Morphological evolution of the lizard skull: a geometric morphometrics survey

Patterns of diversity among lizard skulls were studied from a morphological, phylogenetic, and functional perspective. A sample of 1,030 lizard skulls from 441 species in 17 families was used to create a lizard skull morphospace. This morphospace was combined with a phylogeny of lizard families to summarize general trends in the evolution of the lizard skull. A basal morphological split between the Iguania and Scleroglossa was observed. Iguanians are characterized by a short, high skull, with large areas of attachment for the external adductor musculature, relative to their sister group. The families of the Iguania appear to possess more intrafamilial morphological diversity than families of the Scleroglossa, but rarefaction of the data reveals this to be an artifact caused by the greater number of species represented in Iguanian families. Iguanian families also appear more dissimilar to one another than families of the Scleroglossa. Permutation tests indicate that this pattern is real and not due to the smaller number of families in the Iguanidae. Parallel and convergent evolution is observed among lizards with similar diets: ant and termite specialists, carnivores, and herbivores. However, these patterns are superimposed over the more general phylogenetic pattern of lizard skull diversity. This study has three central conclusions. Different clades of lizards show different patterns of disparity and divergence in patterns of morphospace occupation. Phylogeny imposes a primary signal upon which a secondary ecological signal is imprinted. Evolutionary patterns in skull metrics, taken with functional landmarks, allow testing of trends and the development of new hypotheses concerning both shape and biomechanics.     

Phenotypic diversification and island evolution of pipistrelle bats (Pipistrellus pipistrellus group) in the Mediterranean region inferred from geometric morphometrics and molecular phylogenetics

Aim The Mediterranean Basin is a centre of radiation for numerous species groups. To increase our understanding of the mechanisms underlying speciation and radiation events in this region, we assessed the phenotypic variability within the Pipistrellus pipistrellus–pygmaeus–hanaki species complex. Although bats form the second largest mammalian order, studies of insular evolution in this group are scarce. We approached this problem from a microevolutionary perspective and tested for the recurrence of the insular syndrome. Location The Mediterranean Basin, with a special focus on isolated populations from Corsica, the Maghreb, Cyprus, Cyrenaica and Crete. Methods Phenotypic variability was assessed by cranial morphometrics using the coordinates of 41 3D landmarks and associated geometric‐morphometric methods. We analysed 125 specimens representing all of the lineages in the species complex. Differences between taxa and between insular and continental populations in cranial size, shape, form and allometries were tested using analyses of variance and visualized using boxplots and canonical variate analysis. Relationships between molecular data from a previous study (cytochrome b sequences) and morphometric data were tested with co‐inertia analyses (RV test) and multivariate regressions. Results The three species were relatively well differentiated in cranial size and shape, and each species showed a significant amount of inter‐population variability. Comparisons of pairs of insular versus continental populations revealed heterogeneities in cranial patterns among island phenotypes, suggesting no recurrent insular syndrome. Molecular and phenotypic traits were correlated, except for molecular and lateral cranium shape. Main conclusions The Pipistrellus pipistrellus – pygmaeus – hanaki species complex exhibits phenotypic variability as a result of the fragmentation of its distribution (especially on islands), its phylogenetic and phylogeographic history and, most probably, other evolutionary factors that were not investigated in this study. We found no recurrent pattern of evolution on islands, indicating that site‐specific factors play a prevailing role on Mediterranean islands. The correlation between molecular and phenotypic data is incomplete, suggesting that factors other than phylogenetic relationships, potentially connected with feeding ecology, have played a role in shaping cranial morphology in this species complex.     

Character variation in separate body regions of Gerreidae (Osteichthyes: Teleostei) fishes inferred from geometric morphometrics

Body morphology is a valuable feature for distinguishing teleostean fishes. However, the utility of character variation in separate body regions has yet to be tested. The taxonomy of the Gerreidae family is controversial due to character overlapping among its fish species. This work aims to analyze and compare the body shape variation in three regions, cephalic, trunk, and caudal peduncle, using landmark data and geometric morphometric methods in 17 species and five genera of the family Gerreidae. The pattern of shape variation for the cephalic region consisted of well-defined character states exclusive of each species analyzed. Shape variation in the trunk and caudal peduncle regions does not distinguish all species in this study. This study showed that the dorsal cephalic profile is highly variable among the species, therefore, shape variation in this region is useful for distinguishing Gerreidae species. In contrast, some species within the same genus share similar shape states in the trunk and caudal peduncle regions, with the most shape variation in the dorsal profile and anal fin for the trunk and in the middle of the caudal peduncle.     

Egg size evolution in tropical American arcid bivalves: the comparative method and the fossil record

Marine organisms exhibit a wide range of egg sizes, even among closely related taxa, and egg size is widely considered to be one of the most important components of the life histories of marine species. The nature of the trade-off between egg size and number and the consequences of variation in egg size for offspring growth and survivorship have been extensively modeled. Yet, there is little empirical evidence that supports the relative importance of particular environmental parameters in engendering the tremendous variation in egg size seen in marine organisms. This study compares egg sizes between six geminate species pairs of bivalves in the family Arcidae to determine whether egg size differs in predictable directions between geminate species in the two oceans separated by the Central American isthmus, and whether the direction and timing of egg size evolution among geminates in this family is correlated with both modern and paleoceanographic patterns of oceanic productivity. In all modern members of six geminate pairs, egg size was larger in the species in the western Atlantic than in its sister species the eastern Pacific. This pattern supports the hypothesis that optimal egg size differs in the two oceans due to the low productivity and poor larval feeding environment in the western Atlantic relative to the eastern Pacific. The fossil record of one geminate pair shows that egg size has remained consistently large in the western Atlantic from the Miocene to the Recent, while egg size in the eastern Pacific has decreased to the current small size in less than 2 million years; this suggests that modern-day differences between egg sizes in the western Atlantic and eastern Pacific are due to either an increase in productivity in the eastern Pacific and subsequent selection for smaller eggs in that ocean, or differential patterns of extinction that occurred well after the rise of the isthmus. These results agree with ancestral character state reconstruction using linear parsimony, but differ from squared-change parsimony reconstructions.     

The evolution of cranial form and function in theropod dinosaurs: insights from geometric morphometrics

Theropod dinosaurs, an iconic clade of fossil species including Tyrannosaurus and Velociraptor, developed a great diversity of body size, skull form and feeding habits over their 160+ million year evolutionary history. Here, we utilize geometric morphometrics to study broad patterns in theropod skull shape variation and compare the distribution of taxa in cranial morphospace (form) to both phylogeny and quantitative metrics of biting behaviour (function). We find that theropod skulls primarily differ in relative anteroposterior length and snout depth and to a lesser extent in orbit size and depth of the cheek region, and oviraptorosaurs deviate most strongly from the "typical" and ancestral theropod morphologies. Noncarnivorous taxa generally fall out in distinct regions of morphospace and exhibit greater overall disparity than carnivorous taxa, whereas large-bodied carnivores independently converge on the same region of morphospace. The distribution of taxa in morphospace is strongly correlated with phylogeny but only weakly correlated with functional biting behaviour. These results imply that phylogeny, not biting function, was the major determinant of theropod skull shape.     

The utility of cranial ontogeny for phylogenetic inference: a case study in crocodylians using geometric morphometrics

The degree to which the ontogeny of organisms could facilitate our understanding of phylogenetic relationships has long been a subject of contention in evolutionary biology. The famed notion that ‘ontogeny recapitulates phylogeny’ has been largely discredited, but there remains an expectation that closely related organisms undergo similar morphological transformations throughout ontogeny. To test this assumption, we used three‐dimensional geometric morphometric methods to characterize the cranial morphology of 10 extant crocodylian species and construct allometric trajectories that model the post‐natal ontogenetic shape changes. Using time‐calibrated molecular and morphological trees, we employed a suite of comparative phylogenetic methods to assess the extent of phylogenetic signal in these trajectories. All analyses largely demonstrated a lack of significant phylogenetic signal, indicating that ontogenetic shape changes contain little phylogenetic information. Notably, some Mantel tests yielded marginally significant results when analysed with the morphological tree, which suggest that the underlying signal in these trajectories is correlated with similarities in the adult cranial morphology. However, despite these instances, all other analyses, including more powerful tests for phylogenetic signal, recovered statistical and visual evidence against the assumption that similarities in ontogenetic shape changes are commensurate with phylogenetic relatedness and thus bring into question the efficacy of using allometric trajectories for phylogenetic inference.     

Phylogeny of the superfamily Gelechioidea (Lepidoptera: Obtectomera), with an exploratory application on geometric morphometrics

The superfamily Gelechioidea (Lepidoptera: Obtectomera) has a high species diversity. It consists of more than 18,400 described species and has a global distribution. Among it, large numbers of species were reported to be economically important to people's production and life. However, relationships among families or subfamilies in Gelechioidea have been exceptionally difficult to resolve using morphology or single gene genealogies. Multiple gene genealogies had been used in the molecular phylogenetic studies on Gelechioidea during the past years, but their phylogenetic relationships remain to be controversial mainly due to their limited taxa sampling relative to such high species diversity. In this paper, 89 ingroup species representing 55 genera are sequenced and added to the data downloaded from GenBank, and six species representing four closely related superfamilies are chosen as outgroup. The molecular phylogeny of Gelechioidea is reconstructed based on the concatenated data set composed of one mitochondrial marker (COI) and seven nuclear markers (CAD, EF-1ɑ, GAPDH, IDH, MDH, RpS5, wingless). The phylogenetic results, taking into consideration of the comparative morphological study, show that the clade of Gelechioidea is strongly supported and separated from other superfamilies, which further proves its monophyly. Five families are newly defined: Autostichidae sensu nov., Depressariidae sensu nov., Peleopodidae sensu nov., Ashinagidae sensu nov. and Epimarptidae sensu nov. Meanwhile, a monophyletic “SSABM” clade considered to be closely related is proposed for the first time, consisting of Stathmopodidae, Scythrididae, Ashinagidae, Blastobasidae and Momphidae. Moreover, geometric morphometric analyses using merged landmark data set from fore and hind wings of 118 representative species are conducted. The phenetic tree shows that the monophyly and phylogenetic relationships correspond with the results of molecular phylogeny largely, which well proves its importance and potential application in both phylogenetic reconstruction and species identification.     

Multivariate and geometric morphometrics in the analysis of sexual dimorphism variation in Podarcis lizards

Podarcis bocagei and P. carbonelli are two closely related lacertid species, very similar morphologically and ecologically. We investigated sexual dimorphism patterns presented by both species in allopatry and in sympatry. Sexual size and shape dimorphism patterns were analyzed using both multivariate and geometric morphometric techniques. Multivariate morphometrics revealed a marked sexual dimorphism in both species--males being larger with more robust habitus and females presenting a longer trunk. General patterns of sexual size dimorphism are not modified in sympatry, although there is evidence for some morphological change in male head size. The application of geometric morphometrics offered a more detailed image of head shape and revealed that males present a more developed tympanic area than do females, while females have a more rounded head. Differences in the degree of sexual shape dimorphism were detected in sympatry, but no consistent patterns were observed. From the results of the study, and based on previous knowledge on the populations studied, we conclude that the morphological differences observed are probably not caused by exploitative competition between the species, but rather appear attributable to the modification of the relative influence of sexual and natural selection on both sexes.     

Geometric morphometrics: recent applications to the study of evolution and development

The field of morphometrics is developing quickly and recent advances allow for geometric techniques to be applied easily to many zoological problems. This paper briefly introduces geometric morphometric techniques and then reviews selected areas where those techniques have been applied to questions of general interest. This paper is relevant to non-specialists looking for an entry into geometric morphometric methods and for ideas of how to incorporate them into the study of variation within and between species, the measurement of developmental stability, the role of development in shaping evolution and the special problem of measuring the shape of fossil specimens that are deformed from their original shape.     

Testing different 3D techniques using geometric morphometrics: Implications for cranial fluctuating asymmetry in humans

This study aimed to test the performance of 3D digitizer, CT scanner, and surface scanner in detecting cranial fluctuating asymmetry. Sets of 32 landmarks (6 in the midline and 13 bilateral) were acquired from 14 archeological crania using a 3D digitizer, and from 3D models generated from a CT scanner and surface scanner using Viewbox 4. Levels of shape variation were analyzed in MorphoJ using Procrustes analysis of variance and Principal component analysis. Intra-observer error accounted for 1.7%, 1.8%, and 4.5% of total shape variation for 3D digitizer, CT scanner, and surface scanner respectively. Fluctuating asymmetry accounted for 15%–16% of total shape variation. Variation between techniques accounted for 18% of total shape variation. We found a higher level of missing landmarks in our surface scan data than for both 3D digitizer and CT scanner data, and both 3D model-based techniques sometimes obscured taphonomic damage. All three 3D techniques are appropriate for measuring cranial fluctuating asymmetry. We advise against combining data collected with different techniques.     

Ecology and evolution of the diaspore "burial syndrome"

Hygroscopically active awns or "bristles" have long intrigued scientists. Experimental evidence shows that they are important for diaspore burial in the correct orientation, thereby increasing successful seed germination and seedling survival. Despite these ecological advantages, 38 of the 280 species of grasses in Danthonioideae lack awns. We provide the first study of awns in a phylogenetic context and show that although the awnless state has arisen ca. 25 times independently, the ecological disadvantage of not having an awn also applies in an evolutionary context. Only in Tribolium and Schismus have awnless ancestors diversified to form a clade of primarily awnless descendents. Several of the awnless species in these genera are annual and we find a significant correlation between the evolution of awns and the evolution of life history. A suite of other diaspore traits accompany the awned or awnless states. We interpret the awn as being the visible constituent of a compound "burial syndrome," the two ecological extremes of which may explain the correlation between awns and life history and provide an explanation why awnless species in Tribolium and Schismus persist.     

蜣螂后胸叉骨的几何形态学分析及其适应进化研究

【目的】甲虫的后胸叉骨是基部位于后足基节关节处,端部游离在胸腔内的几丁质构成的内骨骼。后胸叉骨作为胸腹部运动肌肉的联结点,在甲虫运动过程中扮演了重要角色,同时也承载了分类和系统发育信息。蜣螂根据其习性可分为滚粪球和直接掘洞两类行为类型。通过传统的比较形态学方法,我们无法得知滚粪球或直接掘洞的行为对后胸叉骨形态的影响。本研究旨在利用定量的几何形态学方法探究蜣螂后胸叉骨形态对不同行为选择压力的响应关系。【方法】对76种蜣螂后胸叉骨的形态多样性进行二维几何形态学定量评估;利用显微CT和计算机三维重建方法,对直接掘洞类蜣螂和滚粪球类蜣螂的代表种西班牙粪蜣螂Copris hispanus和忠诚泽蜣螂Kheper devotus的后胸叉骨进行三维重建,用于比较两者的三维形态差异。【结果】经过几何形态学分析可知,两类蜣螂后胸叉骨背面观和侧面观的马氏距离和普氏距离的p值均低于0.0001,表明两类蜣螂的后胸叉骨的形态存在显著性差异;通过对C.hispanus和K.devotus后胸叉骨3D模型的比较发现,两类蜣螂后胸叉骨的最大区别在于后胸叉骨的端半部(叉臂和中突)。前者的叉臂细长,中突面积大,背立脊呈窄条状且不发达;后者的叉臂宽扁,叉臂基半部十分宽大,中突面积小,背立脊呈鳍状且十分发达。【结论】滚粪球或直接掘洞的行为会对蜣螂后胸叉骨的形态有显著性影响,蜣螂后胸叉骨形态与滚粪球和直接掘洞两种行为的选择压力显著相关,这与后胸叉骨所附着的胸部肌肉参与相关运动关系密切。本研究为探索昆虫形态与功能关系提供了一个有益范例。     

Correlated evolution of body and fin morphology in the cichlid fishes

Body and fin shapes are chief determinants of swimming performance in fishes. Different configurations of body and fin shapes can suit different locomotor specializations. The success of any configuration is dependent upon the hydrodynamic interactions between body and fins. Despite the importance of body–fin interactions for swimming, there are few data indicating whether body and fin configurations evolve in concert, or whether these structures vary independently. The cichlid fishes are a diverse family whose well‐studied phylogenetic relationships make them ideal for the study of macroevolution of ecomorphology. This study measured body, and caudal and median fin morphology from radiographs of 131 cichlid genera, using morphometrics and phylogenetic comparative methods to determine whether these traits exhibit correlated evolution. Partial least squares canonical analysis revealed that body, caudal fin, dorsal fin, and anal fin shapes all exhibited strong correlated evolution consistent with locomotor ecomorphology. Major patterns included the evolution of deep body profiles with long fins, suggestive of maneuvering specialization; and the evolution of narrow, elongate caudal peduncles with concave tails, a combination that characterizes economical cruisers. These results demonstrate that body shape evolution does not occur independently of other traits, but among a suite of other morphological changes that augment locomotor specialization.     

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.     

The evolution and maintenance of delayed implantation in the mustelidae (mammalia: carnivora)

Diapause, the temporary cessation of development at an early life-history stage, is widespread among animals and plants. The range of taxa exhibiting various forms of diapause indicates its enormous ecological significance and highlights its value as a model for examining life-history trait evolution. However, despite the impact of diapause on species ecology, there is little understanding of its adaptive value in many groups. Furthermore, the relative roles of phylogeny and ecology in determining the contemporary expression of the trait remain unresolved. Delayed implantation (DI) is a type of diapause found in several orders of mammals. It is particularly prevalent in the Mustelidae, with mustelids making up more than half of all mammals known to exhibit DI. This taxon is thus ideal for examining life-history predictors of DI and investigating the mode of evolution. Both maximum likelihood and maximum parsimony methods of ancestral state reconstruction indicated DI to be plesiomorphic in the mustelids, although multiple state changes are required to explain its contemporary distribution. After controlling for phylogeny, species with and without DI could be discriminated using just three variables: longevity, maximum latitude of the geographical distribution, and a term describing maternal investment. Our analyses supported the hypothesis that DI is more prevalent in seasonal climates. We also showed that longer-lived species are more likely to exhibit DI, suggesting a time cost to the trait. We found no correlate for the highly variable duration of DI, which remains unexplained. Although ecological factors can predict the distribution of DI in modern mustelids, phylogenetic constraint is likely to play an important role.