Sexual dimorphism in cranial shape and size in geomyoid rodents: multivariate and evolutionary perspectives

Geomyoid rodents provide a great study system for the analysis of sexual dimorphism. They are polygynic and many inhabit harsh arid environments thought to promote sexual dimorphism. In fact, there has been extensive work published on the sexual size dimorphism of individual populations and species within this rodent clade. However, little work has been undertaken to assess the evolutionary patterns and processes associated with this sexual dimorphism. We use multivariate analyses of cranial measurements in a phylogenetic framework to determine the distribution of size and shape dimorphism among geomyoids and test for Rensch’s rule. Our results suggest that sexual dimorphism is more common in geomyids than heteromyids, but it is not in fact universal. There is evidence for variation in sexual dimorphism across populations. Additionally, in many taxa, geographic variation appears to overwhelm existing sexual dimorphism. We find support for the repeated independent evolution of shape and size dimorphism across geomyoid taxa, but we do not find support for an association between size and shape dimorphism. There is no evidence for Rensch’s rule in geomyoids, whether at the superfamily or family level. Together, our findings suggest that there is no single explanation for the evolution of sexual dimorphism in geomyoids and that, instead, it is the product of numerous evolutionary events. Future studies incorporating phylogenetic relationships will be necessary to paint a more complete picture of the evolution of sexual dimorphism in geomyoids.     

Cranial shape variation and molecular phylogenetic structure of crested newts (Triturus cristatus superspecies: Caudata,Salamandridae) in the Balkans

In the present study, we investigated the degree of congruence between phylogeny, as inferred from mitochondrial (mt)DNA sequences, and cranium shape variation of crested newts (Triturus cristatus superspecies) in the Balkans. These newts belong to four phylogenetic clades defined by mtDNA analysis, and significantly differed in cranial shape. Allometry explained a high percentage of shape variation in crested newts. The clade‐specific allometric slopes significantly diverged for both the ventral cranium and dorsal cranium, indicating that differences in shape between clades could not be a simple consequence of their difference in size. The analysis of hierarchical and spatial variation showed similarity in the patterns of global and spatially localized hierarchical variation of cranial shape. We also found significant congruence between the pattern of cranial shape variation and molecular phylogeny. The differences in morphology of Triturus dobrogicus in comparison to other crested newt clades, including marked differences in cranium shape, is discussed in the context of the evolution and ecology of crested newts. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 348–360.     

A phylogenetic view on skull size and shape variation in the smooth newt (Lissotriton vulgaris,Caudata, Salamandridae)

In this study, we explore skull size and shape variation in the smooth newt, a taxon with substantial morphological differentiation and complex phylogeographic relations. By projecting phylogenies into the morphospace of the skull shape, we explore the variation in and differentiation of this complex morphological structure within a phylogenetic framework. For these analyses, we used a dataset that covers the most southern part of the species’ distribution range, including all conventionally recognized subspecies. The study revealed different patterns of divergence in skull shape between sexes, which is paralleled by intraspecific differentiation. The divergence in dorsal skull shape is concordant with the phylogenetic divergence, as the most diverged clades of the smooth newt (Lissotriton vulgaris kosswigi and Lissotriton vulgaris lantzi) exhibit a skull shape that significantly diverges from the smooth newt’s mean shape configuration. The results of this study also indicate that ventral skull portion, which is more directly related to feeding and foraging, shows higher variation between populations than dorsal skull portion, which appears to be less variable and phylogenetically informative.     

The evolution of the adult body form of the crested newt (Triturus cristatus superspecies,Caudata, Salamandridae)

We characterized the adult body form of the crested newt (Triturus cristatus superspecies) and explored its evolution. From seven morphometric traits, we determined that body size, interlimb distance and head width define the body form. None of the morphometric traits showed a phylogenetic signal. Three body‐shape morphotypes (Triturus dobrogicus + T. cristatus, Triturus carnifex + Triturus macedonicus and Triturus karelinii + Triturus arntzeni) and three body‐size morphotypes (T. dobrogicus, T. cristatus and all other crested newts) could be recognized. The ancestral phenotype (a large body with a short trunk and a wide head) characterized T. karelinii and T. arntzeni. Triturus carnifex and T. macedonicus had a somewhat different phenotype (large body and wide head, accompanied by mild body elongation). The most derived phenotype included body size reduction and more pronounced body elongation in T. cristatus and, especially, in T. dobrogicus. Body elongation occurred by trunk lengthening but not head and tail lengthening. Additionally, contrary to other tetrapods, evolutionary axis elongation in crested newts was followed by a decrease in body size. We advocate the hypothesis that ecology drives the evolution of body form in crested newts.     

Morphing of the phylogeographic lineages of the Balkan alpine newts (Ichthyosaura alpestris, Caudata, Salamandridae): in situ morphological diversification

Numerous alpine newt (Ichthyosaura alpestris) populations from the Balkans, representing all the previously established phylogeographic lineages, were studied for variations in various morphological characteristics (body size and shape, skull qualitative traits and number of trunk vertebrae). Here, we present a decoupling of morphological and mtDNA phylogeographic substructuring in the alpine newt on the Balkan Peninsula. In sharp contrast to other European newts (Triturus spp., Lissotriton spp.), the vast majority of morphological variation in the alpine newt is concentrated at the population level indicating an in situ morphological diversification. We found that the rate of morphological change is similar to the rate of mtDNA change. We hypothesize that the alpine newts are characterized by non-adaptive morphological evolution.     

The evolution of sexual size dimorphism in cottontail rabbits (Sylvilagus,Leporidae)

In mammals, ‘female‐biased’ sexual size dimorphism (SSD), in which females are larger than males, is uncommon. In the present study, we examined Sylvilagus, a purported case of female‐biased SSD, for evolutionary correlations among species between SSD, body‐size, and life‐history variables. We find that: (1) although most species are female‐biased, the degree and direction of SSD vary more than was previously recognized and (2) the degree of SSD decreases with increasing body size. Hence, Sylvilagus provides a new example, unusual for a female‐biased taxon, in which allometry for SSD is consistent with ‘Rensch's Rule’. As a corollary to Rensch's Rule, we observe that changes in SSD in Sylvilagus are typically associated with larger, more significant changes in males than females. Female‐biased SSD could be produced by selection for larger females, smaller males, or both. Although larger female size may be related to high fecundity and the extremely rapid fetal and neonatal growth in Sylvilagus, we find little evidence for a correlation between SSD and various fecundity‐related traits in among‐species comparisons. Smaller male size may confer greater reproductive success through greater mobility and reduced energetic requirements. We propose that a suite of traits (female dispersion, large male home ranges, reduced aggression, and a promiscuous mating system) has favoured smaller males and thus influenced the evolution of SSD in cottontails. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 141–156.     

Skull size and shape variation versus molecular phylogeny: a case study of alpine newts (<Emphasis Type="Italic">Mesotriton alpestris</Emphasis>, Salamandridae) from the Balkan Peninsula

We explored the phylogenetic signal of skull size and shape in alpine newts from the Balkans, a group of European newts that, in spite of their considerable phylogeographic substructuring (as inferred from previous DNA analyses), maintain a conserved phenotype. In terms of skull shape disparity, geometric morphometrics show that the dorsal cranium carries a significant phylogenetic signal, the most notable evidence in this present study. On the contrary, no phylogenetic signal in the shape of the ventral cranium was found. This result indicates that the variation in the shape of the ventral cranium is more prone to other factors and processes, such as adaptations to local environments rather than phylogenetic constraints. Variation in skull size within alpine newts seems to be independent from phylogenetic constraints.     

Climate history,human impacts and global body size of Carnivora (Mammalia: Eutheria) at multiple evolutionary scales

Aim One of the longest recognized patterns in macroecology, Bergmann’s rule, describes the tendency for homeothermic animals to have larger body sizes in cooler climates than their phylogenetic relatives in warmer climates. Here we provide an integrative process‐based explanation for Bergmann’s rule at the global scale for the mammal order Carnivora. Location Global. Methods Our database comprises the body sizes of 209 species of extant terrestrial Carnivora, which were analysed using phylogenetic autocorrelation and phylogenetic eigenvector regression. The interspecific variation in body size was partitioned into phylogenetic (P) and specific (S) components, and mean P‐ and S‐components across species were correlated with environmental variables and human occupation both globally and for regions glaciated or not during the last Ice Age. Results Three‐quarters of the variation in body size can be explained by phylogenetic relationships among species, and the geographical pattern of mean values of the P‐component is the opposite of the pattern predicted by Bergmann’s rule. Partial regression revealed that at least 43% of global variation in the mean phylogenetic component is explained by current environmental factors. In contrast, the mean S‐component of body size shows large positive deviations from ancestors across the Holarctic, and negative deviations in southern South America, the Sahara Desert, and tropical Asia. There is a moderately strong relationship between the human footprint and body size in glaciated regions, explaining 19% of the variance of the mean P‐component. The relationship with the human footprint and the P‐component is much weaker in the rest of the world, and there is no relationship between human footprint and S‐component in any region. Main conclusions Bergmannian clines are stronger at higher latitudes in the Northern Hemisphere because of the continuous alternation of glacial–interglacial cycles throughout the late Pliocene and Pleistocene, which generated increased species turnover, differential colonization and more intense adaptive processes soon after glaciated areas became exposed. Our analyses provide a unified explanation for an adaptive Bergmann’s rule within species and for an interspecific trend towards larger body sizes in assemblages resulting from historical changes in climate and contemporary human impacts.     

Evolution of sexual size dimorphism in grouse and allies (Aves: Phasianidae) in relation to mating competition,fecundity demands and resource division

Sexual size dimorphism (SSD) is often assumed to be driven by three major selective processes: (1) sexual selection influencing male size and thus mating success, (2) fecundity selection acting on females and (3) inter‐sexual resource division favouring different size in males and females to reduce competition for resources. Sexual selection should be particularly strong in species that exhibit lek polygyny, since male mating success is highly skewed in such species. We investigated whether these three selective processes are related to SSD evolution in grouse and allies (Phasianidae). Male‐biased SSD increased with body size (Rensch’s rule) and lekking species exhibited more male‐biased SSD than nonlekking ones. Directional phylogenetic analyses indicated that lekking evolved before SSD, but conclusions were highly dependent on the body size traits and chosen model values. There was no relationship between SSD and male display agility, nor did resource division influence SSD. Although clutch mass increased with female body size it was not related to the degree of SSD. Taken together, the results are most consistent with the hypothesis that lekking behaviour led to the evolution of male‐biased SSD in Phasianidae.     

Cytology, embryology, and evolution of the developmental arrest syndrome in newts of the genus Triturus (Caudata: Salamandridae)

We have examined embryonic development in three species (T. carnifex, T. cristatus, and T. marmoratus) of European newts of the genus Triturus (subgenus Neotriton) in which developmental arrest occurs in embryos that are homomorphic for a chromosomal heteromorphism involving chromosome 1 (Horner and Macgregor: J. Herpetol., 19:261-270, 1985). Embryonic arrest occurred during tailbud stages in all three species, but at a slightly earlier stage in T. marmoratus. Two phenotypes were identified among the arrested embryos. One of these is indistinguishable in embryonic morphology from normal embryos at all stages up to the time of arrest, but the other is characterized by a protruding yolk plug, which persists from the late gastrula/early neurula stage to the tailbud arrest stage and apparently interferes with normal morphogenesis. Evidence is presented that the two arrested phenotypes, which occur in approximately equal numbers, represent embryos that carry the two alternative homomorphic chromosome pairs of chromosome 1 heteromorphism. We conclude that developmental arrest reflects a balanced lethal heterozygosity probably resulting from an unequal exchange of genic material between the homologues of chromosome 1 which occurred in a common ancestor of the Neotriton species.     

Evidence for speciational change in the evolution of ratites (Aves: Palaeognathae)

To perform a comparative analysis of character associations framed in a phylogenetic context (e.g. independent contrasts), a model of character evolution must be assumed. According to phyletic gradualism, morphological change accumulates gradually over time within lineages, and speciation events do not have a major role. Under speciational models, morphological change is assumed to occur during or just after cladogenesis in both daughter species, and the resulting morphologies do not change over long periods of time (stasis), until the next cladogenetic event. A novel method is presented for comparing these models of character evolution that uses permutational multiple phylogenetic regressions. The addition of divergence times to well-corroborated phylogenetic trees and the utilization of the method developed in this paper allows the estimation of relative frequency of gradual change and speciational change from living organisms. This method is applied to a dataset from ratites with the conclusion that, for a range of morphological features, change tends to have been speciational rather than gradual.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 80 , 99–106.     

Role of sexual and natural selection in evolution of body size and shape: a phylogenetic study of morphological radiation in grouse

We use standardized independent contrasts (SICs) to elucidate the effect of ecology and mating systems on morphological radiation in grouse. The analysis of SICs for 38 skeletal measurements from 20 taxa, showed that changes in mating system had a significant effect on body size of both sexes. Sexual size dimorphism in grouse is consistent with Rensch's rule; the slope of the regression of male vs. female size SICs was 1.4, significantly >1. Changes in habitat were associated with accelerated rates of evolution of body proportions. SICs for male and female scores of size independent factors were directly proportional to each other (slope = 1), indicating extreme similarities between male and female ecology. Females, however, were better adapted to longer, more energy efficient flight than males. Size independent morphological differences among grouse are adaptive and are related to the differences in habitat and foraging behaviour among the species.     

Patterns of sexual size dimorphism in stingless bees: Testing Rensch’s rule and potential causes in highly eusocial bees (Hymenoptera: Apidae,Meliponini)

Eusocial insects offer a unique opportunity to analyze the evolution of body size differences between sexes in relation to social environment. The workers, being sterile females, are not subject to selection for reproductive function providing a natural control for parsing the effects of selection on reproductive function (i.e., sexual and fecundity selection) from other kinds of natural selection. Patterns of sexual size dimorphism (SSD) and testing of Rensch's rule controlling for phylogenetic effects were analyzed in the Meliponini or stingless bees. Theory predicts that queens may exhibit higher selection for fecundity in eusocial taxa, but contrary to this, we found mixed patterns of SSD in Meliponini. Non‐Melipona species generally have a female‐biased SSD, while all analyzed species of Melipona showed a male‐biased SSD, indicating that the direction and magnitude of the selective pressures do not operate in the same way for all members of this taxon. The phylogenetic regressions revealed that the rate of divergence has not differed between the two castes of females and the males, that is, stingless bees do not seem to follow Rensch's rule (a slope >1), adding this highly eusocial taxon to the various solitary insect taxa not conforming with it. Noteworthy, when Melipona was removed from the analysis, the phylogenetic regressions for the thorax width of males on queens had a slope significantly smaller than 1, suggesting that the evolutionary divergence has been larger in queens than males, and could be explained by stronger selection on female fecundity only in non‐Melipona species. Our results in the stingless bees question the classical explanation of female‐biased SSD via fecundity and provide a first evidence of a more complex determination of SSD in highly eusocial species. We suggest that in highly eusocial taxa, additional selection mechanisms, possibly related to individual and colonial interests, could influence the evolution of environmentally determined traits such as body size.     

The distribution and taxonomy of Lissotriton newts in Turkey (Amphibia,Salamandridae)

Two and perhaps three taxa of Lissotriton newt occur in Turkey. Their species status is controversial. The distribution of these taxa and the taxonomic status of each are reviewed and discussed. A database of 128 Turkish Lissotriton localities was compiled and species distribution models were constructed. We reiterate that the presence of Lissotriton (vulgaris) lantzi in Turkey is disputed and needs confirmation. The range of Lissotriton (vulgaris) kosswigi is restricted to north-western Anatolia – given the small global range of this Turkey endemic, a closer look at its conservation status is warranted. The distribution of Lissotriton vulgaris schmidtleri covers western Asiatic and European Turkey. The findings support an allopatric distribution of the Turkish Lissotriton species. We reflect on the biological significance of previously reported morphological intermediates between Lissotriton (vulgaris) kosswigi and Lissotriton vulgaris schmidtleri in the light of the recent proposal to recognize kosswigi at the species level. The available data are in line with species status for Lissotriton (vulgaris) lantzi and Lissotriton (vulgaris) kosswigi. Although Lissotriton vulgaris schmidtleri is a genetically diverged taxon as well, the extent of gene flow with parapatric European Lissotriton taxa is as yet unknown.     

Divergence in size,but not in shape: variation in skull size and shape within Ommatotriton newts

Using a geometric morphometric approach, we explored the variation in skull size and skull shape in banded newts (genus Ommatotriton). The genus Ommatotriton is represented by two allopatric, genetically well‐defined species: Ommatotriton ophryticus and O. vittatus. Within each species, two subspecies have been recognised. The samples used in this study cover the geographical and genetic variation within each species. We found statistically significant variation in skull size between species and among populations within species. When corrected for size, there was no significant variation in shape between species. Our results indicate that the variation in skull shape within the genus Ommatotriton is almost entirely due to size‐dependent, allometric shape changes. The exception is the shape of the ventral skull in males. Males of O. ophryticus and O. vittatus significantly diverge in the shape of the ventral cranium. The ventral skull, more precisely the upper jaw and palate, is directly functionally related to feeding. In general, our results indicate that allometry is a significant factor in the morphological variation of banded newts. However, the divergence in the ventral skull shape of males indicates that sexual selection and niche partitioning may have influenced the evolution of skull shape in these newts.     

Phylogeny and biogeography of the family Salamandridae (Amphibia: Caudata) inferred from complete mitochondrial genomes

Phylogenetic relationships of members of the salamander family Salamandridae were examined using complete mitochondrial genomes collected from 42 species representing all 20 salamandrid genera and five outgroup taxa. Weighted maximum parsimony, partitioned maximum likelihood, and partitioned Bayesian approaches all produce an identical, well-resolved phylogeny; most branches are strongly supported with greater than 90% bootstrap values and 1.0 Bayesian posterior probabilities. Our results support recent taxonomic changes in finding the traditional genera Mertensiella, Euproctus, and Triturus to be non-monophyletic species assemblages. We successfully resolved the current polytomy at the base of the salamandrid tree: the Italian newt genus Salamandrina is sister to all remaining salamandrids. Beyond Salamandrina, a clade comprising all remaining newts is separated from a clade containing the true salamanders. Among these newts, the branching orders of well-supported clades are: primitive newts (Echinotriton, Pleurodeles, and Tylototriton), New World newts (Notophthalmus-Taricha), Corsica-Sardinia newts (Euproctus), and modern European newts (Calotriton, Lissotriton, Mesotriton, Neurergus, Ommatotriton, and Triturus) plus modern Asian newts (Cynops, Pachytriton, and Paramesotriton).Two alternative sets of calibration points and two Bayesian dating methods (BEAST and MultiDivTime) were used to estimate timescales for salamandrid evolution. The estimation difference by dating methods is slight and we propose two sets of timescales based on different calibration choices. The two timescales suggest that the initial diversification of extant salamandrids took place in Europe about 97 or 69Ma. North American salamandrids were derived from their European ancestors by dispersal through North Atlantic Land Bridges in the Late Cretaceous ( approximately 69Ma) or Middle Eocene ( approximately 43Ma). Ancestors of Asian salamandrids most probably dispersed to the eastern Asia from Europe, after withdrawal of the Turgai Sea ( approximately 29Ma).     

Scaling of Sexual Dimorphism in Body Mass: A Phylogenetic Analysis of Rensch's Rule in Primates

We examined the relationship between body mass dimorphism, measured as the natural logarithm of the male/female ratio, and body mass, defined as ln (female mass), with interspecific allometry, phylogenetically independent contrasts, and phylogenetic autocorrelation in 105 primate species. We repeated the analyses for Strepsirhini (N = 23), Haplorhini (N = 82), Platyrrhinii (N = 32), and Catarrhini (N = 47). With independent contrasts, there is statistically significant (p < .05) positive allometry in Primates in general, Haplorhini, and Catarrhini, but not in Strepsirhini or Platyrrhini. The steepest slope (0.134) is for Catarrhini. Results differed when we conducted analyses with traditional interspecific allometry. For example, not only was the Catarrhini slope not statistically significant but also the magnitude of the slope was shallower than that of all other groups, except Strepsirhini. The results indicate that phylogenetic effects influence the scaling of sexual size dimorphism, and that the statistical method used has a large impact on the interpretation of this biological relationship. We discuss issues involved in applying these statistical methods in detail.     

Phylogeny suggests nondirectional and isometric evolution of sexual size dimorphism in argiopine spiders

Sexual dimorphism describes substantial differences between male and female phenotypes. In spiders, sexual dimorphism research almost exclusively focuses on size, and recent studies have recovered steady evolutionary size increases in females, and independent evolutionary size changes in males. Their discordance is due to negative allometric size patterns caused by different selection pressures on male and female sizes (converse Rensch's rule). Here, we investigated macroevolutionary patterns of sexual size dimorphism (SSD) in Argiopinae, a global lineage of orb‐weaving spiders with varying degrees of SSD. We devised a Bayesian and maximum‐likelihood molecular species‐level phylogeny, and then used it to reconstruct sex‐specific size evolution, to examine general hypotheses and different models of size evolution, to test for sexual size coevolution, and to examine allometric patterns of SSD. Our results, revealing ancestral moderate sizes and SSD, failed to reject the Brownian motion model, which suggests a nondirectional size evolution. Contrary to predictions, male and female sizes were phylogenetically correlated, and SSD evolution was isometric. We interpret these results to question the classical explanations of female‐biased SSD via fecundity, gravity, and differential mortality. In argiopines, SSD evolution may be driven by these or additional selection mechanisms, but perhaps at different phylogenetic scales.     

Spider dragline silk: correlated and mosaic evolution in high-performance biological materials

The evolution of biological materials is a critical, yet poorly understood, component in the generation of biodiversity. For example, the diversification of spiders is correlated with evolutionary changes in the way they use silk, and the material properties of these fibers, such as strength, toughness, extensibility, and stiffness, have profound effects on ecological function. Here, we examine the evolution of the material properties of dragline silk across a phylogenetically diverse sample of species in the Araneomorphae (true spiders). The silks we studied are generally stronger than other biological materials and tougher than most biological or man-made fibers, but their material properties are highly variable; for example, strength and toughness vary more than fourfold among the 21 species we investigated. Furthermore, associations between different properties are complex. Some traits, such as strength and extensibility, seem to evolve independently and show no evidence of correlation or trade-off across species, even though trade-offs between these properties are observed within species. Material properties retain different levels of phylogenetic signal, suggesting that traits such as extensibility and toughness may be subject to different types or intensities of selection in several spider lineages. The picture that emerges is complex, with a mosaic pattern of trait evolution producing a diverse set of materials across spider species. These results show that the properties of biological materials are the target of selection, and that these changes can produce evolutionarily and ecologically important diversity.