Bat genitalia: allometry, variation and good genes

Male genitalia are typically highly variable across species, for which sexual selection is thought to be responsible. Sexually selected traits characteristically show positive allometry and high phenotypic variation, although genitalia seem to be typified by negative allometry due to stabilizing selection. Additionally, while sexual selection appears to be the primary force responsible for genital evolution, the precise mechanism is unclear, but good-genes selection could be involved. If so, male genital variation should correlate with some male quality measure(s). We investigated the allometry of male Nyctalus noctula genitalia and investigated associations between genital size and three phenotypic measures of male quality (body size, relative body mass, and fluctuating asymmetry (FA)). We found that the penis exhibited positive allometry and high phenotypic variation, and was positively associated with male body size and relative body mass, but not with FA. This pattern is more typical of sexually selected display traits, contrasting with general patterns of genital allometry. The baculum was negatively allometric and was not associated with any quality measure. Our results suggest that the N. noctula penis is under directional sexual selection and is a reliable indicator of male phenotypic quality.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 83 , 497–507.     

Sex combs,allometry, and asymmetry in Drosophila

There has been recent debate about the expected allometry of sexually‐selected traits. Although sexually‐selected traits exhibit a diversity of allometric patterns, signalling characters are frequently positively allometric. By contrast, insect genitalia tend to be negatively allometric, although the allometry of nongenital sexually‐selected characters in insects is largely unknown (with some notable exceptions). It has also been suggested that there should be a negative association between the asymmetry and size of bilaterally‐paired, sexually‐selected traits, although this claim is controversial. We assessed the allometry and asymmetry (fluctuating asymmetry, FA) of a nongenital contact–courtship structure, the sex comb, in replicate populations of three species of Drosophila (we also measured wing FA). Sex combs are sexually‐selected characters used to grasp the female's abdomen and genitalia and to spread her wings prior to and during copulation. Although species differed in the size of the sex combs, all combs were positively allometric, and comb allometry did not generally differ significantly between species or populations. Comb and wing asymmetry did vary across species, although not across populations of the same species. However, FA was trait specific and was never negatively associated with trait size. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 923–934.     

Postnatal Dynamics of Developmental Stability and Canalization of Lizard Head Shape Under Different Environmental Conditions

Developmental stability (DS) and canalization are key determinants of phenotypic variation. To provide a better understanding of how postnatal growth is involved in determining the effects of DS and canalization on phenotypic variation, we studied within- and among-individual variation in head shape in ontogenetic series of lizards inhabiting urban and rural environments. Urban lizards exhibited increased fluctuating asymmetry during the early postnatal stages, but asymmetry levels decreased during growth. By contrast, asymmetry remained constant across the investigated size range in the rural population. In addition, urban juveniles were more variable for symmetric shape and deviated more from the group shape-size allometric trajectory, but both indices declined across ontogeny. Congruent patterns of within- and among-individual variation suggest that both DS and canalization may rely on similar underlying mechanisms. Further, the ontogenetic reduction of variation in the urban population suggests that compensatory growth may aid in buffering phenotypic variation and correcting deviances from the established developmental path. Alternatively, passive mechanisms and population dynamics may also explain the decrease of phenodeviants in urban populations. Significant correlations between symmetric and asymmetric shape, as well as similar integration patterns between the two populations, suggest that similar developmental mechanisms regulate head shape in both environments. Overall, these results highlight the relevance of both pre- and post-natal dynamics in determining levels of phenotypic variation, enhancing our understanding of how organisms respond to perturbations to DS and canalization under stressful conditions.     

Genotype × environment interaction in the allometry of body,genitalia and signal traits in Enchenopa treehoppers (Hemiptera: Membracidae)

Developmental plasticity may promote divergence by exposing genetic variation to selection in novel ways in new environments. We tested for this effect in the static allometry (i.e. scaling on body size) of traits in advertisement signals, body and genitalia. We used a member of the Enchenopa binotata species complex of treehoppers – a clade of plant‐feeding insects in which speciation is associated with colonization of novel environments involving marked divergence in signals, subtle divergence in body size and shape, and no apparent divergence in genitalia. We found no change in mean allometric slopes across environments, but substantial genetic variation and genotype × environment interaction (G × E) in allometry. The allometry of signal traits showed the most genetic variation and G × E, and that of genitalia showed the weakest G × E. Our findings suggest that colonizing novel environments may have stronger diversifying consequences for signal allometry than for genitalia allometry. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 187–196.     

Ecological preference between generalist and specialist rodents: spatial and environmental correlates of phenotypic variation

Different ecological preferences among species may result in differences in response to similar environmental variation. To test this hypothesis, we assessed the patterns of skull and mandible size and shape variation in three Sigmodontinae mice from agroecosystems of central Argentina with increasing degree of specialization: Calomys musculinus, Akodon azarae and Oxymycterus rufus. Spatial patterns in size and shape were analysed after controlling for allometry and sexual dimorphism using a total of 697 specimens. We then evaluated the covariation between shape, climatic and environmental variables and assessed the contribution of distinct climatic and environmental variables to phenotypic variability. Oxymycterus rufus displayed a marked spatial structure, and there was a high correlation between shape, climatic and environmental variables in this species. Climatic and environmental variables had a moderate effect on the phenotype of A. azarae, and were not correlated with morphological variation in C. musculinus. Our study highlights the difference in phenotypic responses to spatial and environmental gradients across coexisting species, specialist species displaying a more marked spatial structure in morphology than generalist species. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112 , 180–203.     

Relationships among ontogenetic,static, and evolutionary allometry

The relationship between ontogenetic, static, and evolutionary levels of allometry is investigated. Extrapolation from relative size relationships in adults to relative growth in ontogeny depends on the variability of slopes and intercepts of ontogenetic vectors relative to variability in length of the vector. If variability in slopes and intercepts is low relative to variability in length, ontogenetic and static allometries will be similar. The similarity of ontogenetic and static allometries was tested by comparing the first principal component, or size vector, for correlations among 48 cranial traits in a cross-sectional ontogenetic sample of rhesus macaques from Cayo Santiago with a static sample from which all age- and sex-related variation had been removed. The vector correlation between the components is high but significantly less than one while two of three allometric patterns apparent in the ontogenetic component are not discernable in the static component. This indicates that there are important differences in size and shape relationships among adults and within ontogenies. Extrapolation from intra- or interspecific phenotypic allometry to evolutionary allometry is shown to depend on the similarity of genetic and phenotypic allometry patterns. Similarity of patterns was tested by comparing the first principal components of the phenotypic, genetic, and environmental correlation matrices calculated using standard quantitative genetic methods. The patterns of phenotypic, genetic, and environmental allometry are dissimilar; only the environmental allometries show ontogenetic allometric patterns. This indicates that phenotypic allometry may not be an accurate guide to patterns of evolutionary change in size and shape.     

The static allometry of sexual and nonsexual traits in vervet monkeys

Sexual traits vary tremendously in static allometry. This variation may be explained in part by body size‐related differences in the strength of selection. We tested this hypothesis in two populations of vervet monkeys, using estimates of the level of condition dependence for different morphological traits as a proxy for body size‐related variation in the strength of selection. In support of the hypothesis, we found that the steepness of allometric slopes increased with the level of condition dependence. One trait of particular interest, the penis, had shallow allometric slopes and low levels of condition dependence, in agreement with one of the most consistent patterns yet detected in the study of allometry, namely that of genitalia exhibiting shallow allometries. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 527–537.     

Quantitative genetic variation in static allometry in the threespine stickleback

The common pattern of replicated evolution of a consistent shape-environment relationship might reflect selection acting in similar ways within each environment, but divergently among environments. However, phenotypic evolution depends on the availability of additive genetic variation as well as on the direction of selection, implicating a bias in the distribution of genetic variance as a potential contributor to replicated evolution. Allometry, the relationship between shape and size, is a potential source of genetic bias that is poorly understood. The threespine stickleback, Gasterosteus aculeatus, provides an ideal system for exploring the contribution of genetic variance in body shape allometry to evolutionary patterns. The stickleback system comprises marine populations that exhibit limited phenotypic variation, and young freshwater populations which, following independent colonization events, have often evolved similar phenotypes in similar environments. In particular, stickleback diversification has involved changes in both total body size and relative size of body regions (i.e., shape). In a laboratory-reared cohort derived from an oceanic Alaskan population that is phenotypically and genetically representative of the ancestor of the diverse freshwater populations in this region, we determined the phenotypic static allometry, and estimated the additive genetic variation about these population-level allometric functions. We detected significant allometry, with larger fish having relatively smaller heads, a longer base to their second dorsal fin, and longer, shallower caudal peduncles. There was additive genetic variance in body size and in size-independent body shape (i.e., allometric elevation), but typically not in allometric slopes. These results suggest that the parallel evolution of body shape in threespine stickleback is not likely to have been a correlated response to selection on body size, or vice versa. Although allometry is common in fishes, this study highlights the need for additional data on genetic variation in allometric functions to determine how allometry evolves and how it influences phenotypic evolution.     

Allometry of the baculum and sexual size dimorphism in American martens and fishers (Mammalia: Mustelidae)

Genitalia are among the most variable of morphological traits, and recent research suggests that this variability may be the result of sexual selection. For example, large bacula may undergo post‐copulatory selection by females as a signal of male size and age. This should lead to positive allometry in baculum size. In addition to hyperallometry, sexually selected traits that undergo strong directional selection should exhibit high phenotypic variation. Nonetheless, in species in which pre‐copulatory selection predominates over post‐copulatory selection (such as those with male‐biased sexual size dimorphism), baculum allometry may be isometric or exhibit negative allometry. We tested this hypothesis using data collected from two highly dimorphic species of the Mustelidae, the American marten (Martes americana) and the fisher (Martes pennanti). Allometric relationships were weak, with only 4.5–10.1% of the variation in baculum length explained by body length. Because of this weak relationship, there was a large discrepancy in slope estimates derived from ordinary least squares and reduced major axis regression models. We conclude that stabilizing selection rather than sexual selection is the evolutionary force shaping variation in baculum length because allometric slopes were less than one (using the ordinary least squares regression model), a very low proportion of variance in baculum length was explained by body length, and there was low phenotypic variability in baculum length relative to other traits. We hypothesize that this pattern occurs because post‐copulatory selection plays a smaller role than pre‐copulatory selection (manifested as male‐biased sexual size dimorphism). We suggest a broader analysis of baculum allometry and sexual size dimorphism in the Mustelidae, and other taxonomic groups, coupled with a comparative analysis and with phylogenetic contrasts to test our hypothesis. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 955–963.     

Phenotypic and genetic variation in male genitalia in the seedbug, Lygaeus equestris (Heteroptera)

Male genitalia evolve through sexual selection and, in insects, tend to show negative static allometry, low phenotypic variation, and are usually relatively small. Much less is known about the genetic variation and heritability of male genitalia. Additionally, in instances where the intromittent organ is greatly elongated, it is unclear whether typical patterns of genital scaling and variation also apply. In the present study, we investigated the allometry, variation, and heritability of male genital length in the seedbug, Lygaeus equestris , a species with a greatly elongated intromittent organ (i.e. almost as long as male body size). We found that genital length was negatively allometric, in spite of its great length, and was no more variable than nongenital traits. Additionally, genital length was significantly heritable and had considerable evolvability.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 400–405.     

Asymmetric size and shape variation in the Central European transect across the house mouse hybrid zone

We studied asymmetric variation of the mandible in the Central European portion of the hybrid zone between two house mouse subspecies, Mus musculus musculus and Mus musculus domesticus. Within introgression classes, defined by the share of diagnostic allozymes, we quantified the directional and fluctuating component of asymmetric variation, as well as skewness and kurtosis of individual asymmetry distributions. Furthermore, in the same manner we re‐analysed asymmetric variation of the ventral side of the skull. According to the quadratic polynomial model, the mandible shape‐fluctuating asymmetry, but not size‐fluctuating asymmetry, was significantly decreased in the centre of the hybrid zone (with a minimum predicted for a hybrid index of 0.41). On the contrary, the skull shape‐fluctuating asymmetry non‐monotonically increased towards the musculus side of the hybrid zone (with a peak predicted for a hybrid index of 0.86). Thus, the impact of hybridization on fluctuating asymmetry is trait‐specific in this portion of the house mouse hybrid zone. The only general feature of asymmetric variation we observed was the shift towards the platykurtosis of asymmetry distributions in the centre of the hybrid zone. Taken together, we suggest genetic variability for right–left asymmetries to be generally increased, but the developmental instability of mandible shape to be decreased, by hybridization. We hypothesize the decrease of developmental instability to be caused by overdominant effects on developmental dynamics rather than by increased heterozygosity. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 13–27.     

Developmental dynamics of ecomorphological convergence in a transcontinental lizard radiation

Phenotypic convergence has confounded evolutionary biologists for centuries, explained as adaptations to shared selective pressures, or alternatively, the result of limited developmental pathways. We tested the relative roles of adaptation and constraint in generating convergent cranial morphologies across a large lizard radiation, the Lacertidae, whose members inhabit diverse environments throughout the Old World and display high amounts of homoplasy associated with ecological niche. Using 3D X‐ray computed tomography, we quantified cranial shape variation associated with ontogeny, allometry, and ecology, covering all lacertid genera and one‐third of species diversity. Landmark‐based geometric morphometrics showed that cranial shape varied significantly among biomes, with substantial convergence among arid‐dwelling lineages. Comparisons of species cranial growth trajectories between biomes revealed that allometric postdisplacement, as evidenced by decreased elevation of a constant ontogenetic slope, drives the convergent paedomorphic appearance of independent arid‐dwelling forms. We hypothesize that observed heterochronic changes reflect temporal compression of ancestral life history in response to extreme environments, with associated phenotypes occurring as by‐products of adaptive shifts in reproductive investment. Although allometry has long been considered a developmental constraint, our results demonstrate that allometric flexibility during early ontogeny produces convergent ecomorphologies over vast temporal and spatial scales, thus dramatically obscuring underlying phylogenetic signals.     

Post-natal ontogeny of the mandible and ventral cranium in <Emphasis Type="Italic">Marmota</Emphasis> species (Rodentia,Sciuridae): allometry and phylogeny

Post-natal ontogenetic variation of the marmot mandible and ventral cranium is investigated in two species of the subgenus Petromarmota (M. caligata, M. flaviventris) and four species of the subgenus Marmota (M. caudata, M. himalayana, M. marmota, M. monax). Relationships between size and shape are analysed using geometric morphometric techniques. Sexual dimorphism is negligible, allometry explains the main changes in shape during growth, and males and females manifest similar allometric trajectories. Anatomical regions affected by size-related shape variation are similar in different species, but allometric trajectories are divergent. The largest modifications of the mandible and ventral cranium occur in regions directly involved in the mechanics of mastication. Relative to other anatomical regions, the size of areas of muscle insertion increases, while the size of sense organs, nerves and teeth generally decreases. Epigenetic factors, developmental constraints and size variation were found to be the major contributors in producing the observed allometric patterns. A phylogenetic signal was not evident in the comparison of allometric trajectories, but traits that allow discrimination of the Palaearctic marmots from the Nearctic species of Petromarmota are present early in development and are conserved during post-natal ontogeny.     

GEOMETRIC MORPHOMETRICS OF DEVELOPMENTAL INSTABILITY: ANALYZING PATTERNS OF FLUCTUATING ASYMMETRY WITH PROCRUSTES METHODS

Although fluctuating asymmetry has become popular as a measure of developmental instability, few studies have examined its developmental basis. We propose an approach to investigate the role of development for morphological asymmetry by means of morphometric methods. Our approach combines geometric morphometrics with the two-way ANOVA customary for conventional analyses of fluctuating asymmetry and can discover localized features of shape variation by examining the patterns of covariance among landmarks. This approach extends the notion of form used in studies of fluctuating asymmetry from collections of distances between morphological landmarks to an explicitly geometric concept of shape characterized by the configuration of landmarks. We demonstrate this approach with a study of asymmetry in the wings of tsetse flies (Glossina palpalis gambiensis). The analysis revealed significant fluctuating and directional asymmetry for shape as well as ample shape variation among individuals and between the offspring of young and old females. The morphological landmarks differed markedly in their degree of variability but multivariate patterns of landmark covariation identified by principal component analysis were generally similar between fluctuating asymmetry (within-individual variability) and variation among individuals. Therefore there is no evidence that special developmental processes control fluctuating asymmetry. We relate some of the morphometric patterns to processes known to be involved in the development of fly wings.     

Sexual selection,phenotypic variation,and allometry in genitalic and non‐genitalic traits in the sexually size‐dimorphic stick insect Micrarchus hystriculeus

The mobility hypothesis could explain the evolution of female‐biased size dimorphism if males with a smaller body size and longer legs have an advantage in scramble competition for mates. This hypothesis is tested by performing a selection analysis in the wild on Micrarchus hystriculeus (Westwood) (Phasmatodea), a sexually size dimorphic stick insect endemic to New Zealand. This analysis examined the form and strength of sexual selection on body size, leg lengths (front, mid and hind), and clasper size (a genitalic trait), and also quantified the degree of phenotypic variation and the allometric scaling pattern of these traits. By contrast to the mobility hypothesis, three lines of evidence were found to support significant stabilizing sexual selection on male hind leg length: a significant nonlinear selection gradient, negative static allometry, and a low degree of phenotypic variation. Hind leg length might be under stabilizing selection in males if having average‐sized legs facilitates female mounting or improves a male's ability to achieve the appropriate copulation position. As predicted, a negative allometric scaling pattern and low phenotypic variation of clasper size is suggestive of stabilizing selection and supports the ‘one‐size‐fits‐all’ hypothesis. Opposite to males, the mid and hind leg lengths of females showed positive static allometry. Relatively longer mid and hind leg lengths in larger females might benefit individuals via the better support of their larger abdomens. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 471–484.     

Does thermal plasticity align with local adaptation? An interspecific comparison of wing morphology in sepsid flies

Although genetic and plastic responses are sometimes considered as unrelated processes, their phenotypic effects may often align because genetic adaptation is expected to mirror phenotypic plasticity if adaptive, but run counter to it when maladaptive. Because the magnitude and direction of this alignment has further consequences for both the tempo and mode of adaptation, they are relevant for predicting an organisms’ reaction to environmental change. To better understand the interplay between phenotypic plasticity and genetic change in mediating adaptive phenotypic variation to climate variability, we here quantified genetic latitudinal variation and thermal plasticity in wing loading and wing shape in two closely related and widespread sepsid flies. Common garden rearing of 16 geographical populations reared across multiple temperatures revealed that wing loading decreases with latitude in both species. This pattern could be driven by selection for increased dispersal capacity in the cold. However, although allometry, sexual dimorphism, thermal plasticity and latitudinal differentiation in wing shape all show similar patterns in the two species, the relationship between the plastic and genetic responses differed between them. Although latitudinal differentiation (south to north) mirrored thermal plasticity (hot to cold) in Sepsis punctum, there was no relationship in Sepsis fulgens. While this suggests that thermal plasticity may have helped to mediate local adaptation in S. punctum, it also demonstrates that genetic wing shape differentiation and its relation to thermal plasticity may be complex and idiosyncratic, even among ecologically similar and closely related species. Hence, genetic responses can, but do not necessarily, align with phenotypic plasticity induced by changing environmental selection pressures.     

EVOLUTION OF VARIATION AND VARIABILITY UNDER FLUCTUATING,STABILIZING, AND DISRUPTIVE SELECTION

How variation and variability (the capacity to vary) may respond to selection remain open questions. Indeed, effects of different selection regimes on variational properties, such as canalization and developmental stability are under debate. We analyzed the patterns of among‐ and within‐individual variation in two wing‐shape characters in populations of Drosophila melanogaster maintained under fluctuating, disruptive, and stabilizing selection for more than 20 generations. Patterns of variation in wing size, which was not a direct target of selection, were also analyzed. Disruptive selection dramatically increased phenotypic variation in the two shape characters, but left phenotypic variation in wing size unaltered. Fluctuating and stabilizing selection consistently decreased phenotypic variation in all traits. In contrast, within‐individual variation, measured by the level of fluctuating asymmetry, increased for all traits under all selection regimes. These results suggest that canalization and developmental stability are evolvable and presumably controlled by different underlying genetic mechanisms, but the evolutionary responses are not consistent with an adaptive response to selection on variation. Selection also affected patterns of directional asymmetry, although inconsistently across traits and treatments.     

Individual variability in tree allometry determines light resource allocation in forest ecosystems: a hierarchical Bayesian approach

Tree species differences in crown size and shape are often highlighted as key characteristics determining light interception strategies and successional dynamics. The phenotypic plasticity of species in response to light and space availability suggests that intraspecific variability can have potential consequences on light interception and community dynamics. Species crown size varies depending on site characteristics and other factors at the individual level which differ from competition for light and space. These factors, such as individual genetic characteristics, past disturbances or environmental micro-site effects, combine with competition-related phenotypic plasticity to determine the individual variability in crown size. Site and individual variability are typically ignored when considering crown size and light interception by trees, and residual variability is relegated to a residual error term, which is then ignored when studying ecological processes. In the present study, we structured and quantified variability at the species, site, and individual levels for three frequently used tree allometric relations using fixed and random effects in a hierarchical Bayesian framework. We focused on two species: Abies alba (silver fir) and Picea abies (Norway spruce) in nine forest stands of the western Alps. We demonstrated that species had different allometric relations from site to site and that individual variability accounted for a large part of the variation in allometric relations. Using a spatially explicit radiation transmission model on real stands, we showed that individual variability in tree allometry had a substantial impact on light resource allocation in the forest. Individual variability in tree allometry modulates species’ light-intercepting ability. It generates heterogeneous light conditions under the canopy, with high light micro-habitats that may promote the regeneration of light-demanding species and slow down successional dynamics.