Static Allometry Research Articles

Sexually divergent selection, allometric constraints, and the evolution of sexual dimorphism in cichlids from Lake Tanganyika.

The evolution of sexual dimorphism is widely acknowledged as manifestation of sex-specific genetic architecture. Although empirical studies suggested that sexual dimorphism evolves as a joint consequence of constraints arising from the genetic architecture and sexually divergent selection, it remains unclear whether and how these established microevolutionary processes scale up to the macroevolutionary patterns of sexual dimorphism among taxa. Here, we studied how sexual selection and parental care drive sexual dimorphism in cichlid fishes from Lake Tanganyika. We found that male-male competition, female choice, and maternal mouthbrooding are associated with sexual dimorphism in body length, body color, and head length, respectively, despite strong allometric relationships between body length and head length. Within-species (static) allometry of head length on body length evolved as sex-specific responses to mouthbrooding where females evolved higher intercepts while males evolved steeper slopes. Thus, selection to increase mouth size in mouthbrooders may have broken down and reorganized the pattern of allometric constraints that are inherently strong and concordant between sexes. Furthermore, sex-specific responses to mouthbrooding left a remarkably clear signature on the macroevolutionary pattern, resulting in a decoupling of co-evolution in parameters of static allometries observed exclusively within maternal mouthbrooders. Our study provides multiple lines of evidence that are consistent with the idea that macroevolutionary patterns of sexual dimorphism in Lake Tanganyika cichlids result from sexually divergent selection. Our approach illustrates that an examination of within-population phenotypic variance in the phylogenetic comparative framework may facilitate nuanced understandings of how macroevolutionary patterns are generated by underlying microevolutionary processes.

Allometry and phylogenetic divergence: Correspondence or incongruence?

The potential connection between trends of within species variation, such as those of allometric change in morphology, and phylogenetic divergence has been a central topic in evolutionary biology for more than a century, including in the context of human evolution. In this study, I focus on size-related shape change in craniofacial proportions using a sample of more than 3200 adult Old World monkeys belonging to 78 species, of which 2942 specimens of 51 species are selected for the analysis. Using geometric morphometrics, I assess whether the divergence in the direction of static allometries increases in relation to phyletic differences. Because both small samples and taxonomic sampling may bias the results, I explore the sensitivity of the main analyses to the inclusion of more or less taxa depending on the choice of a threshold for the minimum sample size of a species. To better understand the impact of sampling error, I also use randomized subsampling experiments in the largest species samples. The study shows that static allometries vary broadly in directions without any evident phylogenetic signal. This variation is much larger than previously found in ontogenetic trajectories of Old World monkeys, but the conclusion of no congruence with phylogenetic divergence is the same. Yet, the effect of sampling error clearly contributes to inaccuracies and tends to magnify the differences in allometric change. Thus, morphometric research at the boundary between micro- and macro-evolution in primates, and more generally in mammals, critically needs very large and representative samples. Besides sampling error, I suggest other non-mutually exclusive explanations for the lack of correspondence between allometric and phylogenetic divergence in Old World monkeys, and also discuss why directions might be more variable in static compared to ontogenetic trajectories. Even if allometric variation may be a poor source of information in relation to phylogeny, the evolution of allometry is a fascinating subject and the study of size-related shape changes remains a fundamental piece of the puzzle to understand morphological variation within and between species in primates and other animals.

Insect Flight Energetics and the Evolution of Size, Form, and Function.

Flying insects vary greatly in body size and wing proportions, significantly impacting their flight energetics. Generally, the larger the insect, the slower its flight wingbeat frequency. However, variation in frequency is also explained by differences in wing proportions, where larger-winged insects tend to have lower frequencies. These associations affect the energy required for flight. The correlated evolution of flight form and function can be further defined using a lineage of closely related bee species varying in body mass. The decline in flight wingbeat frequency with increasing size is paralleled by the flight mass-specific metabolic rate. The specific scaling exponents observed can be predicted from the wing area allometry, where a greater increase (hyperallometry) leads to a more pronounced effect on flight energetics, and hypoallometry can lead to no change in frequency and metabolic rate across species. The metabolic properties of the flight muscles also vary with body mass and wing proportions, as observed from the activity of glycolytic enzymes and the phospholipid compositions of muscle tissue, connecting morphological differences with muscle metabolic properties. The evolutionary scaling observed across species is recapitulated within species. The static allometry observed within the bumblebee Bombus impatiens, where the wing area is proportional and isometric, affects wingbeat frequency and metabolic rate, which is predicted to decrease with an increase in size. Intraspecific variation in flight muscle tissue properties is also related to flight metabolic rate. The role of developmental processes and phenotypic plasticity in explaining intraspecific differences is central to our understanding of flight energetics. These studies provide a framework where static allometry observed within species gives rise to evolutionary allometry, connecting the evolution of size, form, and function associated with insect flight.

A Geometric Morphometrics Approach to the Study of Natural Variations and Hybrid Detection in Populations of Alnus incana (L.) Moench and Alnus rohlenae Vít, Douda and Mandák.

Landmark-based geometric morphometrics (GM) was used to examine, for the first time, spontaneous hybridization between Alnus incana (L.) Moench and Alnus rohlenae Vít, Douda and Mandák, and to assess inter- and intrapopulation variability in leaf shape, leaf size and venation in natural populations in Serbia (Western Balkans). Two geographically distant (30 km) and two close (1.2 km) populations were selected to examine hybridization. The variability in leaf shapes was assessed by canonical variate analysis and linear discriminant analysis performed on the symmetric component of variation. Covariation between the symmetric component of shape variation and the number of pairs of secondary leaf veins was investigated with partial least squares analysis. Static allometry was examined for the first time in the genus Alnus Mill. A higher proportion of A. incana leaves was classified as A. rohlenae in geographically close populations, which is in accordance with the hypothesis about spontaneous hybridization. No single leaf of A. rohlenae was classified as A. incana, indicating that putative hybrids can only be found in grey alder populations. This study demonstrates that GM is a powerful tool for species delimitation and hybrid detection in the genus Alnus and it can be used for preliminary screening in hybrid zones.

Ecological implications of allometric relationships in American alligators (Alligator mississippiensis)

Morphometric allometry, the effect of size on morphological variation, has been of great interest for evolutionary biologist and is currently used in fields such as wildlife ecology to inform management and conservation. We assessed American alligator (Alligator mississippiensis) morphological static allometry across the Greater Everglades ecosystem in South Florida, United States using a robust dataset (~ 22 years) and investigated effects of sex, habitat, and sampling area on morphological relationships. Regression models showed very strong evidence of a linear relationship between variables explaining equal to or above 92% of the variation in the data. Most trait–size relationships (8 out of 11 assessed) showed hyperallometry (positive allometry) with slope deviations from isometry between 0.1 and 0.2 units while the other three relationships were isometric. Sampling area, type of habitat, and in a lesser extent sex influenced allometric coefficients (slope and intercept) across several relationships, likely as result of differing landscapes and ecosystem dynamic alterations and sexual dimorphism. We discuss our findings in terms of the biology of the species as well as the usefulness of our results in the context of ecosystem restoration and conservation of the species. Finally, we provide recommendations when using trait–length relationships to infer population nutritional—health condition and demographics.

The evolution of positive allometry and exaggerated traits in a diverse beetle clade

Abstract Understanding variation in trait allometry and the drivers of variation in sexually selected traits is a major theme in evolutionary biology. The static allometries of sexually selected traits are often positive due to disproportional investment by large individuals into trait size. Comparative studies of weapon allometry are rare, and typically focus on variation along a single dimension (e.g. length), despite weapons often diverging dramatically in shape. Furthermore, studies predominantly focus on groups where weapons have evolved as novel structures (e.g. horns), despite most weapons arising from modifications of existing structures. We test the hypothesis that sexual selection drives variation in static allometry using a phylogenetic comparative approach with 59 brentine weevil species showing remarkable variation in trait exaggeration and sexual size dimorphism (SSD). Contrasting two dimensions of head size exaggeration (a sexually selected trait) and elytron length (a nonsexual trait), positive static allometry was common across both measures of male head size, but not females, and there was positive covariance between male head static allometry and SSD across species. Positive static allometry for male elytron length was less common, but did show positive covariance with SSD, possibly due to the function of wings as compensatory structures for bearing large weapons. Our findings support the hypothesis that sexual selection drives the evolution of allometries both within and among species, and that the modification of existing structures to be used as weapons does not limit the potential for positive static allometry. Read the free Plain Language Summary for this article on the Journal blog.

Maxillary morphology of chimpanzees: Captive versus wild environments.

Morphological studies typically avoid using osteological samples that derive from captive animals because it is assumed that their morphology is not representative of wild populations. Rearing environments indeed differ between wild and captive individuals. For example, mechanical properties of the diets provided to captive animals can be drastically different from the food present in their natural habitats, which could impact cranial morphology and dental health. Here, we examine morphological differences in the maxillae of wild versus captive chimpanzees (Pan troglodytes) given the prominence of this species in comparative samples used in human evolution research and the key role of the maxilla in such studies. Size and shape were analysed using three-dimensional geometric morphometric methods based on computed tomography scans of 94 wild and 30 captive specimens. Captive individuals have on average larger and more asymmetrical maxillae than wild chimpanzees, and significant differences are present in their maxillary shapes. A large proportion of these shape differences are attributable to static allometry, but wild and captive specimens still differ significantly from each other after allometric size adjustment of the shape data. Levels of shape variation are higher in the captive group, while the degree of size variation is likely similar in our two samples. Results are discussed in the context of ontogenetic growth trajectories, changes in dietary texture, an altered social environment, and generational differences. Additionally, sample simulations show that size and shape differences between chimpanzees and bonobos (Pan paniscus) are exaggerated when part of the wild sample is replaced with captive chimpanzees. Overall, this study confirms that maxillae of captive chimpanzees should not be included in morphological or taxonomic analyses when the objective is to characterise the species.

Patterns of Sexual Dimorphism, Static Allometry, and Modularity in the Skull of the Ethiopian White-Footed Mouse, Stenocephalemys albipes (Rodentia: Muridae)

Patterns of Sexual Dimorphism, Static Allometry, and Modularity in the Skull of the Ethiopian White-Footed Mouse, Stenocephalemys albipes (Rodentia: Muridae)

Morphology and diet are decoupled in nearshore notothenoids from King George Island, West Antarctica.

Antarctic notothenioid fishes show wide adaptive morphological radiation, linked to habitat preferences and food composition. However, direct comparisons of phenotypic variability and feeding habits are still lacking, particularly in stages inhabiting nearshore areas. To assess these relationships, we collected juveniles and adults of the most common benthic species inhabiting shallow waters off the South Shetland Islands within a similar size range, the plunderfish Harpagifer antarcticus, the black rockcod Notothenia coriiceps, and the marbled rockcod Notothenia rossii. Individual size ranges varied from 44.0 to 98.9 mm standard length (LS) (H. antarcticus), from 95.8 to 109.3 mm LS (N. coriiceps), and from 63.0 to 113.0 mm LS (N. rossii). Notothenioid fish showed different morphospace variability, being larger for H. antarcticus than the other Notothenia species and associated with the position of the posterior end of the operculum, along with the location and relative size of the eye. The evolutionary allometry was low, but the static allometry was much higher, especially for H. antarcticus and N. rossii. The diet was mainly carnivorous, consisting of amphipods and euphausiids. Macroalgae were scarce or totally absent in the gut contents of all species. Only H. antarcticus showed an increase in the prey number and ingested prey volume with fish size. Finally, there was a significant covariation between shape changes and LS in all species (allometric effects), however, not with prey composition, probably due to the small size range or ontogenetic stage and the relative similarity (or lack of contrast) in the benthic environment that they utilized.

Utilizing geometric morphometrics to investigate gene function during organ growth: Insights through the study of beetle horn shape allometry.

Static allometry is a major component of morphological variation. Much of the literature on the development of allometry investigates how functional perturbations of diverse pathways affect the relationship between trait size and body size. Often, this is done with the explicit objective to identify developmental mechanisms that enable the sensing of organ size and the regulation of relative growth. However, changes in relative trait size can also be brought about by a range of other distinctly different developmental processes, such as changes in patterning or tissue folding, yet standard univariate biometric approaches are usually unable to distinguish among alternative explanations. Here, we utilize geometric morphometrics to investigate the degree to which functional genetic manipulations known to affect the size of dung beetle horns also recapitulate the effect of horn shape allometry. We reasoned that the knockdown phenotypes of pathways governing relative growth should closely resemble shape variation induced by natural allometric variation. In contrast, we predicted that if genes primarily affect alternative developmental processes, knockdown effects should align poorly with shape allometry. We find that the knockdown effects of several genes (e.g., doublesex, Foxo) indeed closely aligned with shape allometry, indicating that their corresponding pathways may indeed function primarily in the regulation of relative trait growth. In contrast, other knockdown effects (e.g., Distal-less, dachs) failed to align with allometry, implicating these pathways in potentially scaling-independent processes. Our findings moderate the interpretation of studies focusing on trait length and highlight the usefulness of multivariate approaches to study allometry and phenotypic plasticity.

Rensch's rule: linking intraspecific to evolutionary allometry.

Sexual dimorphism describes phenotypic differences between the sexes; the most prominent of which is sexual size dimorphism (SSD). Rensch's rule (RR) is an allometric trend in which SSD increases in male-larger taxa and decreases in female-larger ones. Covariation between a trait and overall size within and across species can both be affected by sexual and natural selection. Thus, intraspecific allometric variation could influence the expression of RR. Here we used computer simulations to dissect how RR emerges under specific allometric patterns of intraspecific sexual differentiation in a trait. We found that sexual differentiation in static allometric slopes is the main determinant of RR. Based on our findings, RR and its converse can manifest in both body size and other traits. As a realistic showcase, we also examined RR and static allometry of different body parts in Mediterranean green lizards to establish whether intraspecific and evolutionary allometry are linked. Here, we identified RR and its converse for different traits, where the amount of sexual differentiation in static allometric slopes within species had a significant contribution to RR. Integrating the simulations and the empirical case we corroborate that sexual differentiation in static allometric slopes is a major parameter affecting evolutionary allometry.

Sexual size and shape dimorphism, and allometric scaling in the pupal and adult traits of Eristalis tenax.

The patterns and amount of variation in size, shape, and/or life history traits between females and males are fundamentally important to gain the comprehensive understanding of the evolution of phenotypic diversity. In addition, the covariation of phenotypic traits can significantly contribute to morphological diversification and sexual dimorphism (SD). Using linear and geometric morphometrics, 237 Eristalis tenax specimens sampled from five populations were, therefore, comparatively assessed for the variation in sexual size dimorphism (SSD), sexual shape dimorphism (SShD), and life history traits, as well as for trait covariation (ontogenetic and static allometry). Pupal body, adult wing, and body mass traits were analyzed. Female-biased SSD was observed for pupal length, width, and centroid size, adult wing centroid size, mass, wing loading, and wing area. Conversely, pupal length/width ratio, developmental time, and mass were not found to be sexually dimorphic. Next, wing SShD, but not pupal body SShD was revealed, while allometry was found to be an important "determinant of SD" at the adult stage, with only a minor impact at the pupal stage. By comparing the patterns of covariance (based on allometric slope and intercept) between respective body mass and morphometric traits of pupae and adults, greater variation in allometric slopes was found in adult traits, while static allometries of the two stages significantly differed, as well. Finally, the results indicate that changes in the allometric intercept could be an important source of intraspecific variation and SD in drone fly adults.

Temperature-driven heterochrony as a main evolutionary response to climate changes in conodonts.

Can we predict the evolutionary response of organisms to climate changes? The direction of greatest intraspecific phenotypic variance is thought to correspond to an 'evolutionary line of least resistance', i.e. a taxon's phenotype is expected to evolve along that general direction, if not constrained otherwise. In particular, heterochrony, whereby the timing or rate of developmental processes are modified, has often been invoked to describe evolutionary trajectories and it may be advantageous to organisms when rapid adaptation is critical. Yet, to date, little is known empirically as to which covariation patterns, whether static allometry, as measured in adult forms only, or ontogenetic allometry, the basis for heterochrony, may be prevalent in what circumstances. Here, we quantify the morphology of segminiplanate conodont elements during two distinct time intervals separated by more than 130 Myr: the Devonian-Carboniferous boundary and the Carnian-Norian boundary (Late Triassic). We evidence that the corresponding species share similar patterns of intraspecific static allometry. Yet, during both crises, conodont evolution was decoupled from this common evolutionary line of least resistance. Instead, it followed heterochrony-like trajectories that furthermore appear as driven by ocean temperature. This may have implications for our interpretation of conodonts' and past marine ecosystems' response to environmental perturbations.

Static allometries do not reflect evolutionary allometry in exaggerated weaponry of male New Zealand sheetweb spiders (Cambridgea spp.).

Across the animal kingdom, exaggerated weaponry is frequently used by one sex to contest access for potential mates. Within species, if disproportionate investment in weaponry confers an advantage to larger individuals, this may result in positive static allometry. It is predicted that the same selective pressures may also lead to positive evolutionary allometry, where larger species bear disproportionately large weapons on average, compared with smaller species. Furthermore, in species with stronger sexual selection, the static allometries of those weapons are expected to steepen. All adult males across the New Zealand sheetweb spider genus Cambridgea bear exaggerated chelicerae, which are used to compete for control of females' webs. Here, we characterize the distribution of chelicera lengths within each sex of 12 Cambridgea species to show that chelicerae almost always exhibit positive static allometry in males while female chelicera lengths are consistently isometric. We use comparative phylogenetic methods to demonstrate that the slopes of static allometries steepen in males of larger species but that the ratio of average chelicera length to cephalothorax width is tightly conserved across taxa, leading to an isometric evolutionary allometry. While static allometries indeed steepen in larger species, possibly due to stronger sexual selection, this conservation of relative trait size suggests that chelicera length is subject to other stabilizing selective pressures. Changes to species body plans might be constrained, while still allowing for disproportionate investment in weapon traits in the upper range of intraspecific body sizes.

Can Patterns of Static Allometry be Inferred from Regimes of Sexual Selection in the Japanese Beetle?

Can Patterns of Static Allometry be Inferred from Regimes of Sexual Selection in the Japanese Beetle?

Evolutionary allometry and ecological correlates of fang length evolution in vipers.

Traits for prey acquisition form the phenotypic interface of predator-prey interactions. In venomous predators, morphological variation in venom delivery apparatus like fangs and stingers may be optimized for dispatching prey. Here, we determine how a single dimension of venom injection systems evolves in response to variation in the size, climatic conditions and dietary ecology of viperid snakes. We measured fang length in more than 1900 museum specimens representing 199 viper species (55% of recognized species). We find both phylogenetic signal and within-clade variation in relative fang length across vipers suggesting both general taxonomic trends and potential adaptive divergence in fang length. We recover positive evolutionary allometry and little static allometry in fang length. Proportionally longer fangs have evolved in larger species, which may facilitate venom injection in more voluminous prey. Finally, we leverage climatic and diet data to assess the global correlates of fang length. We find that models of fang length evolution are improved through the inclusion of both temperature and diet, particularly the extent to which diets are mammal-heavy diets. These findings demonstrate how adaptive variation can emerge among components of complex prey capture systems.

Evaluation of Body Size Indicators for Morphological Analyses in Two Sister Species of Genus Dorcus (Coleoptera, Lucanidae).

The relationship between trait and body size, i.e., the scaling relationship or static allometry, is an essential concept for investigating trait size. However, usage of an inappropriate body size indicator can lead to misinterpretation of morphology. In this study, we examined several possible body size indicators in two closely related stag beetle species, Dorcus rectus and Dorcus amamianus. We raised animals in captivity and used pupal weight as a measure of true, or overall body size, and then evaluated six adult morphological traits to test whether these traits could be reliably used as body size indicators in static scaling relationship comparisons. We analyzed two comparisons, between sexes in same species and between species in same sex. We showed that the most appropriate body size indicators differ depending on the comparisons. Our results indicated that the scaling relationship of focal traits could be over- or under-estimated depending on which body size indicators are used.

Evaluating the drivers and engines of morphological diversification in the invasive geckoHemidactylus mabouia(Moreau de Jonnès, 1818) (Squamata: Gekkonidae)

AbstractDevelopment determines the range of possible phenotypes that can be produced and exposed to selection and has a major role in the evolutionary trajectories of species. Nevertheless, development is itself subject to evolutionary forces. Here, we describe differences at the ontogenetic and population levels in head and limb proportions of the invasive gecko Hemidactylus mabouia, to assess the developmental mechanisms and extrinsic forces associated with morphological diversification during colonization of novel habitats. We have found that allometric trajectories of most skeletal traits remain constant throughout postnatal development. Linear morphometric analysis did not find multivariate differences between ontogenetic stages or sexes. When comparing populations, our results showed that the divergence of the corresponding external measures was explained by shifts in the intercept of static allometry curves, indicating that differences arose early in development. Populations aggregated into two morphological groups that did not correspond to the groups formed on the basis of genetic structure. Using two different approaches, we found support for an adaptive hypothesis when comparing observed patterns of morphological variation with that expected under neutral evolutionary models.

Correction to: Deceived, but not betrayed: static allometry suggests female ornaments in the long‑tailed dance fly (Rhamphomyia longicauda) exaggerate condition to males

Correction to: Deceived, but not betrayed: static allometry suggests female ornaments in the long‑tailed dance fly (Rhamphomyia longicauda) exaggerate condition to males

Size variation, allometry and mating success in Aotearoa|New Zealand kelp flies (Coelopidae)

The need to respond quickly to the presence of an ephemeral resource required for breeding is often a feature of scramble competition mating systems. Scramble competition mating systems can feature extreme levels of sexual conflict and coercive mating by males. As a result, sexual selection can act on various traits used by males to overcome female resistance behaviours. Selection on these traits may result in significant intra and intersexual size variation and sexual dimorphism. Additionally, traits that influence mating success in males often show positive static allometry. Kelp flies (Coelopidae) are a small family of Diptera which specialise on wrack (beach cast marine macroalgae), a highly ephemeral resource. The mating system of these flies involves high levels of sexual conflict, with females rejecting all male mating attempts. In this study we describe intra and intersexual size variation and static allometry of traits in two of Aotearoa|New Zealand’s species, Coelopella curvipes and Chaetocoelopa littoralis. In addition, we investigate the mating behaviour of C. littoralis under ecologically relevant mating conditions. We found high levels of variation in both species with significant evidence of sexual dimorphism across all traits measured in C. littoralis, and in mid tibia length in C. curvipes. Furthermore, mid tibia length in both species exhibits positive static allometry and is disproportionally larger in larger males, suggesting that this trait in particular may be under strong sexual selection. We found that larger male C. littoralis which attempt to mate are significantly more likely to mate successfully demonstrating a large-size advantage in this species similar to findings across the Coelopidae. However, we only found a non-significant trend towards a mating advantage for males with longer mid-tibiae. We discuss these findings with reference to the population dynamics and ecology of these species.