Patterns of intracolumnar size variation inform the heterochronic mechanisms underlying extreme body shape divergence in microcephalic sea snakes

Sea snakes (Hydrophiinae) that specialize on burrowing eel prey have repeatedly evolved tiny heads and reduced forebody relative to hindbody girths. Previous research has found that these “microcephalic” forms have higher counts of precaudal vertebrae, and postnatal ontogenetic changes cause their hindbodies to reach greater girths relative to their forebodies. We examine variation in vertebral size along the precaudal axis of neonates and adults of three species. In the nonmicrocephalic Hydrophis curtus, these intracolumnar patterns take the form of symmetrical curved profiles, with longer vertebrae in the midbody (50% of body length) relative to distal regions. In contrast, intracolumnar profiles in the microcephalic H. macdowelli and H. obscurus are strongly asymmetrical curves (negative skewness) due to the presence of numerous, smaller‐sized vertebrate in the forebody (anterior to the heart). Neonate and adult H. macdowelli and H. obscurus specimens all exhibit this pattern, implying an onset of fore‐ versus hindbody decoupling in the embryo stage. Based on this, we suggest plausible developmental mechanisms involving the presence and positioning of Hox boundaries and heterochronic changes in segmentation. Tests of our hypotheses would give new insights into the drivers of rapid convergent shifts in evolution, but will ultimately require studies of gene expression in the embryos of relevant taxa.     

Evolution of extreme ontogenetic allometric diversity and heterochrony in pythons,a clade of giant and dwarf snakes

Ontogenetic allometry, how species change with size through their lives, and heterochony, a decoupling between shape, size, and age, are major contributors to biological diversity. However, macroevolutionary allometric and heterochronic trends remain poorly understood because previous studies have focused on small groups of closely related species. Here, we focus on testing hypotheses about the evolution of allometry and how allometry and heterochrony drive morphological diversification at the level of an entire species‐rich and diverse clade. Pythons are a useful system due to their remarkably diverse and well‐adapted phenotypes and extreme size disparity. We collected detailed phenotype data on 40 of the 44 species of python from 1191 specimens. We used a suite of analyses to test for shifts in allometric trajectories that modify morphological diversity. Heterochrony is the main driver of initial divergence within python clades, and shifts in the slopes of allometric trajectories make exploration of novel phenotypes possible later in divergence history. We found that allometric coefficients are highly evolvable and there is an association between ontogenetic allometry and ecology, suggesting that allometry is both labile and adaptive rather than a constraint on possible phenotypes.     

Evolutionary history of elongation and maximum body length in moray eels (Anguilliformes: Muraenidae)

Body shape and size are important axes of organismal diversification. The elongate body form has evolved repeatedly in disparate vertebrate clades, and is associated with a variety of maximum body lengths. We used a time‐calibrated phylogeny for 40 species of moray eels to analyse the evolution of elongation and the morphological mechanisms underlying variation in body shape and maximum body length. We find that body elongation in morays evolves independently of elongation of the vertebral column. In contrast, maximum body length evolves by a different mechanism: through region‐specific increases in vertebral number, elongation of individual vertebral centra, and postembryonic somatic growth. We reconstruct an ancestral moray eel and provide evidence for accelerated morphological evolution in three highly elongate species that are associated with a burrowing lifestyle. We compare these patterns with those described for other vertebrates, and show that body shape and body length may evolve independently of each other and (in the case of shape) of the vertebral column. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 861–875.     

The ontogenetic allometry of body morphology and chemical composition in dairy goat wethers

We studied the ontogenetic growth of goat wethers (castrated male goats) of the Saanen and Swiss Alpine breeds based on a large range of intraspecific body mass (BM). The body parts and the chemical constituents of the empty body were described by the allometric function by using BM and the empty body mass (EBM) as the predictors for morphological traits and chemical composition, respectively. We fitted the allometric scaling function by applying the SAS NLMIXED procedure, but to evaluate assumptions regarding variances in morphological and compositional traits, we combined the scaling function with homoscedastic (MOD1), and the heteroscedastic exponential (MOD2) and power-of-the-mean (MOD3) variance functions. We also predicted the ontogenetic growth by using the traditional log-log transformation and back-transformed results into the arithmetic scale (MOD4). We obtained predictions from MOD4 in the arithmetic scale by a two-step process, and evaluated MOD1, MOD2 and MOD3 by a model selection framework, and compared MOD4 with MOD1, MOD2 and MOD3 based on goodness-of-fit measures. Based on information criteria for model selection, heterogeneous variance functions were more likely to describe 10 over 36 traits with a low level of model selection uncertainty. One trait was predicted by averaging the MOD1 and MOD2 variance functions; and nine traits were better described by averaging the MOD2 and MOD3 variance functions. The predictions for other 16 traits were averaged from MOD1, MOD2 and MOD3. However, MOD4 better described 11 traits according to the goodness-of-fit measures. Depending on the variable being analyzed, the body parts and the chemical amounts exhibited the three types of allometric behavior with respect to BM and EBM, that is, positive, negative and isometric ontogenetic growth. Reference BMs, that is, 20, 27, 35 and 45 kg, were used to compute the net protein and energy requirements based on the first derivative of the scaling function, and the results were presented in reference to the EBM and EBM^0.75. Both the net protein and energy requirements scaled to EBM^0.75 increased from 20 to 45 kg of BM.     

Postmetamorphic ontogenetic allometry and the evolution of skull shape in Nest‐building frogs Leptodactylus (Anura: Leptodactylidae)

Allometry constitutes an important source of morphological variation. However, its influence in head development in anurans has been poorly explored. By using geometric morphometrics followed by statistical and comparative methods we analyzed patterns of allometric change during cranial postmetamorphic ontogeny in species of Nest‐building frogs Leptodactylus (Leptodactylidae). We found that the anuran skull is not a static structure, and allometry plays an important role in defining its shape in this group. Similar to other groups with biphasic life‐cycle, and following a general trend in vertebrates, ontogenetic changes mostly involve rearrangement in rostral, otoccipital, and suspensorium regions. Ontogenetic transformations are paralleled by shape changes associated with evolutionary change in size, such that the skulls of species of different intrageneric groups are scaled to each other, and small and large species show patterns of paedomorphic/peramorphic features, respectively. Allometric trajectories producing those phenotypes are highly evolvable though, with shape change direction and magnitude varying widely among clades, and irrespective of changes in absolute body size. These results reinforce the importance of large‐scale comparisons of growth patterns to understand the plasticity, evolution, and polarity of morphological changes in different clades.     

The evolution of extreme shell shape variation in the land snail Ainohelix editha: a phylogeny and hybrid zone analysis

Ainohelix editha from Hokkaido, Japan, exhibit great geographical variation in their shell morphology. In particular, A. editha in two quite separate locations, Shimamaki and Samani, are striking because they are extremely flat and have a sharp keel, whereas at adjacent sites the shells are globular or depressed-globular. We used mitochondrial 16S rRNA and nuclear ITS-2 sequences to infer a phylogeny among 47 snails from 29 locations. Snails from the two keeled-flat populations clustered separately in the phylogeny, suggesting that this unusual shell form could have evolved independently. A morphological analysis of shells collected along a transect between keeled-flat and globular snail sites showed a cline for shell shape and the angle of the keel. Two different mtDNA lineages were found across the transect, with a cline for an ITS-2 single nucleotide polymorphism. Together, the results may suggest a lack of reproductive isolation between keeled-flat and globular snails, with possible introgression by hybridization.     

Chondrocranial development in larval Rana sylvatica (Anura: Ranidae): morphometric analysis of cranial allometry and ontogenetic shape change

This study provides baseline quantitative data on the morphological development of the chondrocranium in a larval anuran. Both linear and geometric morphometric methods are used to quantitatively analyze size-related shape change in a complete developmental series of larvae of the wood frog, Rana sylvatica. The null hypothesis of isometry was rejected in all geometric morphometric and most linear morphometric analyses. Reduced major axis regressions of 11 linear chondrocranial measurements on size indicate a mixture of allometric and isometric scaling. Measurements in the otic and oral regions tend to scale with negative allometry and those associated with the palatoquadrate and muscular process scale with isometry or positive allometry. Geometric morphometric analyses, based on a set of 11 chondrocranial landmarks, include linear regression of relative warp scores and multivariate regression of partial warp scores and uniform components on log centroid size. Body size explains about one-quarter to one-third of the total shape variation found in the sample. Areas of regional shape transformation (e.g., palatoquadrate, otic region, trabecular horns) are identified by thin-plate spline deformation grids and are concordant with linear morphometric results. Thus, the anuran chondrocranium is not a static structure during premetamorphic stages and allometric patterns generally follow scaling predictions for tetrapod cranial development. Potential implications regarding larval functional morphology, cranial development, and chondrocranial evolution in anurans are discussed.     

Patterns of cranial ontogeny in lacertid lizards: morphological and allometric disparity

We explored the ontogenetic dynamics of the morphological and allometric disparity in the cranium shapes of twelve lacertid lizard species. The analysed species (Darevskia praticola, Dinarolacerta mosorensis, Iberolacerta horvathi, Lacerta agilis, L. trilineata, L. viridis, Podarcis erhardii, P. melisellensis, P. muralis, P. sicula, P. taurica and Zootoca vivipara) can be classified into different ecomorphs: terrestrial lizards that inhabit vegetated habitats (habitats with lush or sparse vegetation), saxicolous and shrub‐climbing lizards. We observed that there was an overall increase in the morphological disparity (MD) during the ontogeny of the lacertid lizards. The ventral cranium, which is involved in the mechanics of jaw movement and feeding, showed higher levels of MD, an ontogenetic shift in the morphospace planes and more variable allometric patterns than more conserved dorsal crania. With respect to ecology, the allometric trajectories of the shrub‐climbing species tended to cluster together, whereas the allometric trajectories of the saxicolous species were highly dispersed. Our results indicate that the ontogenetic patterns of morphological and allometric disparity in the lacertid lizards are modified by ecology and functional constraints and that the identical mechanisms that lead to intraspecific morphological variation also produce morphological divergence at higher taxonomic levels.     

The complex ecology of genitalia: Gonopodium length and allometry in the Trinidadian guppy

Male genitalia present an extraordinary pattern of rapid divergence in animals with internal fertilization, which is usually attributed to sexual selection. However, the effect of ecological factors on genitalia divergence could also be important, especially so in animals with nonretractable genitalia because of their stronger interaction with the surrounding environment in comparison with animals with retractable genitalia. Here, we examine the potential of a pervasive ecological factor (predation) to influence the length and allometry of the male genitalia in guppies. We sampled guppies from pairs of low‐predation (LP) and high‐predation (HP) populations in seven rivers in Trinidad, and measured their body and gonopodium length. A key finding was that HP adult males do not have consistently longer gonopodia than do LP adult males, as had been described in previous work. However, we did find such divergence for juvenile males: HP juveniles have longer gonopodia than do LP juveniles. We therefore suggest that an evolutionary trend toward the development of longer gonopodia in HP males (as seen in the juveniles) is erased after maturity owing to the higher mortality of mature males with longer gonopodia. Beyond these generalities, gonopodium length and gonopodium allometry were remarkably variable among populations even within a predation regime, thus indicating strong context dependence to their development/evolution. Our findings highlight the complex dynamics of genitalia evolution in Trinidadian guppies.     

Integration and modularity of teleostean pectoral fin shape and its role in the diversification of acanthomorph fishes

Phenotypic integration and modularity describe the strength and pattern of interdependencies between traits. Integration and modularity have been proposed to influence the trajectory of evolution, either acting as constraints or facilitators. Here, we examine trends in the integration and modularity of pectoral fin morphology in teleost fishes using geometric morphometrics. We compare the fin shapes of the highly diverse radiation of acanthomorph fishes to lower teleosts. Integration and modularity are measured using two‐block partial least squares analysis and the covariance ratio coefficient between the radial bones and lepidotrichia of the pectoral fins. We show that the fins of acanthomorph fishes are more tightly integrated but also more morphologically diverse and faster evolving compared to nonacanthomorph fishes. The main pattern of shape covariation in nonacanthomorphs is concordant with the main trajectory of evolution between nonacanthomorphs and acanthomorphs. Our findings support a facilitating role for integration during the acanthomorph diversification. Potential functional consequences and developmental mechanisms of fin integration are discussed.     

The estimation and evolution of hominin body mass

Body mass is a critical variable in many hominin evolutionary studies, with implications for reconstructing relative brain size, diet, locomotion, subsistence strategy, and social organization. We review methods that have been proposed for estimating body mass from true and trace fossils, consider their applicability in different contexts, and the appropriateness of different modern reference samples. Recently developed techniques based on a wider range of modern populations hold promise for providing more accurate estimates in earlier hominins, although uncertainties remain, particularly in non-Homo taxa. When these methods are applied to almost 300 Late Miocene through Late Pleistocene specimens, the resulting body mass estimates fall within a 25–60 kg range for early non-Homo taxa, increase in early Homo to about 50–90 kg, then remain constant until the Terminal Pleistocene, when they decline.     

Sizing the Jurassic theropod dinosaur Allosaurus: assessing growth strategy and evolution of ontogenetic scaling of limbs

Allosaurus is one of the most common Mesozoic theropod dinosaurs. We present a histological analysis to assess its growth strategy and ontogenetic limb bone scaling. Based on an ontogenetic series of humeral, ulnar, femoral, and tibial sections of fibrolamellar bone, we estimate the ages of the largest individuals in the sample to be between 13-19 years. Growth curve reconstruction suggests that maximum growth occurred at 15 years, when body mass increased 148 kg/year. Based on larger bones of Allosaurus, we estimate an upper age limit of between 22-28 years of age, which is similar to preliminary data for other large theropods. Both Model I and Model II regression analyses suggest that relative to the length of the femur, the lengths of the humerus, ulna, and tibia increase in length more slowly than isometry predicts. That pattern of limb scaling in Allosaurus is similar to those in other large theropods such as the tyrannosaurids. Phylogenetic optimization suggests that large theropods independently evolved reduced humeral, ulnar, and tibial lengths by a phyletic reduction in longitudinal growth relative to the femur.     

Humeral epiphyseal shape in the felidae: The influence of phylogeny,allometry, and locomotion

Bone morphology of the cats (Mammalia: Felidae) is influenced by many factors, including locomotor mode, body size, hunting methods, prey size and phylogeny. Here, we investigate the shape of the proximal and distal humeral epiphyses in extant species of the felids, based on two‐dimensional landmark configurations. Geometric morphometric techniques were used to describe shape differences in the context of phylogeny, allometry and locomotion. The influence of these factors on epiphyseal shape was assessed using Principal Component Analysis, Linear Discriminant functions and multivariate regression. Phylogenetic Generalised Least Squares was used to examine the association between size or locomotion and humeral epiphyseal shape, after taking a phylogenetic error term into account. Results show marked differences in epiphyseal shape between felid lineages, with a relatively large phylogenetic influence. Additionally, the adaptive influences of size and locomotion are demonstrated, and their influence is independent of phylogeny in most, but not all, cases. Several features of epiphyseal shape are common to the largest terrestrial felids, including a relative reduction in the surface area of the humeral head and increased robusticity of structures that provide attachment for joint‐stabilising muscles, including the medial epicondyle and the greater and lesser tubercles. This increased robusticity is a functional response to the increased loading forces placed on the joints due to large body mass. J. Morphol., 2012. © 2012 Wiley Periodicals, Inc.     

The developmental and physiological basis of body size evolution in an insect

The evolution of body size is a dominant feature of animal evolution. However, little is known about how the underlying developmental mechanisms that determine size change as body size evolves. Here we report on a case of body size evolution in the tobacco hornworm Manduca sexta that occurred over a period of nearly 30 years. We take advantage of an extensive series of physiological studies performed in the early 1970s that established the parameters that regulate body size in this species and compare their values with those of modern individuals that are descendants of the same colony. We show that three of the five processes that determine adult body size changed during this period, while two remained constant. Changes in these three developmental processes completely account for the observed evolutionary change in body size.     

The evolution of large body size in orangutans: A model for hominoid divergence

Recent Miocene fossil discoveries of large hominoids resemble orangutans. Since the evolution of large body size was functionally related to a powerful masticatory system in Miocene ape radiations, a better understanding of adaptations in extant orangutans will be informative of hominoid evolution. It is suggested here, based on the behavioral ecology of extant orangutans, that foraging energetics and large body size are tied to a dietary shift that provided access to and utilization of resources not generally available to other primates.     

Size and shape interspecific divergence patterns partly reflect phylogeny in an Onthophagus species‐complex (Coleoptera: Scarabaeidae)

Polyphenism has been suggested as an accelerator for morphological evolution and speciation. In the dung beetles of the genus Onthophagus, horn expression is polyphenic: large males develop horns whereas smaller males express greatly reduced or no horns. Horn static allometries seem to diverge rapidly amongst extant taxa, a process which might trigger changes in the male genital morphology, thus possibly promoting speciation as a by‐product. It can therefore be hypothesized that interspecific distances in allometries and, possibly, in other morphological traits mirror phylogenetic distances. In this study we first assessed the phylogenetic relationships amongst three closely related taxa belonging to the so‐called ‘Onthophagus fracticornis‐similis‐opacicollis’ species‐complex by sequencing the mitochondrial gene cytochrome oxidase subunit 1 (cox1). Biomolecular results indicated three independent lineages, the closest relationships being found between Onthophagus similis and Onthophagus opacicollis. Then we assessed the extent to which divergence pattern of horn static allometries and size and shape divergence patterns of one genital (paramere) and two nongenital (head and epipharynx) structures mirrored the phylogenetic relationships. Interspecific divergence patterns of horn static allometries, paramere, and head shape were found to be congruent with the evolutionary relationships inferred from biomolecular data. Nevertheless, paramere size and epipharynx shape showed patterns not consistent with the phylogeny. Furthermore, the relative size of nongenital structures showed little interspecific divergence compared to their shapes. Our results suggest that size and shape interspecific divergence mirror phylogeny only in part; they also indicate that distinct morphological traits may differ in their tendency to evolve in concert, and that size and shape of the same trait can evolve independently across species. © 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 162 , 482–498.     

Patterns of musculoskeletal growth and dimensional changes associated with selection and developmental plasticity in domestic and wild strain turkeys

Domestication is a type of experimental evolution in which humans have artificially selected for specific desired traits. Selected strain animals can be utilized to identify correlated responses by comparing them to the wild strain. In particular, domestic turkeys have been selected for increased body mass and high‐growth rate, most significantly over the past 60 years. Yet it remains unclear how artificial selection has affected the morphology and evolution of the musculoskeletal system as a whole. Here, we compare growth rate over 21 weeks, hind limb bone scaling across ontogeny via in vivo CT scanning, and muscle proportions in wild and domestic turkeys to identify differences in structural scaling and the potential contributions of selection and developmental plasticity to whole‐organism morphology. The domestic turkeys grew at a higher rate (0.14 kg/day vs. 0.05 kg/day) and reached over 3 times the body mass of wild birds. Comparing the proportional muscle masses in adult turkeys, only the trunk had a greater mass ratio in the domestic turkey, driven solely by M. pectoralis (2.8 times larger). The proportional increase in only breast meat and no other muscles highlights the surgical precision attainable with artificial selection. The domestic turkey femur and tibiotarsus displayed increases in polar moment of area, apparently maintaining torsional strength as body mass increased. The lack of dimensional change in the more vertically held tarsometatarsus is consistent with the pattern expected due to developmental plasticity. These results from the domestic turkey emphasize that there are morphological limits to preserving the balance between growth and function, and varying rates of trait evolution can further complicate this equilibrium.     

Allometric growth and adaptive value of exaggerated body parts in the larvae of Gratiana spadicea (Klug) (Coleoptera: Chrysomelidae)

1. Larvae of tortoise beetles present exaggerated body parts in association with an abdominal shield, which is made of faeces and exuviae that are deposited on the urogomphi throughout ontogeny. Growth trajectories and scaling relationships of these functional structures associated with the shield, if any, are unknown. 2. This study of Gratiana spadicea first tested, under field conditions, whether there is adaptive value associated with the shield regarding protection against predation and sunlight. Then, under laboratory conditions, the growth trajectory and allometric relationships among body parts were investigated, including scoli, individual and apparent furcae, and shield. The influence of food deprivation on the development of these structures was also determined. 3. Findings from previous studies were confirmed, suggesting that the adaptive value assigned to the shield is related to protection against predators. The present study demonstrated for the first time that the shield acts as a parasol in cassidines, decreasing the exposure of their larval body to sunlight. The scoli and apparent furca are exaggerated structures of G. spadicea, the development of which involves allometric growth and greater energetic investment (positive allometry) during ontogeny. There was proportionally less energetic investment for somatic construction of individual furca (negative allometry) due to the accumulation of the exuviae. 4. The possible consequences, in terms of developmental costs and survivorship benefits associated with the evolution of such exaggerated structures, are discussed.     

Head shape evolution in monitor lizards (Varanus): interactions between extreme size disparity,phylogeny and ecology

Characterizing patterns of observed current variation, and testing hypotheses concerning the potential drivers of this variation, is fundamental to understanding how morphology evolves. Phylogenetic history, size and ecology are all central components driving the evolution of morphological variation, but only recently have methods become available to tease these aspects apart for particular body structures. Extant monitor lizards (Varanus) have radiated into an incredible range of habitats and display the largest body size range of any terrestrial vertebrate genus. Although their body morphology remains remarkably conservative, they have obvious head shape variation. We use two‐dimensional geometric morphometric techniques to characterize the patterns of dorsal head shape variation in 36 species (375 specimens) of varanid, and test how this variation relates to size, phylogenetic history and ecology as represented by habitat. Interspecific head shape disparity is strongly allometric. Once size effects are removed, principal component analysis shows that most shape variation relates to changes in the snout and head width. Size‐corrected head shape variation has strong phylogenetic signal at a broad level, but habitat use is predictive of shape disparity within phylogenetic lineages. Size often explains shape disparity among organisms; however, the ability to separate size and shape variation using geometric morphometrics has enabled the identification of phylogenetic history and habitat as additional key factors contributing to the evolution of head shape disparity among varanid lizards.