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.

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.

Exceptionally Steep Brain-Body Evolutionary Allometry Underlies the Unique Encephalization of Osteoglossiformes.

Brain-body static allometry, which is the relationship between brain size and body size within species, is thought to reflect developmental and genetic constraints. Existing evidence suggests that the evolution of large brain size without accompanying changes in body size (that is, encephalization) may occur when this constraint is relaxed. Teleost fish species are generally characterized by having close-fitting brain-body static allometries, leading to strong allometric constraints and small relative brain sizes. However, one order of teleost, Osteoglossiformes, underwent extreme encephalization, and its mechanistic bases are unknown. Here, I used a dataset and phylogeny encompassing 859 teleost species to demonstrate that the encephalization of Osteoglossiformes occurred through an increase in the slope of evolutionary (among-species) brain-body allometry. The slope is virtually isometric (1.03 ± 0.09 SE), making it one of the steepest evolutionary brain-body allometric slopes reported to date, and it deviates significantly from the evolutionary brain-body allometric slopes of other clades of teleost. Examination of the relationship between static allometric parameters (intercepts and slopes) and evolutionary allometry revealed that the dramatic steepening of the evolutionary allometric slope in Osteoglossiformes was a combined result of evolution in the slopes and intercepts of static allometry. These results suggest that the evolution of static allometry, which likely has been driven by evolutionary changes in the rate and timing of brain development, has facilitated the unique encephalization of Osteoglossiformes.

Static allometry of a small-bodied omnivore: body size and limb scaling of an island fox and inferences for Homo floresiensis.

Island dwarfing is a paraphyletic adaptation across numerous mammalian genera. From mammoths to foxes, extreme body size reduction is shared by diverse organisms that migrate to an island environment. Because it largely occurs owing to ecological variables, not phylogenetic ones, skeletal characters in a dwarfed taxon compared with its ancestor may appear abnormal. As a result, allometric patterns between body size and morphological traits may differ for an island dwarf compared with its ancestor. The diminutive Late Pleistocene hominin, Homo floresiensis, displays a unique character suite that is outside of the normal range of variation for any extinct or extant hominin species. To better explain these as ecological traits due to island dwarfing, this research looks at how dwarfing on islands influences limb scaling and proportions in an organism in a similar ecological niche as H. floresiensis. Here, I analyze absolute limb lengths and static allometry of limb lengths regressed on predicted body mass of dwarfed island foxes and their nondwarfed relatives. Dwarfed island foxes have significantly smaller intercepts but steeper slopes of all limb elements regressed on predicted body mass than the mainland gray fox. These allometric alterations produce limbs in the island fox that are significantly shorter than predicted for a nondwarfed gray fox of similar body mass. In addition, the humerofemoral, intermembral, and brachial indices are significantly different. These results provide a novel model for understanding skeletal variation of island endemic forms. Unique body size and proportions of H. floresiensis are plausible as ecological adaptations and likely not examples of symplesiomorphies with Australopithecus sp. Caution should be exerted when comparing an island dwarf with a closely related species as deviations from allometric expectations may be common.

Allometric scaling of aerobic fitness outputs in school-aged pubertal girls.

BACKGROUND: This study aimed to determine the allometric exponents for concurrent size descriptors (stature, body mass and fat-free mass) and also to examine the contribution of chronological age and pubertal status combined with above mentioned size descriptors to explain inter-individual variability in the peak of oxygen uptake (VO2peak) among girls during circumpubertal years. METHODS: The final sample included 51 girls (10.7-13.5 years). VO2peak was derived from an incremental progressive maximal protocol using a motorized treadmill. Anthropometry included body mass, stature and skinfolds. Measurements were performed by a single trained observer. Sexual maturation was assessed as self-reported stage of pubic hair (PH) development. Static allometric models were explored as an alternative to physiological output per unit of size descriptors. Allometry also considered chronological age and sexual maturation as dummy variable (PH2 vs. PH3 and PH3 vs. PH4). RESULTS: Scaling coefficients for stature, body mass and fat-free mass were 1.463 (95%CI: 0.476 to 2.449), 0.516 (95%CI: 0.367 to 0.666) and 0.723 (95%CI: 0.494 to 0.951), respectively. The inclusion of sexual maturation increased explained variance for VO2peak (55% for PH2 vs. PH3 and 47% for PH3 vs. PH4). Body mass was identified as the most prominent body size descriptor in the PH2 vs. PH3 while fat-free mass was the most relevant predictor combined with PH3 vs. PH4. CONCLUSIONS: Body mass and fat-free mass seemed to establish a non-linear relationship with VO2peak. Across puberty, inter-individual variability in VO2peak is explained by sexual maturation combined with whole body during early puberty and by sexual maturation and fat-free mass during late puberty. Additional studies need to confirm ontogenetic allometric models during years of maximal growth.

The First Morphometric Study of the Horn Morphological Pattern in a Geotrupidae: The Case of the Dor Beetle Ceratophyus rossii Jekel, 1865.

Among beetles, thousands of species develop horns, the size of which is often extraordinarily disproportionate with respect to body size. The Scarabaeidae is the family in which horned species are most predominant, but other families, such as the Geotrupidae (dor beetles), also show remarkable horns, although in a more limited number of species. Horn expression mechanisms are well documented in Scarabaeidae but, despite the wealth of studies on this family, the horn morphological pattern of the Geotrupidae, to our knowledge, has never been investigated. In this paper, we describe for the first time the horn expression pattern in a dor beetle. As a study species, we chose Ceratophyus rossii, an Italian endemic dor beetle of the protected Mediterranean maquis in Tuscany, which shows remarkable head and pronotal horns in males and a notable cephalic horn in females. We identified and modeled shape and size horn patterns combining traditional and geometric morphometric approaches. We discuss the results in the wider landscape of developmental models described for other, more well-characterized, scarab beetles.

Ontogenetic and static allometry in the human face: contrasting Khoisan and Inuit.

OBJECTIVES: Regional differences in modern human facial features are present at birth, and ontogenetic allometry contributes to variation in adults. However, details regarding differential rates of growth and timing among regional groups are lacking. We explore ontogenetic and static allometry in a cross-sectional sample spanning Africa, Europe and North America, and evaluate tempo and mode in two regional groups with very different adult facial morphology, the Khoisan and Inuit. MATERIALS AND METHODS: Semilandmark geometric morphometric methods, multivariate statistics and growth simulations were used to quantify and compare patterns of facial growth and development. RESULTS: Regional-specific facial morphology develops early in ontogeny. The Inuit has the most distinct morphology and exhibits heterochronic differences in development compared to other regional groups. Allometric patterns differ during early postnatal development, when significant increases in size are coupled with large amounts of shape changes. All regional groups share a common adult static allometric trajectory, which can be attributed to sexual dimorphism, and the corresponding allometric shape changes resemble developmental patterns during later ontogeny. DISCUSSION: The amount and pattern of growth and development may not be shared between regional groups, indicating that a certain degree of flexibility is allowed for in order to achieve adult size. In early postnatal development the face is less constrained compared to other parts of the cranium allowing for greater evolvability. The early development of region-specific facial features combined with heterochronic differences in timing or rate of growth, reflected in differences in facial size, suggest different patterns of postnatal growth.

Allometric modelling of peak oxygen uptake in male soccer players of 8-18 years of age.

BACKGROUND: Peak oxygen uptake (VO2peak) is routinely scaled as mL O2 per kilogram body mass despite theoretical and statistical limitations of using ratios. AIM: To examine the contribution of maturity status and body size descriptors to age-associated inter-individual variability in VO2peak and to present static allometric models to normalize VO2peak in male youth soccer players. SUBJECTS AND METHODS: Total body and estimates of total and regional lean mass were measured with dual energy X-ray absorptiometry in a cross-sectional sample of Portuguese male soccer players. The sample was divided into three age groups for analysis: 8-12 years, 13-15 years and 16-18 years. VO2peak was estimated using an incremental maximal exercise test on a motorized treadmill. Static allometric models were used to normalize VO2peak. RESULTS: The independent variables with the best statistical fit explained 72% in the younger group (lean body mass: k = 1.07), 52% in mid-adolescent players (lean body mass: k = 0.93) and 31% in the older group (body mass: k = 0.51) of variance in VO2peak. The inclusion of the exponential term pubertal status marginally increased the explained variance in VO2peak (adjusted R(2 )= 36-75%) and provided statistical adjustments to the size descriptors coefficients. CONCLUSION: The allometric coefficients and exponents evidenced the varying inter-relationship among size descriptors and maturity status with aerobic fitness from early to late-adolescence. Lean body mass, lean lower limbs mass and body mass combined with pubertal status explain most of the inter-individual variability in VO2peak among youth soccer players.

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.

Extreme range in adult body size reveals hidden trade-offs among sexually selected traits.

Sexually selected weapons used to monopolize mating opportunities are predicted to trade-off with traits used in competition for fertilization. Yet, the limited size range typically found among adults of a species often precludes clear comparisons between population-level and individual-level relative trait investment. The jousting weevil, Brentus anchorago (Coleoptera: Brentidae), varies more than 26-fold in body mass, which is among the most extreme adult body size ranges of any solitary terrestrial species. We reveal a trade-off at a population level: hypermetric scaling in male weapons (slope = 1.59) and a closely mirrored reversal in allocation to postcopulatory traits (slope = 0.54). Yet, at the individual level, we find the opposite pattern; males that invest relatively more in weapons for their size class also invest more in postcopulatory traits. Across 36 dung beetle and 41 brentine weevil species, we find the allometric slope explains more trait variation at larger body size ranges; in brentines, population-level scaling patterns become more detectable in species with a larger range in adult body size. Our findings reveal that population-level allometries and individual-level trade-offs can both be important in shaping relative trait allocation; we highlight that the adult body size range is rarely examined but may be integral to gaining a deeper understanding of trade-offs in reproductive allocation.

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.

Ontogenetic progression of individual head size in the larvae of the beetle Trypoxylus dichotomus (Coleoptera: Scarabaeidae): catch-up growth within stages and per-stage growth rate changes across stages.

The ontogenetic progression of insect larval head size has received much attention due to its fundamental and practical importance. However, although previous studies have analyzed the population mean head size, such an approach may not be appropriate for developmental studies of larval head sizes when the trajectory of individual head size growth is correlated with pre-molt head size and developmental stage. Additionally, there is covariation between the head and body sizes; however, few studies have compared the ontogenetic progression of individual head sizes with that of individual body sizes. In this investigation, the per-stage growth rates (PSGRs) for head width (HW) and cubic-rooted body mass at the beginning of each instar (body size, BS) were assessed in Trypoxylus dichotomus. Linear models were used to test the size- and instar-dependence of the ontogenetic progression of individual HW and BS. The individual PSGRs of the HW (iPSGRH) and BS (iPSGRB) were then compared. In addition, the allometric relationship between HW and BS was examined. The iPSGRH was negatively correlated with the pre-molt HW at every instar (i.e., head catch-up growth). Furthermore, the mean iPSGRH at L2 was relatively higher than that at L1 when the pre-molt HW was used as covariate in the analysis (i.e., instar-effect), whereas the mean iPSGRH decreased ontogenetically. The iPSGRB showed catch-up growth and instar-effects similar to those of iPSGRH; however, iPSGRH was found to be lower than iPSGRB. Due to the differences between the PSGRs for the larval head and body, the larval head size showed negative ontogenetic allometry against body size.

Changing allometric relationships among fossil and Recent populations in two colonial species.

Allometry is vital for understanding the mechanisms underlying phenotypic evolution. Despite a large body of literature on allometry, studies based on fossil time series are limited for solitary organisms and nonexistent for colonial organisms. Allometric relationships have been found to be relatively constant across Recent populations of the same species, separated by space, but variable among fossil populations separated by thousands of years. How stable are allometric relationships at the module level for colonial organisms? We address this question using two extant species of the cheilostome bryozoan Microporella with fossil records spanning the Pleistocene of New Zealand. We investigate size covariation between feeding modules and three traits with separate functions (reproductive, resource uptake, and defense). We found that within-population (static) allometry can change on timescales of at least 0.1 million years. These within-population relationships do not consistently predict overintraspecific evolutionary allometry, which in turn does not predict those estimated at the genus level. Different functional traits are constrained to different extents by module size with defensive traits being the least constrained and most evolvable, compared with reproductive and resource uptake traits. Our study highlights the potential of colonial organisms in understanding the constraints and drivers of long-term phenotypic change.

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.

Allometry and morphological trait relationship in the sexually dimorphic Chinese dobsonfly, Acanthacorydalisasiatica (Wood-Mason, 1884) (Megaloptera, Corydalidae).

Male insects with large weapons such as horns and elongate mandibles would be expected to invest more on such structures than other parts of the body for advantages in male to male competition for mating. In male genitalia, however, intermediate size provides a better fit for more females than small or large sizes, and such a male would leave more offspring regardless of their body size. These predictions were tested using a static allometry analysis between body size and other trait sizes. Acanthacorydalisasiatica is a large dobsonfly (Megalotera) and males have conspicuously large mandibles used as weapons. We examined the hypothesis that the male mandibles of this sexually dimorphic species are sexually selected to enlarge, whereas the male genitalia are stable to be intermediate regardless of a great variation in body size. The results, as predicted, showed positive allometry between male body size and mandible length but negative allometry between male body size and ectoproct length (a male grasping structure). Sperm are transferred through a small spermatophore attached externally to the female genital opening, so it may be evolutionarily unnecessary to develop an enlarged male genital size. In contrast, there may be a trade-off between male mandible size and wing length, because of negative allometry between body size and wing length in males but isometry between them in females.

Male Horn Lack of Allometry May be Tied to Food Relocation Behaviour in Lifting Dung Beetles (Coleoptera, Scarabaeidae, Eucraniini).

The small dung beetle tribe Eucraniini includes extremely specialized species that have been defined as "lifters" according to their food relocation behaviour. They are characterized by the presence of well-developed expansions on the head and pronotum, which can be included in the large and varied group of horns, whose presence is usually related to complex reproductive tactics. In this study, two closely related species, Anomiopsoides cavifrons and A. heteroclyta, were examined employing traditional and geometric morphometrics to test whether the Eucraniini has polymorphic males that might exhibit different reproductive tactics, as in the sister tribe Phanaeini, for which a male trimorphism was demonstrated. If also present in Eucraniini polyphenism could be considered a plesiomorphy common to the two clades. The inter- and intraspecific shape variation and object symmetry of the head and the scaling relationships between body size and traits were evaluated. Marked interspecific and small intraspecific differences in shape variation, high symmetry, and similar isometric growth patterns were shown in both species. The hypothesis of male polymorphism in Anomiopsoides was thus rejected. Instead, the results supported the alternative hypothesis that Eucraniini lacks male polymorphism, perhaps due to functional constraints affecting the shape of the structures involved in their peculiar food relocating behaviour.

Conservative whole-organ scaling contrasts with highly labile suborgan scaling differences among compound eyes of closely related Formica ants.

Static allometries determine how organ size scales in relation to body mass. The extent to which these allometric relationships are free to evolve, and how they differ among closely related species, has been debated extensively and remains unclear; changes in intercept appear common, but changes in slope are far rarer. Here, we compare the scaling relationships that govern the structure of compound eyes of four closely related ant species from the genus Formica. Comparison among these species revealed changes in intercept but not slope in the allometric scaling relationships governing eye area, facet number, and mean facet diameter. Moreover, the scaling between facet diameter and number was conserved across all four species. In contrast, facet diameters from distinct regions of the compound eye differed in both intercept and slope within a single species and when comparing homologous regions among species. Thus, even when species are conservative in the scaling of whole organs, they can differ substantially in regional scaling within organs. This, at least partly, explains how species can produce organs that adhere to genus wide scaling relationships while still being able to invest differentially in particular regions of organs to produce specific features that match their ecology.

Sexual dimorphism of facial appearance in ageing human adults: A cross-sectional study.

In the forensic sciences, knowledge of facial ageing is very important in searching for both dead and living individuals. Ageing estimations typically model the biological profile, which can be compared to missing persons. The main goals of this current study were to construct ageing trajectories for adult human faces of both sexes and evaluate sexual dimorphism in relation to static allometry. Our study was based on the analysis of three-dimensional facial surface models of 194 individuals 20-80 years of age. The evaluation consisted of a dense correspondence analysis of facial scans and multivariate statistics. It was shown that both age and sex have a significant influence on facial form and shape. Male features included a longer face, with more protruded foreheads, eyebrow ridges and nose, including the region under the upper lip and mandible region, but more retruded cheeks compared to females. Ageing in both sexes shared common traits, such as more pronounced roundness of the face (rectangular in males), decreased facial convexity, increased visibility of skin folds and wrinkles connected with the loss of skin elasticity, and soft tissue stretching, especially in the orbital area and lower face; however, male faces exhibited more intense ageing changes. The above-mentioned sexual dimorphic traits tended to diminish in the elderly age category, though overall sexual dimorphism was heightened with age. The static allometric relationships between size and form or shape were similar in both sexes, except that the larger faces of elderly males displayed more intensive ageing changes.

Allometric constraints and the evolution of allometry.

Morphological traits often covary within and among species according to simple power laws referred to as allometry. Such allometric relationships may result from common growth regulation, and this has given rise to the hypothesis that allometric exponents may have low evolvability and constrain trait evolution. We formalize hypotheses for how allometry may constrain morphological trait evolution across taxa, and test these using more than 300 empirical estimates of static (within-species) allometric relations of animal morphological traits. Although we find evidence for evolutionary changes in allometric parameters on million-year, cross-species time scales, there is limited evidence for microevolutionary changes in allometric slopes. Accordingly, we find that static allometries often predict evolutionary allometries on the subspecies level, but less so across species. Although there is a large body of work on allometry in a broad sense that includes all kinds of morphological trait-size relationships, we found relatively little information about the evolution of allometry in the narrow sense of a power relationship. Despite the many claims of microevolutionary changes of static allometries in the literature, hardly any of these apply to narrow-sense allometry, and we argue that the hypothesis of strongly constrained static allometric slopes remains viable.