound prey in the former and sabre-driving forces during prey-killing in the latter. Simulated prey-crushing bites indicate that Kolponomos and sea otters exhibit alternative structural stiffness-bite efficiency combinations in mandibular biomechanical adaptation for shell-crushing. This unique feeding system of Kolponomos exemplifies a mosaic of form-function convergence relative to other Carnivora.     

Variation in morphology and functional performance across distinct evolutionary lineages of the Moorish gecko (Tarentola mauritanica) from the Iberian Peninsula

Deciphering the mechanisms that underlie morphological and functional diversity is essential for understanding how organisms adapt to their environment. Interestingly, phenotypic divergence does not necessarily correspond to the geographic and genetic separation between populations. Here, we explored the morphological and functional divergence among populations of two genetically differentiated clades of the Moorish gecko, Tarentola mauritanica. We used linear and geometric morphometrics to quantify morphological variation and investigated how it translates into biting and CLIMBING PERFORMANCE, to better understand the mechanisms potentially underlying population and lineage divergence. We found marked morphological differences between clades, both in body size and head shape. However, much of this differentiation is more strongly related to local variation between populations of the same clade, suggesting that recent ecological events may be more influential than deep evolutionary history in shaping diversity patterns in this group. Despite a lack of association between morphology and functional diversification in the locomotor system of the Moorish gecko, straightforward links are observed between head morphology and biting performance, providing more hints on the possible underlying causes. Indeed, variation in bite force is mostly determined by size variation and sexual dimorphism, and differences between the two clades concern how sexual variation is expressed, reinforcing the idea that both social and ecological factors contribute in shaping differentiation. Interestingly, the individuals from the islets off the coast of Murcia exhibit particular morphological and functional traits, which suggests that the ecological conditions related to insularity may drive the phenotypic differentiation of this population.     

Rare ecomorphological convergence on a complex adaptive landscape: Body size and diet mediate evolution of jaw shape in squirrels (Sciuridae)

Convergence is widely regarded as compelling evidence for adaptation, often being portrayed as evidence that phenotypic outcomes are predictable from ecology, overriding contingencies of history. However, repeated outcomes may be very rare unless adaptive landscapes are simple, structured by strong ecological and functional constraints. One such constraint may be a limitation on body size because performance often scales with size, allowing species to adapt to challenging functions by modifying only size. When size is constrained, species might adapt by changing shape; convergent shapes may therefore be common when size is limiting and functions are challenging. We examine the roles of size and diet as determinants of jaw shape in Sciuridae. As expected, size and diet have significant interdependent effects on jaw shape and ecomorphological convergence is rare, typically involving demanding diets and limiting sizes. More surprising is morphological without ecological convergence, which is equally common between and within dietary classes. Those cases, like rare ecomorphological convergence, may be consequences of evolving on an adaptive landscape shaped by many‐to‐many relationships between ecology and function, many‐to‐one relationships between form and performance, and one‐to‐many relationships between functionally versatile morphologies and ecology. On complex adaptive landscapes, ecological selection can yield different outcomes.     

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.     

Do functional demands associated with locomotor habitat,diet, and activity pattern drive skull shape evolution in musteloid carnivorans?

A major goal of evolutionary studies is to better understand how complex morphologies are related to the different functions and behaviours in which they are involved. For example, during locomotion and hunting behaviour, the head and the eyes have to stay at an appropriate level in order to reliably judge distance as well as to provide postural information. The morphology and orientation of the orbits and cranial base will have an impact on eye orientation. Consequently, variation in orbital and cranial base morphology is expected to be correlated with aspects of an animal's lifestyle. In this study, we investigate whether the shape of the skull evolves in response to the functional demands imposed by ecology and behaviour using geometric morphometric methods. We test if locomotor habitats, diet, and activity pattern influence the shape of the skull in musteloid carnivorans using (M)ANOVAs and phylogenetic (M)ANOVAs, and explore the functional correlates of morphological features in relation to locomotor habitats, diet, and activity pattern. Our results show that phylogeny, locomotion and, diet strongly influence the shape of the skull, whereas the activity pattern seems to have a weakest influence. We also show that the locomotor environment is highly integrated with foraging and feeding, which can lead to similar selective pressures and drive the evolution of skull shape in the same direction. Finally, we show similar responses to functional demands in musteloids, a super family of close related species, as are typically observed across all mammals suggesting the pervasiveness of these functional demands.     

Reconciling the convergence of supraspinous fossa shape among hominoids in light of locomotor differences

Differences in scapular morphology between modern humans and the African and lesser apes are associated with the distinct locomotor habits of these groups. However, several traits, particularly aspects of the supraspinous fossa, are convergent between Homo and Pongo—an unexpected result given their divergent locomotor habits. Many morphological assessments of the scapula rely on the limited number of static landmarks available, and traditional approaches like these tend to oversimplify scapular shape. Here, we present the results of two geometric morphometric (GM) analyses of hominoid supraspinous fossa shape—one employing five homologous landmarks and another with 83 sliding semilandmarks—alongside those of traditional methods to evaluate if three-dimensional considerations of fossa shape afford more comprehensive insights into scapular shape and functional morphology. Traditional measures aligned Pongo and Homo with narrow and transversely oriented supraspinous fossae, whereas African ape and Hylobates fossae are broader and more obliquely situated. However, our GM results highlight that much of the convergence between Homo and Pongo is reflective of their more medially positioned superior angles. These approaches offered a more complete assessment of supraspinous shape and revealed that the Homo fossa, with an intermediate superior angle position and moderate superoinferior expansion, is actually reminiscent of the African ape shape. Additionally, both Pongo and Hylobates were shown to have more compressed fossae, something that has not previously been identified through traditional analyses. Thus, the total morphological pattern of the Pongo supraspinous fossa is unique among hominoids, and possibly indicative of its distinctive locomotor habits. Am J Phys Anthropol 156:498–510, 2015. © 2015 Wiley Periodicals, Inc.     

Points on the curve: An analysis of methods for assessing the shape of vertebrate claws

The form of amniote claws has been extensively investigated, often with inferences about ecological association being drawn from studies of their geometry. Various methods have been used to quantify differences in the geometry of claws, but rarely have the underlying assumptions of such methods been addressed. Here, we use one set of bird claws and apply six methods (five that have been previously used, and a new one) that are tasked with comparing their shape. In doing so, we compare the (1) ability of these methods to represent the shape of the claw; (2) validity of the assumptions made about underlying claw geometry; (3) their ability to be applied unambiguously; and (4) their ability to differentiate between predetermined functional clusters. We find that of the six methods considered only the geometric morphometric approach reveals differences in the shapes of bird claws. Our comparison shows that geometry‐based methods can provide a general estimate of the degree of curvature of claw arcs, but are unable to differentiate between shapes. Of all of the geometry‐based approaches, we conclude that the adjusted version of the Zani (2000) method is the most useful because it can be applied without ambiguity, and provides a reliable estimate of claw curvature. The three landmarks that define that method (tip and base of the claw arc, plus the intersection between said claw arc and a line drawn perpendicular from the midpoint of tip and claw base) do not all bear biological significance, but relatively clearly circumscribe the length‐to‐height ratio of the claw, which relates to its curvature. Overall, our comparisons reveal that the shape of avian claws does not differ significantly between climbing and perching birds, and that the utilization of preordained functional clusters in comparative data analysis can hinder the discovery of meaningful differences in claw shape. J. Morphol. 278:150–169, 2017. © 2016 Wiley Periodicals,Inc.     

Dental topographic and three-dimensional geometric morphometric analysis of carnassialization in different clades of carnivorous mammals (Dasyuromorphia,Carnivora, Hyaenodonta)

The evolution of carnassial teeth in mammals, especially in the Carnivora, has been subject of many morphometric and some dental topographic studies. Here, we use a combination of dental topographic analysis (Dirichlet normal energy) and 3D geometric morphometrics of less and high carnassialized lower teeth of carnivoran, dasyuromorph and hyaenodont taxa. Carnassial crown curvature, as indicated by Dirichlet normal energy, is high in lesser carnassialized teeth and low in higher carnassialized teeth, where it is influenced by the reduction of crown features such as cusps and crests. PC1 of the geometric morphometric analysis is linked to enlargement of the carnassial blade, reduction of the talonid crushing basin and an increasingly asymmetric cervix line with an enlarged mesial flexure in more carnassialized teeth. Distribution of PC1 values further indicates that along the tooth row of dasyuromorphs (m2–m4) and hyaenodonts (m1–m3) the most distal carnassial is the most carnassialized (principal carnassial), and in most taxa with overall higher carnassialized teeth, carnassialization successively increases from the anterior to the posterior tooth position along the tooth row. PC2 indicates that a longitudinal elongated carnassial is present in caniforms and in unspecialized feliforms, which separates these taxa in morphospace from all dasyuromorphs, hyaenodonts and specialized feliforms. An ancestral state reconstruction shows that this longitudinal elongation may be a plesiomorphic ancestral state for the Carnivora, which is different from the Dasyuromorphia and the Hyaenodonta. This elongation, enabling the presence of a longitudinally aligned carnassial blade as well as a complete talonid basin, might have provided the Carnivora with an advantage in terms of adaptive versatility.     

Functional implications of dicynodont cranial suture morphology

Cranial suture morphology of Lystrosaurus and the generalized dicynodont Oudenodon was investigated to determine the strain environment during mastication, which in turn may indicate a difference in cranial function between the two taxa. Finite element (FE) analysis indicated that less strain accumulated in the cranium of Lystrosaurus during orthal bite simulations than in Oudenodon. Despite the overall difference in strain magnitude, moderate to high FE‐predicted strain accumulated in similar areas of the cranium of both taxa. The suture morphology in these cranial regions of Lystrosaurus and Oudenodon was investigated further by examination of histological sections and supplemented by observations of serial sections and computed tomography (CT) scans. The predominant type of strain from selected blocks of finite elements that contain sutures was determined, enabling comparison of suture morphology to strain type. Drawing from strain‐suture correlations established in extant taxa, the observed patterns of sutural morphology for both dicynodonts were used to deduce cranial function. The moderate to high compressive and tensile strain experienced by the infraorbital bar, zygomatic arch, and postorbital bar of Oudenodon and Lystrosaurus may have been decreased by small adjustive movements at the scarf sutures in those regions. Disparities in cranial suture morphology between the two taxa may reflect differences in cranial function. For instance, the tongue and groove morphology of the postorbital‐parietal suture in Oudenodon could have withstood the higher FE‐predicted tensile strain in the posterior skull roof. The scarf premaxilla‐nasal suture of Lystrosaurus provided an additional region of sutural mobility in the anterior surface of the snout, suggesting that Lystrosaurus may have employed a different biting regime than Oudenodon. The morphology of several sutures sampled in this study correlated with the FE‐predicted strain, although other cranial functional hypotheses remain to be tested. J. Morphol., 2010. © 2010 Wiley‐Liss, Inc.     

Predicting ecological and phenotypic differentiation in the wild: a case of piscivorous fish in a fishless environment

Environmental variation drives ecological and phenotypic change. How predictable is differentiation in response to environmental change? Answering this question requires the development and testing of multifarious a priori predictions in natural systems. We employ this approach using Gobiomorus dormitor populations that have colonized inland blue holes differing in the availability of fish prey. We evaluated predictions of differences in demographics, habitat use, diet, locomotor and trophic morphology, and feeding kinematics and performance between G. dormitor populations inhabiting blue holes with and without fish prey. Populations of G. dormitor independently diverged between prey regimes, with broad agreement between observed differences and a priori predictions. For example, in populations lacking fish prey, we observed male‐biased sex ratios, a greater use of shallow‐water habitat, and larger population diet breadths as a result of greater individual diet specialization. Furthermore, we found predictable differences in body shape, mouth morphology, suction generation capacity, strike kinematics, and feeding performance on different prey types, consistent with the adaptation of G. dormitor to piscivory when coexisting with fish prey and to feeding on small invertebrates in their absence. The results of the present study suggest great potential in our ability to predict population responses to changing environments, which is an increasingly important capability in a human‐dominated, ever‐changing world. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 588–607.     

Ecomorphological disparity in an adaptive radiation: opercular bone shape and stable isotopes in Antarctic icefishes

To assess how ecological and morphological disparity is interrelated in the adaptive radiation of Antarctic notothenioid fish we used patterns of opercle bone evolution as a model to quantify shape disparity, phylogenetic patterns of shape evolution, and ecological correlates in the form of stable isotope values. Using a sample of 25 species including representatives from four major notothenioid clades, we show that opercle shape disparity is higher in the modern fauna than would be expected under the neutral evolution Brownian motion model. Phylogenetic comparative methods indicate that opercle shape data best fit a model of directional selection (Ornstein–Uhlenbeck) and are least supported by the “early burst” model of adaptive radiation. The main evolutionary axis of opercle shape change reflects movement from a broad and more symmetrically tapered opercle to one that narrows along the distal margin, but with only slight shape change on the proximal margin. We find a trend in opercle shape change along the benthic–pelagic axis, underlining the importance of this axis for diversification in the notothenioid radiation. A major impetus for the study of adaptive radiations is to uncover generalized patterns among different groups, and the evolutionary patterns in opercle shape among notothenioids are similar to those found among other adaptive radiations (three‐spined sticklebacks) promoting the utility of this approach for assessing ecomorphological interactions on a broad scale.     

Functional niche partitioning in Therizinosauria provides new insights into the evolution of theropod herbivory

Dietary specialization is generally considered to be a crucial factor in driving morphological evolution across extant and extinct vertebrates. The ability to adapt to a specific diet and to exploit ecological niches is thereby influenced by functional morphology and biomechanical properties. Differences in functional behaviour and efficiency can therefore allow dietary diversification and the coexistence of similarly adapted taxa. Therizinosauria, a group of secondarily herbivorous theropod dinosaurs, is characterized by a suite of morphological traits thought to be indicative of adaptations to an herbivorous diet. Digital reconstruction, theoretical modelling and computer simulations of the mandibles of therizinosaur dinosaurs provides evidence for functional niche partitioning in adaptation to herbivory. Different mandibular morphologies present in therizinosaurians were found to correspond to different dietary strategies permitting coexistence of taxa. Morphological traits indicative of an herbivorous diet, such as a downturned tip of the lower jaw and an expanded postdentary region, were identified as having stress mitigating effects. The more widely distributed occurrence of these purported herbivorous traits across different dinosaur clades suggests that these features also could have played an important role in the evolution and acquisition of herbivory in other groups.     

Variation in the digging apparatus of the subterranean silvery mole-rat, Heliophobius argenteocinereus (Rodentia, Bathyergidae): the role of ecology and geography

The skull of most subterranean tooth-digging rodents is markedly affected by their digging mode. In the present study, we investigated the cranial variation in a strictly subterranean, highly specialized Afrotropical tooth-digger, Heliophobius argenteocinereus (Bathyergidae, Rodentia), using a geometric morphometric approach and evaluated the effect of different factors on size and shape differences among four populations. No evidence for sexual dimorphism was found in skull size or shape. The cranial shape variation was large and influenced mainly by the type of habitat (miombo woodland versus farmland and grassland) and the latitudinal gradient. The dorsal side of the skull appears to be more plastic and adaptable to local environments, as well as more independent of size, than the ventral side. Only the shortening of the rostrum is presumably an adaptive process independent of size that leads to an increase of efficacy of the tooth-digging apparatus in Heliophobius , whereas the increase in the in-force and the more procumbent incisors both comprise size-related changes caused by ontogenetic allometric growth.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 822–831.     

What is bred in the bone: Ecomorphological associations of pelvic girdle form in greater Antillean Anolis lizards

Ecological niche partitioning of Anolis lizards of the Greater Antillean islands has been the focus of many comparative studies, and much is known about external morphological convergence that characterizes anole ecomorphs. Their internal anatomy, however, has rarely been explored in an ecomorphological context, and it remains unknown to what degree skeletal morphology tracks the diversity and ecological adaptation of these lizards. Herein, we employ CT scanning techniques to visualise the skeleton of the pelvic girdle in situ, and 3D geometric morphometrics to compare the form of the ilium, ischium, and pubis within and between ecomorphs. We examine 26 species of anoles representing four ecomorphs (trunk‐ground, trunk‐crown, crown‐giant, twig) from three islands (Jamaica, Hispaniola, and Puerto Rico). The subtle variations in pelvic girdle morphology discovered are directly associable with all three parameters that we set out to focus on: phylogenetic relationship, specimen size, and assigned ecomorph category. Morphometric variation that correlates with size and/or phylogenetic signal varies between species and cannot be eliminated from the data set without markedly reducing its overall variability. The discovered patterns of skeletal variation are consistent with the demands of locomotor mechanics pertinent to the structural configuration of the microhabitat of three of the four ecomorphs, with the fourth having no discernible distinctive features. This manifests itself chiefly in the relative anteroposterior extent and anteroventral inclination of the ilium and pubis, which differ between ecomorphs and are postulated to reflect optimization of the direction of muscle vectors of the femoral protractors and retractors. Our investigation of the form of the pelvic girdle of anoles allows us to generalize our findings to entire ecomorph categories within a broad phylogenetic and biogeographic context. Differences in the form and configuration of the postcranial skeleton are directly related to ecological patterns.     

The impact of diet,habitat use,and behaviour on head shape evolution in homalopsid snakes

An organism's morphology is driven by selection on function while being constrained by phylogenetic and developmental factors as well as functional trade‐offs. If selection on function is strong and solutions limited, then convergence is expected. In this paper we quantify head shape in a group of ecologically diverse snakes (homalopsid snakes) differing in habitat use and diet using three‐dimensional geometric morphometric approaches. Using data on head shape we explore whether snakes eating different prey show different morphologies. Moreover, we test whether head shape is constrained by other factors such as habitat use, burrow use, or activity pattern. Our results demonstrate similar head shapes in species consuming similar prey. Snakes that capture elusive prey under water differ from those that capture and swallow prey like frogs or crustaceans. Moreover, habitat use, the use of burrows, and activity pattern also significantly impact head shape in this group of snakes. However, this signal appears to be partly confounded by the diet signal. For axes discriminating specifically between habitat use groups or animals that use burrows vs. those that do not shapes were in accordance with our predictions. Our results suggests an adaptive signal in the evolution of head shape in homalopsid snakes with diet, habitat use and the use of burrows all influencing the evolution of head shape in the group.