Morphological disparity and evolutionary rates of cranial and postcranial characters in sloths (Mammalia,Pilosa, Folivora)

Sloth morphological evolution has been widely studied qualitatively, with comparative anatomy and morpho-functional approaches, or through quantitative assessments of morphological variation using morphometrics. Only recently, however, have folivoran morphological disparity and evolutionary rates begun to be evaluated using discrete character data. Nonetheless, patterns of morphological evolution in separate character partitions have not been investigated, neither the relative influence of, on the one hand, phylogeny, and on the other, dietary and locomotory adaptations of sloths. Here we evaluate those patterns using a phylomorphospace approach, quantifying morphological disparity and evolutionary rates, and investigating possible drivers of morphological evolution for cranial and postcranial characters in Folivora. The evolution of the morphology in those partitions is associated with distinct patterns of disparity among clades and ecological groups, even though the two partitions do not differ substantially in overall evolutionary tempo. Historical processes shaped the morphological evolution of sloths more consistently than ecological ones, although changes in postcranial characters also seem to be associated with locomotory adaptations, in which morphological convergences were much more common. We also discuss important methodological trade-offs in investigations of partitioned datasets mostly composed of fossil taxa.     

PATTERNS OF QUANTITATIVE VARIATION IN LEPIDOPTERAN WING MORPHOLOGY: THE CONVERGENT GROUPS HELICONIINAE AND ITHOMIINAE (PAPILIONOIDEA: NYMPHALIDAE)

Wing morphology has historically been a major focus in taxonomic and evolutionary studies of lepidopterans. However, general patterns of quantitative variation and diversification in wing sizes and shapes and the factors underlying them have been unexplored. A morphometric study of wing variation in the convergent heliconine and ithomine butterflies reveals remarkable similarities, both in their morphologies at a given size and in their patterns of allometry and variability. The groups differ primarily in the relative lengths of inner and outer forewing margins, with larger species being more similar across groups than smaller ones. Allometric size-scaling variation accounts for more than 90% of the total morphological variation in the two groups and thus seems to be the major determinant of wing shape. Forewings and hind wings are isometric in size (area) with respect to one another; however, wing shape within and among groups is significantly allometric, resulting in considerable shape differences between small and large species. A strong trend of increasing variability from anterior to posterior along the wings is consistent with hypotheses of aerodynamic constraint. Wings and bodies represent classical morphological “character suites” in that size and shape variation are more tightly correlated within suites than among them. Such complexes argue against the overriding importance of aerodynamic factors, such as wing load and muscle development, in constraining gross morphology.     

On the reality and recognisability of asexual organisms: morphological analysis of the masticatory apparatus of bdelloid rotifers

Species concepts and definitions have been a long-standing debate in evolutionary biology since before Darwin, and almost all proposed solutions are based upon grouping and clustering, with species conceived as somehow biological distinct entities, originated and maintained mainly by reproductive isolation. Lacking reproductive exchange, asexual organisms such as bdelloid rotifers, the best-supported clade of so-called 'ancient asexuals', pose an interesting challenge to debates over the reality of species. However, few data are available on bdelloid rotifers. The only evidence has been that bdelloid species have been more consistently recognised than in their sister sexual group, the monogonont rotifers, across successive taxonomic treatments, but this is confounded by the much lesser degree of taxonomic interest in bdelloids. We applied geometric morphometrics analyses on shape and size of hard masticatory pieces, named trophi, of 1420 bdelloids, belonging to 48 populations of eight traditional species, to test the hypothesis of recognisability of bdelloids. Our morphological analysis confirms that traditional bdelloid species are separated distinct entities, possessing trophi morphologies divided by gaps between taxa, similar to patterns of morphological features in sexually reproducing organisms. In common with most microscopic understudied organisms, bdelloid rotifers harbour much previously undescribed diversity: we found significant differences in trophi morphology within traditional species, revealing the existence of cryptic taxa, similar to those also found in facultatively sexual monogonont rotifers. We confirm that recognisability in bdelloids is not qualitatively different from other small understudied animals such as monogononts, and that sexual versus asexual reproduction does not lead to differences in morphological diversity patterns, as previously suggested based on interpretation of taxonomic revisions.     

CONSTRAINTS ON MAMMALIAN FORELIMB DEVELOPMENT: INSIGHTS FROM DEVELOPMENTAL DISPARITY

Tetrapod limb development has been studied extensively for decades, yet the strength and role of developmental constraints in this process remains unresolved. Mammals exhibit a particularly wide array of limb morphologies associated with various locomotion modes and behaviors, providing a useful system for identifying periods of developmental constraint and conserved developmental mechanisms or morphologies. In this study, landmark‐based geometric morphometrics are used to investigate levels and patterns of morphological diversity (disparity) among the developing forelimbs of four mammals with diverse limb morphologies: mice, opossums, horses, and pigs. Results indicate that disparity among the forelimbs of these species slightly decreases or stays the same from the appearance of the limb ridge to the bud stage, and increases dramatically from the paddle through tissue regression stages. Heterochrony exhibited by the precocial opossum limb was not found to drive these patterns of morphological disparity, suggesting that the low disparity of the middle stages of limb development (e.g., paddle stage) is driven by processes operating within the limb and is likely not a result of embryo‐wide constraint.     

Differing evolutionary patterns underlie convergence on elongate morphology in endemic fishes of Lake Waccamaw, North Carolina

An extensive body of research has recently demonstrated patterns of parallel and/or convergent evolution that arise from divergent natural selection pressures exerted across environmental gradients. These studies, although providing some of our best empirical evidence for natural selection, have focused on rather narrow phylogenetic scopes, more often than not comparing patterns of morphological change among closely‐related taxa within a single genus. Organisms in replicated populations in these studies are often assumed to have accomplished convergence via similar underlying processes. However, such assumptions cannot be made when looking at evolution across broader phylogenetic and ecological spectra. In the present study, we assessed morphological change across a much broader scale to test whether similar evolutionary and developmental patterns underlie convergence. Specifically, we studied morphological change that has occurred in a novel lake environment (Lake Waccamaw, North Carolina, USA) where three phylogenetically‐disparate fishes representing different orders have speciated and independently evolved streamlined morphologies relative to their deeper‐bodied progenitors occupying nearby streams and coastal regions. Geometric morphometric analyses revealed that, although the bulk of shape change between environments is similar across taxa, significant species‐specific responses, concordant with differing expectations based on the ecologies of these taxa, were also found. Moreover, allometry analyses indicated that the developmental patterns underlying this change also differ across taxa. The present study provides evidence that, within a common environment, convergence can be achieved by different evolutionary and developmental patterns in phylogenetically‐ and ecologically‐disparate taxa. Finally, these results contradict the commonly‐held hypothesis that fishes should be more streamlined in streams than lakes and emphasize the need to also consider other environmental characteristics, such as water clarity and physical complexity, in studies of divergence. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98 , 636–645.     

Allometric space and allometric disparity: a developmental perspective in the macroevolutionary analysis of morphological disparity

Here, we advance novel uses of allometric spaces--multidimensional spaces specifically defined by allometric coefficients--with the goal of investigating the focal role of development in shaping the evolution of morphological disparity. From their examination, operational measures of allometric disparity can be derived, complementing standard signals of morphological disparity through an intuitive and process-oriented refinement of established analytical protocols used in disparity studies. Allometric spaces thereby become a promising context to reveal different patterns of evolutionary developmental changes and to assess their relative prevalence and importance. Such spaces offer a novel domain of investigation of phenotypic variation and should help in detecting large-scale trends, thus placing various macroevolutionary phenomena in an explicitly developmental context. Ammonoidea (Cephalopoda) at the Lower-Middle Jurassic transition were chosen as a case study to illustrate this methodological approach. We constructed two phenotypic spaces: a static, adult one (adult morphospace) and a dynamic, developmental one (allometric space). Comparative disparity analyses show a strikingly stable occupation in both spaces, despite extensive change in taxonomic composition. In contrast, disparity analyses of subclades reveal clearly distinct morphological and allometric disparity dynamics. Allometric approaches allow developmental insights into morphological diversification otherwise intractable from the analysis of adult morphospace alone.     

Fossil evidence of evolutionary convergence in juvenile dental morphology and upper canine replacement in sabertooth carnivores

The convergent suite of morphological traits characterizing the mammalian sabertooth ecomorphology is well documented, including modifications of the dental and osteological portions of the masticatory apparatus from a less‐specialized carnivore condition. Equally important is how those specialized adult morphologies developed through ontogeny because previous studies have shown that growing such specialized craniodental traits may require evolutionary modification of growth patterns and tooth replacement mechanisms. Despite the understanding of convergent morphological specialization in adult sabertooth carnivores, the possibility of a convergent ontogenetic trajectory toward those adult morphologies has not been rigorously examined. The present study examines numerous previously undescribed juvenile nimravid specimens. The results provide insights about nimravid ontogeny and show, for the first time, that the nimravid sabertooth lineage included species in which the permanent upper canine erupted within a lingual concavity of the deciduous upper canine until it reached comparable crown height beyond the alveolar border. Furthermore, this investigation assesses the juvenile morphology and upper canine replacement of felid and barbourofelid sabertooth taxa. The results provide evidence of convergence in deciduous upper canine morphology of three sabertooth carnivore lineages (i.e., nimravid, felid, and barbourofelid), as well as preliminary evidence of convergence in the upper canine replacement process. It might be beneficial for studies of extreme morphological specialization to simultaneously consider convergence in adult morphologies and how morphologies change through ontogeny.     

Evolutionary integration of the frog cranium

Evolutionary integration (covariation) of traits has long fascinated biologists because of its potential to elucidate factors that have shaped morphological evolution. Studies of tetrapod crania have identified patterns of evolutionary integration that reflect functional or developmental interactions among traits, but no studies to date have sampled widely across the species-rich lissamphibian order Anura (frogs). Frogs exhibit a vast range of cranial morphologies, life history strategies, and ecologies. Here, using high-density morphometrics we capture cranial morphology for 172 anuran species, sampling every extant family. We quantify the pattern of evolutionary modularity in the frog skull and compare patterns in taxa with different life history modes. Evolutionary changes across the anuran cranium are highly modular, with a well-integrated “suspensorium” involved in feeding. This pattern is strikingly similar to that identified for caecilian and salamander crania, suggesting replication of patterns of evolutionary integration across Lissamphibia. Surprisingly, possession of a feeding larval stage has no notable influence on cranial integration across frogs. However, late-ossifying bones exhibit higher integration than early-ossifying bones. Finally, anuran cranial modules show diverse morphological disparities, supporting the hypothesis that modular variation allows mosaic evolution of the cranium, but we find no consistent relationship between degree of within-module integration and disparity.     

ADAPTIVE RADIATIONS,ECOLOGICAL SPECIALIZATION,AND THE EVOLUTIONARY INTEGRATION OF COMPLEX MORPHOLOGICAL STRUCTURES

The evolutionary integration of complex morphological structures is a macroevolutionary pattern in which morphogenetic components evolve in a coordinated fashion, which can result from the interplay among processes of developmental, genetic integration, and different types of selection. We tested hypotheses of ecological versus developmental factors underlying patterns of within‐species and evolutionary integration in the mandible of phyllostomid bats, during the most impressive ecological and morphological radiation among mammals. Shape variation of mandibular morphogenetic components was associated with diet, and the transition of integration patterns from developmental to within‐species to evolutionary was examined. Within‐species (as a proxy to genetic) integration in different lineages resembled developmental integration regardless of diet specialization, however, evolutionary integration patterns reflected selection in different mandibular components. For dietary specializations requiring extensive functional changes in mastication patterns or biting, such as frugivores and sanguivores, the evolutionary integration pattern was not associated with expected within‐species or developmental integration. On the other hand, specializations with lower mastication demands or without major functional reorganization (such as nectarivores and carnivores), presented evolutionary integration patterns similar to the expected developmental pattern. These results show that evolutionary integration patterns are largely a result of independent selection on specific components regardless of developmental modules.     

Do different disparity proxies converge on a common signal? Insights from the cranial morphometrics and evolutionary history of Pterosauria (Diapsida: Archosauria)

Disparity, or morphological diversity, is often quantified by evolutionary biologists investigating the macroevolutionary history of clades over geological timescales. Disparity is typically quantified using proxies for morphology, such as measurements, discrete anatomical characters, or geometric morphometrics. If different proxies produce differing results, then the accurate quantification of disparity in deep time may be problematic. However, despite this, few studies have attempted to examine disparity of a single clade using multiple morphological proxies. Here, as a case study for this question, we examine the disparity of the volant Mesozoic fossil reptile clade Pterosauria, an intensively studied group that achieved substantial morphological, ecological and taxonomic diversity during their 145+ million-year evolutionary history. We characterize broadscale patterns of cranial morphological disparity for pterosaurs for the first time using landmark-based geometric morphometrics and make comparisons to calculations of pterosaur disparity based on alternative metrics. Landmark-based disparity calculations suggest that monofenestratan pterosaurs were more diverse cranially than basal non-monofenestratan pterosaurs (at least when the aberrant anurognathids are excluded), and that peak cranial disparity may have occurred in the Early Cretaceous, relatively late in pterosaur evolution. Significantly, our cranial disparity results are broadly congruent with those based on whole skeleton discrete character and limb proportion data sets, indicating that these divergent approaches document a consistent pattern of pterosaur morphological evolution. Therefore, pterosaurs provide an exemplar case demonstrating that different proxies for morphological form can converge on the same disparity signal, which is encouraging because often only one such proxy is available for extinct clades represented by fossils. Furthermore, mapping phylogeny into cranial morphospace demonstrates that pterosaur cranial morphology is significantly correlated with, and potentially constrained by, phylogenetic relationships.     

Evolutionary constraints in hind wing shape in Chinese dung beetles (Coleoptera: Scarabaeinae)

This study examines the evolution hindwing shape in Chinese dung beetle species using morphometric and phylogenetic analyses. Previous studies have analyzed the evolution of wing shape within a single or very few species, or by comparing only a few wing traits. No study has analyzed wing shape evolution of a large number of species, or quantitatively compared morphological variation of wings with proposed phylogenetic relationships. This study examines the morphological variation of hindwings based on 19 landmarks, 119 morphological characters, and 81 beetle species. Only one most parsimonious tree (MPT) was found based on 119 wing and body characters. To better understand the possible role of the hindwing in the evolution of Scarabaeinae, additional phylogenetic analyses were proposed based on the only body features (106 characters, wing characters excluded). Two MPT were found based on 106 body characters, and five nodes were collapsed in a strict consensus. There was a strong correlation between the morphometric tree and all phylogenetic trees (r>0.5). Reconstructions of the ancestral wing forms suggest that Scarabaeinae hindwing morphology has not changed substantially over time, but the morphological changes that do occur are focused at the base of the wing. These results suggest that flight has been important since the origin of Scarabaeinae, and that variation in hindwing morphology has been limited by functional constraints. Comparison of metric disparity values and relative evolutionary sequences among Scarabaeinae tribes suggest that the primitive dung beetles had relatively diverse hindwing morphologies, while advanced dung beetles have relatively similar wing morphologies. The strong correlation between the morphometric tree and phylogenetic trees suggest that hindwing features reflect the evolution of whole body morphology and that wing characters are suitable for the phylogenetic analyses. By integrating morphometric and cladistic approaches, this paper sheds new light on the evolution of dung beetle hind wings.     

Did natural selection or genetic drift produce the cranial diversification of neotropical monkeys?

A central controversy among biologists is the relative importance of natural selection and genetic drift as creative forces shaping biological diversification (Fisher 1930; Wright 1931). Historically, this controversy has been an effective engine powering several evolutionary research programs during the last century (Provine 1989). While all biologists agree that both processes operate in nature to produce evolutionary change, there is a diversity of opinion about which process dominates at any particular organizational level (from DNA and proteins to complex morphologies). To address this last level, we did a broadscale analysis of cranial diversification among all living New World monkeys. Quantitative genetic models yield specific predictions about the relationship between variation patterns within and between populations that may be used to test the hypothesis that genetic drift is a sufficient explanation for morphological diversification. Diversity at several levels in a hierarchy of taxonomic/phylogenetics relationship was examined from species within genera to families within superfamilies. The major conclusion is that genetic drift can be ruled out as the primary source of evolutionary diversification in cranial morphology among taxa at the level of the genus and above as well as for diversification of most genera. However, drift may account for diversification among species within some Neotropical primate genera, implying that morphological diversification associated with speciation need not be adaptive in some radiations.     

Analysing disparity by applying combined morphological and molecular approaches to French and Japanese carabid beetles

The expression of morphological disparity within a clade is related to its history and to the environmental parameters within which it develops. Recent developments in geometric morphometries allow quantitative estimation of morphological disparity, and facilitate comparisons with genetic data intended to provide phylogenetic information. Such comparisons were made between two sets of ground beetle species from regions that differ biogeographically and environmentally: 12 post-glacial reinvading species from NE France; and 15 Japanese species less likely to be affected by the Pleistocene glacial events. Genetic relationships were inferred from mitochondrial DNA (ND5 gene). Morphological divergences among the species were analysed using Procrustes ver. 2.0, based on 64 landmarks (generalized analyses and computation of additive distance trees). The established morphospaces indicate distinct disparity patterns in France and Japan, even though the genetic data show that neither of the two sets arc monophyletic, and that they are in fact intermixed in the same clade. This discrepancy is partly related to the presence of extreme (elongated) morphologies in the Japanese set. But the stronger disparity observed amongjapanese species does not correspond to greater genetic differences. Those extreme morphologies appear to be related to the degree of endemicity of the species. The differences between the French and Japanese morphological patterns are discussed in the context of possible geographic factors and climatic changes during the Pleistocene.     

Patterns of Evolutionary Divergence and Convergence in the Bushy-Tailed Woodrat (Neotoma cinerea) Across Western North America

The degree of concordance between patterns of divergence in genetic and morphological characters provides insight into the process of evolutionary diversification. We analyzed species-wide morphological variation in a broadly distributed species of small mammal, the bushy-tailed woodrat (Neotoma cinerea), for comparison against a recently developed mitochondrial phylogeny. We focused our analyses on patterns of qualitative and quantitative craniodental morphological variation throughout the distribution of this taxon. We found strong concordance between the morphology of one prominent craniodental feature (sphenopalatine vacuity) and the major mitochondrial lineages, but only minimal differentiation in overall morphometric variation between these clades. Further, in contrast to the largely east–west subdivision of mitochondrial and sphenopalatine vacuity variation, cluster analyses of morphometric variation revealed a north–south morphological subdivision irrespective of mitochondrial clade. Our combined character sets are best explained by a deep history of evolutionary divergence within this taxon accompanied or followed by broad-scale convergent or parallel evolution.     

Contrasting global‐scale evolutionary radiations: phylogeny,diversification, and morphological evolution in the major clades of iguanian lizards

Parallel evolutionary radiations in adjacent locations have been documented in many systems, but typically at limited geographical scales. Here, we compare patterns of evolutionary radiation at the global scale in iguanian lizards, the dominant clade of lizards. We generated a new time‐calibrated phylogeny including 153 iguanian species (based on mitochondrial and nuclear data) and obtained data on morphology and microhabitats. We then compared patterns of species diversification, morphological disparity, and ecomorphological relationships in the predominantly Old World and New World clades (Acrodonta and Pleurodonta, respectively), focusing on the early portions of these radiations. Acrodonts show relatively constant rates of species diversification and disparity over time. In contrast, pleurodonts show an early burst of species diversification and less‐than‐expected morphological disparity early in their history, and slowing diversification and increasing disparity more recently. Analyses including all species (with MEDUSA) suggest accelerated diversification rates in certain clades within both Acrodonta and Pleurodonta, which strongly influences present‐day diversity patterns. We also find substantial differences in ecomorphological relationships between these clades. Our results demonstrate that sister clades in different global regions can undergo very different patterns of evolutionary radiation over similar time frames. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ●● , ●●–●●.     

Combining ontogenetic and evolutionary scales of morphological disparity: a study of early Jurassic ammonites

Two major research themes in Evolutionary Developmental Biology and in Paleobiology, respectively, have each become central for the analysis and interpretation of morphological changes in evolution: the study of ontogeny/phylogeny connections, mainly within the widespread and controversial framework of heterochrony; and the study of morphological disparity, the morphological signal of biodiversity, describing secular changes in morphospace occupation during the history of any given clade. Although enriching in their respective fields, these two themes have remained rather isolated to date, despite the potential value of integrating them as some recent studies begin to suggest. Here, we explore the recent notion of developmental morphospace-morphospace carrying ontogenetic information-as a potential tool for bridging the gap between disparity dynamics and developmental dynamics. We elaborate this approach with a case study of Early Jurassic ammonite family Hildoceratidae (Mollusca, Cephalopoda). Morphometric analyses of the shell shape of 20 species spanning the morphological spectrum of the family are used to quantify and contrast juvenile and adult disparity levels. Adult disparity is significantly greater than juvenile disparity at the family level; yet, some subclades also display different patterns. In addition, comparisons of ontogenetic trajectories underline the prevalence of heterochrony-based evolutionary modifications within subfamilies (via ontogenetic scaling); they also point to the probable existence of pervasive developmental constraints structuring inhomogeneous morphospace occupation.