Ontogeny Of Sexual Size Dimorphism Research Articles

Complex ontogeny of sexual size dimorphism in a female-larger gecko: Implications of determinate growth for lizard body size and life-history evolution.

Ectothermic vertebrates such as reptiles were assumed to be indeterminate growers, which means that there is no terminal point in time or size for growth in their lifetime. In recent years, evidence for the determinate nature of growth in lizards has accumulated, necessitating a re-examination of models of their ontogeny and evolution of sexual size dimorphism (SSD). In the female-larger gecko Paroedura vazimba, we monitored post-embryonic growth over a period of 15 months. After hatching, females grew faster than males but also reached their final body size, that is, closed growth of their vertebrae, earlier than males. The closure of bone growth in females correlates with the onset of reproductive maturation. We compared this pattern with the previously minutely studied, male-larger species Paroedura picta, where we documented determinate growth as well. We propose a model to explain the evolutionary switches in the direction of SSD in lizards based on bipotential effects of ovarian hormones on growth. In this model, male growth is assumed to require no male-specific growth modifier, such as sex-limited hormonal regulators, while growth is feminized by ovarian hormones in females. Low levels of ovarian hormones can promote bone growth, but high levels associated with maturation of the reproductive organs promote senescence of bone growth plates and thus cessation of bone growth. We suggest that models on growth, life-history and evolution of body size in many lizards should acknowledge their determinate nature of growth.

Ontogeny of sexual size dimorphism revisited: Females grow for a longer time and also faster.

Sex-specific mechanisms of the determination of insect body sizes are insufficiently understood. Here we use the common heath moth, Ematurga atomaria (Lepidoptera: Geometridae) to examine how larval growth trajectories differ between males and females. We monitored the development of 1379 larvae in controlled laboratory conditions. Sexually dimorphic development times during the first four instars were associated with sexual size dimorphism (SSD) in the beginning of the fifth (last) instar, when females were on average 15% heavier than males. Similarly, the duration of the last instar was about 13% longer in females. Further, we specifically focussed on the estimates of differential (instantaneous) growth rates of the larvae based on 24h mass increments of the 2nd, 3rd, 4th and 5th day in the beginning of the last instar. We calculated ‘allometric’ differential growth rates as the per-day increase in cube-root-transformed mass of the larvae. We found that allometric growth rates were slightly but significantly larger in females than in males. As this measure of growth rate (in contrast to the relative growth rate, based on the ratio of masses recorded at consecutive measurements) did not depend on body size, it allows an unambiguous separation of the effects of sex and size. We conclude that in accordance with an emerging general pattern, larger female body size in E. atomaria is achieved primarily by means of a longer growth period. Furthermore, our study shows that the differential growth rate can also be sexually dimorphic and contribute to SSD. This contribution, however, is lower than that of the development time by an order of magnitude. In addition to development periods and growth rates, other parameters of the non-linear growth curves of insect larvae also need to be considered in the context of SSD determination. In particular, weight loss prior to pupation was shown to be considerably larger in females than in males.

Hidden complexity in the ontogeny of sexual size dimorphism in male-larger beetles

Sexual size dimorphism (SSD) is widespread among animals, but its developmental mechanisms are not fully undestood. We investigated the proximate causes of SSD in three male-larger and one monomorphic scarab beetles using detailed monitoring of growth in individual instars. Apart from the finding that SSD in all three male-larger species started to develop already in the first larval instar, we generally found a high variability in SSD formation among the species as well as among instars. Overall, sexual differences in developmental time, average growth rate, as well as in the shape of the growth trajectory seem to be the mechanisms responsible for SSD ontogeny in scarab beetles. In the third instar, when the larvae attain most of their mass, the males had a similar or even lower instantaneous growth rate than females and SSD largely developed as a consequence of a longer period of rapid growth in males even in cases when the sexes did not differ in the total duration of this instar. Our results demonstrate that a detailed approach, examining not only the average growth rate and developmental time, but also the shape of the growth trajectory, is necessary to elucidate the complex development of SSD.

Endogenous control of sexual size dimorphism: Gonadal androgens have neither direct nor indirect effect on male growth in a Madagascar ground gecko (Paroedura picta)

Changes in the effect of gonadal androgens on male growth are considered as a possible mechanism allowing shifts in magnitude and even direction of sexual size dimorphism in vertebrates, particularly squamate reptiles. Positive effects of gonadal androgens on male growth were found in several male-larger species of lizards. Contrastingly, we document that in the male-larger Madagascar ground gecko (Paroedura picta) gonadal androgens do not affect male growth under constant thermal conditions. However, the absence of a thermal gradient might prevent the potential indirect effect of gonadal androgens on growth via the influence of circulating hormones on an individual’s thermoregulation and hence metabolic rate. In order to study this, we monitored the growth and body temperature of socially isolated sham-operated and castrated males of the same species in a thermal gradient. We also compared the oxygen consumption and activity between the treatment groups in the open field to test the effect of gonadal hormones on these traits potentially affecting growth. Even under a thermal gradient we found no effect of gonadal androgens on growth rate or final body dimensions. Castration also did not significantly affect oxygen consumption or activity in the open field test. Together with our previous findings, we can exclude both the direct effect of male gonadal androgens on the ontogeny of sexual size dimorphism via the influence on the growth axis, and the indirect influence of gonadal androgens acting on the ontogeny of SSD through the effect on thermoregulation, metabolic rate and activity.

The ontogeny of sexual size dimorphism of a moth: when do males and females grow apart?

Sexual dimorphism in body size (sexual size dimorphism) is common in many species. The sources of selection that generate the independent evolution of adult male and female size have been investigated extensively by evolutionary biologists, but how and when females and males grow apart during ontogeny is poorly understood. Here we use the hawkmoth, Manduca sexta, to examine when sexual size dimorphism arises by measuring body mass every day during development. We further investigated whether environmental variables influence the ontogeny of sexual size dimorphism by raising moths on three different diet qualities (poor, medium and high). We found that size dimorphism arose during early larval development on the highest quality food treatment but it arose late in larval development when raised on the medium quality food. This female-biased dimorphism (females larger) increased substantially from the pupal-to-adult stage in both treatments, a pattern that appears to be common in Lepidopterans. Although dimorphism appeared in a few stages when individuals were raised on the poorest quality diet, it did not persist such that male and female adults were the same size. This demonstrates that the environmental conditions that insects are raised in can affect the growth trajectories of males and females differently and thus when dimorphism arises or disappears during development. We conclude that the development of sexual size dimorphism in M. sexta occurs during larval development and continues to accumulate during the pupal/adult stages, and that environmental variables such as diet quality can influence patterns of dimorphism in adults.

Ontogeny of sexual size dimorphism and environmental quality in Guatemalan children

Human growth data from Guatemalan school children were analyzed to test the hypothesis that the degree of sexual size dimorphism (SSD) in height is reduced for people living under more adverse environmental quality. The sample consists of 2,560 girls and 3,262 boys, 6-16.99 years of age, from the two major Guatemalan ethnic groups, Maya of very low socioeconomic status (SES) and Ladino of high, middle, and low SES. SES was estimated by questionnaire and ethnographic observation. All data are from the Longitudinal Study of Child Development of the Universidad del Valle de Guatemala. Significance of SSD was tested within each whole year age category (e.g., 6.0-6.9 years) by SES for Ladinos and Maya. Ethnic groups were then compared for each age category to determine whether the SSD values were significantly different between groups. Statistically significant height SSD was found for 10 of the 11 age categories for the high SES Ladinos, 8 of the 11 age categories for middle SES Ladinos, 3 of the 11 low SES Ladino age categories, and 0 of the 11 very low SES Maya age categories. For all SES and ethnic groups SSD tended to decrease between 6 and 11 years of age and then increase after age 12 years. A poor quality environment for growth and development, as estimated by SES, was found to reduce or eliminate statistically significant SSD. Patterns of biological maturation before and after puberty also seem to contribute to age changes in SSD.

Sexual Differences in Post-Hatching Saunders's Gulls: Size, Locomotor Activity, and Foraging Skill

Various selection pressures induce the degree and direction of sexual size dimorphism in animals. Selection favors either larger males for contests over mates or resources, or smaller males are favored for maneuverability; whereas larger females are favored for higher fecundity, or smaller females for earlier maturation for reproduction. In the genus of Larus (seagulls), adult males are generally known to be larger in size than adult females. However, the ontogeny of sexual size dimorphism is not well understood, compared to that in adults. The present study investigates the ontogeny of sexual size dimorphism in Saunders's gulls (Larus saundersi) in captivity. We artificially incubated fresh eggs collected in Incheon, South Korea, and measured body size, locomotor activity, and foraging skill in post-hatching chicks in captivity. Our results indicated that the sexual differences in size and locomotor activity occurred with the post-hatching development. Also, larger males exhibited greater foraging skills for food acquisition than smaller females at 200 days of age. Future studies should assess how the adaptive significance of the sexual size dimorphism in juveniles is linked with sexual divergence in survival rates, intrasexual contests, or parental effort in sexes.

Ontogeny of pronounced female-biased sexual size dimorphism in the Malaysian cat gecko (Aeluroscalabotes felinus: Squamata: Eublepharidae): A test of the role of testosterone in growth regulation

Species differences in the effect of male gonadal androgens on male growth are considered a possible mechanism allowing shifts in magnitude and even direction of sexual size dimorphism (SSD) in squamate reptiles. According to the bipotential growth regulation hypothesis, the androgen testosterone (T) enhances male growth in species with male-biased SSD and conversely inhibits male growth in males of female-larger species. In the present study, we describe the ontogeny of the pronounced female-biased SSD and report the effect of T on growth via hormonal manipulations in males and females of the Malaysian cat gecko (Aeluroscalabotes felinus). In accord with the predictions of the bipotential growth regulation hypothesis, growth was inhibited by replacement of T in castrated males. Additionally, exogenous T inhibited growth of females to male-typical levels. Nevertheless, male castration alone did not significantly affect growth, contrary to the prediction of the bipotential growth regulation hypothesis, which contradicts the generality of this hypothesis. Application of exogenous T to females can interfere with normal ovarian function. Therefore, although not directly tested in this study, we suggest that ovarian effects on the ontogeny of SSD in A. felinus are consistent with our results. The development of SSD is a function of differential growth between the sexes, and potential sex-specific growth regulation in both males and females should be taken into account as possible proximate mechanisms responsible for SSD.

Growth in Skull Length and Width of the Arctic Wolf: Comparison of Models and Ontogeny of Sexual Size Dimorphism

We compared four classical nonlinear growth curves (Gompertz, Logistic, Richards, and von Bertalanffy) in modeling observed skull condylobasal length and zygomatic width as a function of age in wild arctic wolves (Canis lupus arctos). We analyzed gender-specific growth patterns and the ontogeny of sexual size dimorphism in this species as revealed by the best model from these alternatives. For both genders and skull size measurements, the size-at-age data provided the best support for the von Bertalanffy model because of higher fitting degrees, lower root mean squared standard deviation of data points about the fitted growth curve, Akaike weight of 37.4% or higher, and fewer parameters derived directly from metabolic laws. Male asymptotic condylobasal length was 3.2% longer, and zygomatic width 4.1% wider, than in females. Sexual size dimorphism in this species develops in part because males grow faster, which might benefit them in terms of reproductive success and the capture and killing of large ungulate prey.

Body length and mass growth of the brown bear (Ursus arctos) in northern Canada: model selection based on information theory and ontogeny of sexual size dimorphism

We compared four nonlinear growth functions in modeling body length and mass size-at-age data for the brown bear ( Ursus arctos L., 1758) in northern Canada of wide-ranging body sizes and ages. Then, we analyzed the sex differences in patterns of growth and ontogeny of sexual dimorphism in this species revealed by the best model from these alternatives. The von Bertalanffy function proved to be the most parsimonious model because it was easy to fit, with higher fitting degrees, lower root mean squared standard deviation of data points about fitted growth curve, larger Akaike weight, and fewer parameters derived directly from metabolic laws that accurately estimated the observed body length and mass growth profiles. Our growth models indicated an association between sexual growth divergence and the onset of reproduction in females, together with more rapid and prolonged male growth. These findings suggest that sexual size dimorphism develops in part by constraints on female growth from high energetic costs of reproduction. In contrast, males do not experience a comparable energetic trade-off after reaching sexual maturity and apparently allocate available energetic resources to growing faster and longer to produce larger body size, which benefits more competitive males in terms of increased reproductive success.

Ontogeny of Sexual Size Dimorphism in Monitor Lizards: Males Grow for a Longer Period, but not at a Faster Rate

Monitor lizards belong to the largest and the most sexually dimorphic lizards in terms of size, making this group an ideal model for studies analyzing ontogenetic causes of sexual dimorphism. Understanding of these ontogenetic factors is essential to the current discussion concerning patterns of sexual dimorphism in animals. We examined the ontogenetic trajectories of body weight and snout-vent length to analyze the emergence of sexual size dimorphism. Experimental animals were 22 males and 13 females of mangrove-dwelling monitors (Varanus indicus) hatched at the Prague Zoo. They were regularly weighed and measured up to the age of 33-40 months, and subsequently sexed by ultrasonographic imaging. The logistic growth equation was used to describe and analyze the observed growth patterns. Our results confirm considerable sexual size dimorphism in the mangrove monitor. The mean asymptotic body weight of males was nearly three times higher than that of females. As the body size of male and female hatchlings is almost equal, and the growth rate parameter (K) of the logistic growth equation as well as the absolute growth rate up to the age of 12 months do not differ between the sexes, size differences between fully grown males and females should be attributed to timing of the postnatal growth. Males continue to grow several months after they reach the age when the growth of females is already reduced. Therefore, the sexual size dimorphism emerges and sharply increases at this period.

Macroevolutionary pattern of sexual size dimorphism in geckos corresponds to intraspecific temperature‐induced variation

Many animal lineages exhibit allometry in sexual size dimorphism (SSD), known as 'Rensch's rule'. When applied to the interspecific level, this rule states that males are more evolutionary plastic in body size than females and that male-biased SSD increases with body size. One of the explanations for the occurrence of Rensch's rule is the differential-plasticity hypothesis assuming that higher evolutionary plasticity in males is a consequence of larger sensitivity of male growth to environmental cues. We have confirmed the pattern consistent with Rensch's rule among species of the gecko genus Paroedura and followed the ontogeny of SSD at three constant temperatures in a male-larger species (Paroedura picta). In this species, males exhibited larger temperature-induced phenotypic plasticity in final body size than females, and body size and SSD correlated across temperatures. This result supports the differential-plasticity hypothesis and points to the role phenotypic plasticity plays in generating of evolutionary novelties.

Inbreeding, outbreeding, infant growth, and size dimorphism in captive Indian rhinoceros (Rhinoceros unicornis)

Effects of inbreeding and outbreeding on gestation period, birth mass, infant mortality, and growth, as well as the ontogeny of sexual size dimorphism, were analyzed in captive Indian rhinoceros (Rhinoceros unicornis L., 1758) using studbook data. Neither gestation period nor birth mass were affected by inbreeding. However, inbred calves grew slower and had a lower mortality rate than non-inbred ones. It is suggested that the severe bottleneck experienced in the early twentieth century by the Kaziranga population, from which most captive-born Indian rhinoceroses descend, resulted in strong inbreeding with consequent purging of recessive lethal alleles. Outbred individuals (offspring of matings between individuals from the Kaziranga and the Chitwan populations) had a higher infant mortality rate, suggesting that the two populations are genetically partially incompatible. Among captive individuals, adult males were found to be heavier (2300 kg) and larger (shoulder height = 172 cm) than females (1800 kg, 160 cm). There were, however, no sex differences in gestation period, birth mass, or infant growth. This suggests that sexual dimorphism in adults is the result of a longer growth period in males rather than a difference in growth rate between the sexes.

Gender and viability selection on morphology in fledgling pied flycatchers.

Until recently, analyses of gender-dependent differences in viability selection and the ontogeny of sexual size dimorphism have been plagued by difficulties in determining the sex of nestling birds on the basis of morphology. Recently, this problem was overcome using molecular sex identification to report for the first time body-size-mediated antagonistic selection on the viability of male and female collared flycatchers. We used molecular sex identification to analyse natural selection on fledgling viability, sexual size dimorphism and effects of parasites in relation to gender in a Mediterranean population of the related pied flycatcher Ficedula hypoleuca. There was directional positive selection on fledgling weight but no selection on tarsus length. Fledgling weight was the most important determinant of fledgling survival, with heavier fledglings having increased viability. Although selective trends were of the same sign for both sexes, only among female fledglings were selection differentials and gradients statistically significant. Therefore, similar trends in selection were revealed in analyses of a data set where sex was ignored and in separate analyses using same-sex sibship trait means. Mite nest ectoparasites negatively affected fledgling weight, and the effects were stronger in female than male fledglings. There was no effect of parasitism on the tarsus length in males, as previously reported in retrospective analyses performed without knowledge of sex until recruitment. Overall, selection on fledgling viability on the basis of morphological traits and hatching date was not confounded by an individual's gender.

Growth and ontogeny of sexual size dimorphism in the mandrill (Mandrillus sphinx).

We present body mass (N = 419) and crown-rump length (CRL, N = 210) measurements from 38 male and 49 female mandrills born into a semifree-ranging colony in order to describe growth from birth to adulthood, and to investigate maternal influences upon growth. Adult male mandrills are 3.4 times the body mass, and 1.3 times the CRL, of adult females. Body mass dimorphism arises from a combination of sex differences in length of the growth period (females attain adult body mass at 7 years, males at 10 years) and growth rate. Both sexes undergo a subadult growth spurt in body mass, and this is much more dramatic in males (peak velocity 551 g/months +/- 89 SEM at 84-96 months). CRL dimorphism arises from bimaturism (females attain adult CRL at 6 years, males after 10 years), and neither sex shows a particular subadult growth spurt in CRL. Sexual size dimorphism thus represents important time and metabolic costs to males, who mature physically approximately 3-4 years after females. Considerable interindividual variation occurs in the size-for-age of both sexes, which is related to maternal variables. Older mothers have heavier offspring than do younger mothers, and higher-ranking mothers have heavier offspring than do lower ranking mothers. Mass advantages conferred upon offspring during lactation by older and higher-ranking mothers tend to persist postweaning in both sexes. Thus maternal factors affect reproductive success in both sexes, influencing the age at which offspring mature and begin their reproductive career.

Ontogeny of Sexual Size Dimorphism in the Tropical Garden Lizard, Calotes versicolor (Daud.)

Ontogeny of Sexual Size Dimorphism in the Tropical Garden Lizard, Calotes versicolor (Daud.)

THE EVOLUTION OF SEXUAL SIZE DIMORPHISM IN THE HOUSE FINCH. III. DEVELOPMENTAL BASIS

Sexual size dimorphism of adults proximately results from a combination of sexually dimorphic growth patterns and selection on growing individuals. Yet, most studies of the evolution of dimorphism have focused on correlates of only adult morphologies. Here we examined the ontogeny of sexual size dimorphism in an isolated population of the house finch (Carpodacus mexicanus). Sexes differed in growth rates and growth duration; in most traits, females grew faster than males, but males grew for a longer period. Sexual dimorphism in bill traits (bill length, width, depth) and in body traits (wing, tarsus, and tail length; mass) developed during different periods of ontogeny. Growth of bill traits was most different between sexes during the juvenile period (after leaving the nest), whereas growth of body traits was most sexually dimorphic during the first few days after hatching. Postgrowth selection on juveniles strongly influenced sexual dimorphism in all traits; in some traits, this selection canceled or reversed dimorphism patterns produced by growth differences between sexes. The net result was that adult sexual dimorphism, to a large degree, was an outcome of selection for survival during juvenile stages. We suggest that previously documented fast and extensive divergence of house finch populations in sexual size dimorphism may be partially produced by distinct environmental conditions during growth in these populations.Corresponding Editor: T. Mousseau

The evolution of sexual size dimorphism in the house finch. III. Developmental basis.

Sexual size dimorphism of adults proximately results from a combination of sexually dimorphic growth patterns and selection on growing individuals. Yet, most studies of the evolution of dimorphism have focused on correlates of only adult morphologies. Here we examined the ontogeny of sexual size dimorphism in an isolated population of the house finch (Carpodacus mexicanus). Sexes differed in growth rates and growth duration; in most traits, females grew faster than males, but males grew for a longer period. Sexual dimorphism in bill traits (bill length, width, depth) and in body traits (wing, tarsus, and tail length; mass) developed during different periods of ontogeny. Growth of bill traits was most different between sexes during the juvenile period (after leaving the nest), whereas growth of body traits was most sexually dimorphic during the first few days after hatching. Postgrowth selection on juveniles strongly influenced sexual dimorphism in all traits; in some traits, this selection canceled or reversed dimorphism patterns produced by growth differences between sexes. The net result was that adult sexual dimorphism, to a large degree, was an outcome of selection for survival during juvenile stages. We suggest that previously documented fast and extensive divergence of house finch populations in sexual size dimorphism may be partially produced by distinct environmental conditions during growth in these populations.

Parasites and the ontogeny of sexual size dimorphism in a passerine bird

Explanations of sexual size dimorphism in animals have generally relied on theoretical predictions of sexual selection, niche differentiation, and sex ratio theories, whereas proximate influences on size dimorphisms are undescribed in wild populations. We describe the differential effects of mite nest ectoparasites on the growth of the tarsus, a measure of skeletal size, in nestling pied flycatchers, Ficedula hypoleuca, depending on sex. The detrimental effects of mites were suffered by males to a higher degree than females. It is proposed that parasites may interact with both host hormones and the host immune system to cause sexual size dimorphisms in young animals.

Socioecology and the ontogeny of sexual size dimorphism in anthropoid primates

This study examines statistical correlations between socioecological variables (including measures of group composition, intermale competition, and habitat preference) and the ontogeny of body size sexual dimorphism in anthropoid primates. A regression-based multivariate measure of dimorphism in body weight ontogeny is derived from a sample of 37 species. Quantitative estimates of covariation between socioecological variables and this multivariate measure are evaluated. Statistically significant covariation between the ontogeny of dimorphism and socioecological variables, with the possible exception of habitat preference, is observed. Sex differences in ontogeny are lacking in species that exhibit low levels of intermale competition and are classifiable as species with monogamous/polyandrous mating systems. Among dimorphic species, two modes of dimorphic growth are apparent, which seem to be related to different kinds of group compositions. Multimale/multifemale species tend to become dimorphic through bimaturism (sex differences in duration of growth) with minimal sex differences in growth rate. Single-male/multifemale species tend to attain dimorphism through differences in rate of growth, often with limited bimaturism. Measures of intermale competition may also covary with these modes of dimorphic growth, but the relations among these variables are sometimes ambiguous. Correlations between dimorphic growth and behavioral variables may reflect alternative life history strategies in primates. Specifically, the ways in which risks faced by subadult males are distributed and the relations of these risks to growth rates seem to influence the evolution of size ontogenies. The absence of dimorphic ontogeny in some species can be tied to similar distributions of risk in each sex. In taxa that become dimorphic primarily through rate differences in growth, the lifetime distribution of risks for males may change rapidly. In contrast, males may face a pattern of uniformly changing or stable risk in species that become dimorphic through bimaturism. Finally, much variation recorded by this study remains unexplained, providing additional evidence of the need to specially examine female ontogeny before primate body size dimorphism can be satisfactorily explained.