Disentangling the Size and Shape Components of Sexual Dimorphism

Evolutionary Biology - Many organisms are sexually dimorphic, reflecting sex-specific selection pressures. But although sexual dimorphism may consist of different variables from size to shape and...     

Geographical Variation in Body Size and Sexual Size Dimorphism in an Australian Lizard,Boulenger's Skink (Morethia boulengeri)

Ecogeographical rules help explain spatial and temporal patterns in intraspecific body size. However, many of these rules, when applied to ectothermic organisms such as reptiles, are controversial and require further investigation. To explore factors that influence body size in reptiles, we performed a heuristic study to examine body size variation in an Australian lizard, Boulenger''s Skink Morethia boulengeri from agricultural landscapes in southern New South Wales, south-eastern Australia. We collected tissue and morphological data on 337 adult lizards across a broad elevation and climate gradient. We used a model-selection procedure to determine if environmental or ecological variables best explained body size variation. We explored the relationship between morphology and phylogenetic structure before modeling candidate variables from four broad domains: (1) geography (latitude, longitude and elevation), (2) climate (temperature and rainfall), (3) habitat (vegetation type, number of logs and ground cover attributes), and (4) management (land use and grazing history). Broad phylogenetic structure was evident, but on a scale larger than our study area. Lizards were sexually dimorphic, whereby females had longer snout-vent length than males, providing support for the fecundity selection hypothesis. Body size variation in M. boulengeri was correlated with temperature and rainfall, a pattern consistent with larger individuals occupying cooler and more productive parts of the landscape. Climate change forecasts, which predict warmer temperature and increased aridity, may result in reduced lizard biomass and decoupling of trophic interactions with potential implications for community organization and ecosystem function.     

四眼斑水龟个体大小和体形的两性异形

研究龟鳖的两性异形对理解形态适应具有重要意义。通过测量41只(21♀,20♂)成体四眼斑水龟(Sacalia quadriocellata)的20个形态特征指标,研究四眼斑水龟个体大小和体形的两性异形。结果表明:除头长、头宽、尾长和尾长肛前段长外,四眼斑水龟其他的形态特征均与背甲长呈正相关。雌性的背甲长、腹甲长、腹甲中线长、腹甲曲线长显著大于雄性;雄性的头长、头宽、后肢长、尾长和尾长肛前段长显著大于雌性;雌雄两性的体重、体周长、前肢长、腹甲宽、肛盾切口长、肛盾切口宽以及除背甲长外的所有背甲形态特征指标均无显著差异。研究结果表明,四眼斑水龟存在个体大小和体形两性异形。     

Sexual Size Dimorphism,Canine Dimorphism,and Male-Male Competition in Primates

Sexual size dimorphism is generally associated with sexual selection via agonistic male competition in nonhuman primates. These primate models play an important role in understanding the origins and evolution of human behavior. Human size dimorphism is often hypothesized to be associated with high rates of male violence and polygyny. This raises the question of whether human dimorphism and patterns of male violence are inherited from a common ancestor with chimpanzees or are uniquely derived. Here I review patterns of, and causal models for, dimorphism in humans and other primates. While dimorphism in primates is associated with agonistic male mate competition, a variety of factors can affect male and female size, and thereby dimorphism. The causes of human sexual size dimorphism are uncertain, and could involve several non-mutually-exclusive mechanisms, such as mate competition, resource competition, intergroup violence, and female choice. A phylogenetic reconstruction of the evolution of dimorphism, including fossil hominins, indicates that the modern human condition is derived. This suggests that at least some behavioral similarities with Pan associated with dimorphism may have arisen independently, and not directly from a common ancestor.     

Becoming Different But Staying Alike: Patterns of Sexual Size and Shape Dimorphism in Bills of Hummingbirds

Hummingbirds are known for their distinctive patterns of sexual dimorphism, with many species exhibiting sex-related differences in various ecologically-relevant traits, including sex-specific differences in bill shape. It is generally assumed that such patterns are consistent across all hummingbird lineages, yet many taxa remain understudied. In this study we examined patterns of sexual size and sexual shape dimorphism in bills of 32 of 35 species in the monophyletic Mellisugini lineage. We also compared patterns of bill size dimorphism in this group to other hummingbird lineages, using data from 219 hummingbird species. Overall, the presence and degree of sexual size dimorphism was similar across all hummingbird lineages, with the majority of Mellisugini species displaying female-biased sexual size dimorphism, patterns that remain unchanged when analyzed in a phylogenetic context. Surprisingly however, we found that sexual dimorphism in bill shape was nearly absent in the Mellisugini clade, with only 3 of the 32 species examined displaying bill shape dimorphism. Based on observations in other hummingbird lineages, the lack of sexual shape dimorphism in Mellisugini is particularly unusual. We hypothesize that the patterns of sexual size dimorphism observed here may be the consequence of differential selective forces that result from competition for ecological resources. We further propose that an influential mechanism underlying shape dimorphism is competition and niche segregation. Taken together, the evolutionary changes in patterns of sexual shape dimorphism observed in Mellisugini suggest that the evolutionary trends of sexual dimorphism in the Trochilidae are far more dynamic than was previously believed.     

Sexual Size Dimorphism in Anurans: Ontogenetic Determination Revealed by an Across-Species Comparison

Ever since Darwin, why and how sexual size dimorphism (SSD) arises among the animal kingdom has puzzled evolutionary biologists. While comparative analyses focus on ultimate causes of this phenomenon, few attempts have been made to quantify its ontogenetic basis. Here we deal with the latter issue using the skeletochronology-based demographic data gathered from the literature for anurans, a group of indeterminately growing vertebrates typically exhibit female-biased SSD. Both non- and phylogenetically corrected analyses showed (1) SSD was correlated positively with the sex difference in adult mean age but negatively with the corresponding difference in annual growth rate, (2) the sex difference in adult mean age tended to be negatively correlated with that in growth rate, and (3) the sex difference in adult mean age was positively correlated with that in age at maturity. We conclude that in anuran lineages, the degree of SSD bias towards females is mediated by sexual bimaturation: females mature later than males, and thus live longer and attain larger despite growing slower. Stronger fecundity selection benefits to females, despite incurring growth cost, in combination with the benefits to males from increased reproductive opportunities resulting from earlier maturity, should be the primary evolutionary drivers of the typically female-biased SSD.     

Sexual Size Dimorphism and Body Condition in the Australasian Gannet

Sexual size dimorphism is widespread throughout seabird taxa and several drivers leading to its evolution have been hypothesised. While the Australasian Gannet (Morus serrator) has previously been considered nominally monomorphic, recent studies have documented sexual segregation in diet and foraging areas, traits often associated with size dimorphism. The present study investigated the sex differences in body mass and structural size of this species at two colonies (Pope’s Eye, PE; Point Danger, PD) in northern Bass Strait, south-eastern Australia. Females were found to be 3.1% and 7.3% heavier (2.74 ± 0.03, n = 92; 2.67 ± 0.03 kg, n = 43) than males (2.66 ± 0.03, n = 92; 2.48 ± 0.03 kg, n = 43) at PE and PD, respectively. Females were also larger in wing ulna length (0.8% both colonies) but smaller in bill depth (PE: 2.2%; PD: 1.7%) than males. Despite this dimorphism, a discriminant function provided only mild accuracy in determining sex. A similar degree of dimorphism was also found within breeding pairs, however assortative mating was not apparent at either colony (R² < 0.04). Using hydrogen isotope dilution, a body condition index was developed from morphometrics to estimate total body fat (TBF) stores, where TBF(%) = 24.43+1.94*(body mass/wing ulna length) – 0.58*tarsus length (r² = 0.84, n = 15). This index was used to estimate body composition in all sampled individuals. There was no significant difference in TBF(%) between the sexes for any stage of breeding or in any year of the study at either colony suggesting that, despite a greater body mass, females were not in a better condition than males. While the driving mechanism for sexual dimorphism in this species is currently unknown, studies of other Sulids indicate segregation in foraging behaviour, habitat and diet may be a contributing factor.     

Absence of Mate Choice and Postcopulatory Benefits in a Species with Extreme Sexual Size Dimorphism

Most hypotheses related to the evolution of female‐biased extreme sexual size dimorphism (SSD) attribute the differences in the size of each sex to selection for reproduction, either through selection for increased female fecundity or selection for male increased mobility and faster development. Very few studies, however, have tested for direct fitness benefits associated with the latter – small male size. Mecaphesa celer is a crab spider with extreme SSD, whose males are less than half the size of females and often weigh 10 times less. Here, we test the hypotheses that larger size in females and smaller size in males are sexually selected through differential pre‐ and postcopulatory reproductive benefits. To do so, we tested the following predictions: matings between small males and large females are more likely to occur due to mate choice; females mated to small males are less likely to accept second copulation attempts; and matings between small males and large females will result in larger clutches of longer‐lived offspring. Following staged mating trials in the laboratory, we found no support for any of our predictions, suggesting that SSD in M. celer may not be driven by pre‐ or post‐reproductive fitness benefits to small males.     

Sex Ratio and Sexual Size Dimorphism in a Toad-headed Lizard,Phrynocephalus guinanensis

Phrynocephalus guinanensis has sexual dimorphism in abdominal coloration, but its ontogenetic development of sexual size dimorphism(SSD) is unknown. Using mark-recapture data during four days each year from August from 2014 to 2016, we investigated the development of sex ratios, SSD, sex-specific survivorship and growth rates in a population of P. guinanensis. Our results indicated that the sex ratio of males to females was 1:2.8. Males had a lower survival rate(6%) than females(14%) across the age range from hatchling to adult, which supported the discovered female-biased sex ratio potentially associated with the low survival rate of males between hatchlings and juveniles. Male-biased SSD in tail length and head width existed in adults rather than in hatchling or juvenile lizards. The growth rates in body dimensions were undistinguishable between the sexes during the age from hatchling to juvenile, but the growth rate in head length from juvenile to adult was significantly larger in males than females. Average growth rate of all morphological measurements from hatchling to juvenile were larger compared with corresponding measurements from juvenile to adult, but only being significant in tail length, head width, abdomen length in females and snout-vent length in males. We provided a case study to strengthen our understanding of the important life history traits on how a viviparous lizard population can survive and develop their morphology in cold climates.     

大山雀身体大小的性二态及其季节变化

动物中普遍存在雌雄个体身体大小的性二态现象。了解近缘种之间身体大小性二态现象的差异,可为深入探讨身体大小性二态现象的潜在驱动机制提供证据。国外对欧亚大山雀(Parus major)的研究发现,其喙长、跗跖长、翅长等6项身体大小指标存在着明显的性二态,且喙长的性二态存在季节间差异。大山雀(P.cinereus)曾被作为欧亚大山雀的一个亚种,其形态和行为与欧亚大山雀存在着诸多相似之处。为探讨大山雀是否也存在身体大小性二态及季节性差异,本研究分析了2018至2020年间在河南董寨国家级自然保护区捕捉的226只(雌性96只和雄性130只)大山雀的喙长、头喙长、跗跖长、翅长、尾长和体长这6项体征指标的两性差异及其季节变化。结果显示,大山雀上述6项身体大小指标均存在不同程度的性二态现象,且雄性个体仅喙长与雌性的差异不显著,其余5项指标均显著大于雌性。此外,身体大小指标的两性差异不随季节显著变化,但两性的跗跖长在秋季均显著短于冬季和繁殖季,尾长在繁殖季均显著长于秋季和冬季。上述结果表明,大山雀身体大小的性二态及其季节性差异与欧亚大山雀并不完全相似。无论其身体大小存在性二态和季节变化的原因,还是其与欧亚大山雀在身体大小性二态模式上的差别,都有待今后进一步研究。     

Variation and Sexual Dimorphism of Body Size in the Plateau Brown Frog along an Altitudinal Gradient

Variation in body size and sexual size dimorphism(SSD) can have important consequences for animal ecology, behavior, population dynamics and the evolution of life-history traits. Organisms are expected to be larger in colder climate(i.e., Bergmann's rule) and SSD varies with body size(i.e., Rensch's rule). However, the underlying mechanisms are still elusive. The plateau brown frog(Rana kukunoris), a medium-sized anuran species with femalebiased SSD, is endemic to the Qinghai-Tibetan Plateau(QTP). From 1797 m(Maoxiang'ping) to 3453 m(Heihe'qiao) in the eastern margin of the QTP, we surveyed 10 populations of R. kukunoris and collected phalanges and snout vent length(SVL) data for 258 adult individuals(199 males versus 59 females). Based on these data, we explored how body size and SSD varying along the altitudinal gradient and examined the corresponding effects of temperature. We found body size to be larger at higher altitude for males but not for females, with likely effects from the temperature on the variation in male body size. Sex differences in growth rates may be the main cause of the variation in SSD. Our results suggested that only males follow the Bergmann's rule and variation in SSD of R. kukunoris do not support the Rensch's rule and its inverse. Therefore, the variations of body size can be different between sexes and the applicability of both Bergmann's rule and Rensch's rule should depend on species and environment where they live.     

灰椋鸟身体大小和内脏器官形态的两性差异

鸟类性二态现象广泛存在,比如身体大小、羽色等,性二态很可能是自然选择和性选择共同作用的结果.为了探索和更好地了解雀形目鸟类身体大小性二态的进化,在2019年繁殖季节早期研究了灰椋鸟(Sturnus cineraceus)野外种群身体大小和内脏器官形态的两性差异.结果表明,除嘴宽外,其他身体特征参数均雄性显著大于雌性,表...     

Assessment of Patterns of Fluctuating Asymmetry and Sexual Dimorphism in Carabid Body Shape

The measurement tool most used to estimate developmental stability (DS) is fluctuating asymmetry (FA), which is a measure of the small random deviations that occur between the left and right sides of bilaterally symmetrical traits. In the Biobío Region of Chile, forest plantations are a widely extended phenomenon, which affect 27% of the surface area of the region and which are dominated by the monoculture of Pinus radiata. This study evaluated the presence of FA in the body shape of two populations of Ceroglossus chilensis (Eschscholtz) in two 13-year-old forest plantations (commercial thinning) using insects collected with interception traps. Since the biotic and abiotic components of forest plantations are subject to continual anthropic modifications that affect almost all ecological processes, including population dynamics, community composition, and material and energy flows, these characteristics are reflected in the DS of individuals. The results showed that there was greater precision using geometric morphometrics to detect the presence of asymmetry in plantations due to shape analysis, as proposed by studies in antennal morphology using traditional measures. It should be noted that the populations were exposed to different environments; the population in the Coast Range is more humid, while the Andes Foothills population is in a drier area with drier soils. In spite of this, there was minimum phenotypic variation detected at the population level, which reflected the different environments and may be associated with patterns of environmental phenotypic plasticity.     

Sexual Strategy and Size Dimorphism in Rattlesnakes: Integrating Proximate and Ultimate Causation

SYNOPSIS. Integrating proximate and ultimate causes and effectssimultaneously in the study of behavior is challenging and complex,but useful. This is equivalent to asking both "How?" (in thesense of proximate mechanisms) and "Why?" (in the sense of ultimateevolutionary payoffs) an organism operates in one way and notanother. Sex differences in rattlesnake (i) size and growthand (ii) mating and reproductive strategies and tactics, providea good theoretical and empirical context in which to attemptsuch integration. We employ interdisciplinary and multidisciplinaryapproaches in our behavioral and physiological work, but wemean something different by "integrative," that amounts to thesimultaneous study of both proximate and ultimate levels ofcausation and explanation. Though not always feasible, thisapproach represents an important goal to work towards becauseit attempts to represent faithfully the complexity inherentin living systems. To this end, we also employ a variety ofmodeling approaches, which entrain intuition, generate new hypotheses,and sharpen inference. Individual-based simulations, for example,offer promise for broad, integrative programs of biologicalresearch.     

The Dilemma of Choosing a Reference Character for Measuring Sexual Size Dimorphism,Sexual Body Component Dimorphism,and Character Scaling: Cryptic Dimorphism and Allometry in the Scorpion Hadrurus arizonensis

Sexual differences in morphology, ranging from subtle to extravagant, occur commonly in many animal species. These differences can encompass overall body size (sexual size dimorphism, SSD) or the size and/or shape of specific body parts (sexual body component dimorphism, SBCD). Interacting forces of natural and sexual selection shape much of the expression of dimorphism we see, though non-adaptive processes may be involved. Differential scaling of individual features can result when selection favors either exaggerated (positive allometry) or reduced (negative allometry) size during growth. Studies of sexual dimorphism and character scaling rely on multivariate models that ideally use an unbiased reference character as an overall measure of body size. We explored several candidate reference characters in a cryptically dimorphic taxon, Hadrurus arizonensis. In this scorpion, essentially every body component among the 16 we examined could be interpreted as dimorphic, but identification of SSD and SBCD depended on which character was used as the reference (prosoma length, prosoma area, total length, principal component 1, or metasoma segment 1 width). Of these characters, discriminant function analysis suggested that metasoma segment 1 width was the most appropriate. The pattern of dimorphism in H. arizonensis mirrored that seen in other more obviously dimorphic scorpions, with static allometry trending towards isometry in most characters. Our findings are consistent with the conclusions of others that fecundity selection likely favors a larger prosoma in female scorpions, whereas sexual selection may favor other body parts being larger in males, especially the metasoma, pectines, and possibly the chela. For this scorpion and probably most other organisms, the choice of reference character profoundly affects interpretations of SSD, SBCD, and allometry. Thus, researchers need to broaden their consideration of an appropriate reference and exercise caution in interpreting findings. We highly recommend use of discriminant function analysis to identify the least-biased reference character.     

Maternal Size and Age Shape Offspring Size in a Live-Bearing Fish,Xiphophorus birchmanni

Many studies of offspring size focus on differences in maternal investment that arise from ecological factors such as predation or competition. Classic theory predicts that these ecological factors will select for an optimal offspring size, and therefore that variation in a given environment will be minimized. Yet recent evidence suggests maternal traits such as size or age could also drive meaningful variation in offspring size. The generality of this pattern is unclear, as some studies suggest that it may represent non-adaptive variation or be an artifact of temporal or spatial differences in maternal environments. To clarify this pattern, we asked how maternal size, age and condition are related to each other in several populations of the swordtail Xiphophorus birchmanni. We then determined how these traits are related to offspring size, and whether they could resolve unexplained intra-population variation in this trait. We found that female size, age, and condition are correlated within populations; at some of these sites, older, larger females produce larger offspring than do younger females. The pattern was robust to differences among most, but not all, sites. Our results document a pattern that is consistent with recent theory predicting adaptive age- and size-dependence in maternal investment. Further work is needed to rule out non-adaptive explanations for this variation. Our results suggest that female size and age could play an under-appreciated role in population growth and evolution.     

Differential Migration by Sex in the Great Bustard: Possible Consequences of an Extreme Sexual Size Dimorphism

We explored migration patterns in Great bustards ( Otis tarda ), a species that shows strong sexual selection and the most extreme sexual size dimorphism among birds. The aim was to explain differential migration, examining whether Great bustards fulfil the main predictions of bird migration theory hypotheses and sexual segregation theory hypotheses. We radio-tracked the seasonal movements of 65 males and 68 females in central Spain. We found four main sexual differences. First, the proportion of migratory males was higher than that of migratory females (86% vs. 51%). Second, males abandoned the leks immediately after the mating season (late May to early Jun.), whereas females remained there for another 3–7 mo. Third, 54% of the migratory males used two different post-breeding areas, the first located northwards at 82 km from the breeding sites in summer, and the second southwards at 50 km in autumn–winter. Migratory females used only one area in autumn–winter which coincided geographically with that of males. And fourth, males returned to the breeding areas earlier (between Sep. and Mar.) than females (between Jan. and Apr.). These results show that the Great bustard is a differential migrant by sex in central Spain and support the weather sensitivity hypothesis (males were less tolerant to summer heat) and the specialization hypothesis (exclusive maternal care of the brood by females). Sexual differences in migratory behaviour are probably ultimately determined by the strong sexual selection in this species.     

Implications of Male and Female Contributions to Sexual Size Dimorphism for Inferring Behavior in the Hominin Fossil Record

Sexual dimorphism is commonly used to directly infer or support reconstructions of social behavior in early hominins. This is often done by comparing the magnitude of sexual size dimorphism to that seen in extant primates and extrapolating a likely social behavior. Such comparisons are of limited value, though, allowing only the inference of strong male–male competition when dimorphism is strong. Recent studies have begun to focus on the selective factors that impact female body size, and thereby size dimorphism. Considerations of changes in male and female size in the fossil record potentially allow insight into the meaning of changes in sexual dimorphism through time. To illustrate, I compare estimates of body mass dimorphism for four hominin taxa to assess changes in male and female size. Assuming that early Homo represents a single taxon, sexual size dimorphism increased in early Homo through an increase in male size, but was subsequently reduced through an increase in female size in Homo erectus. This would imply a significant increase in sexual selection acting on males in early Homo. An increase in female size with a loss of dimorphism in Homo erectus would imply a simultaneous shift in female optimal body size through selection for increased female fecundity, and/or an increase in female resource abundance, coupled with a shift in selection acting on male size. Although none of these inferences are certain, the exercise illustrates the potential for considering how dimorphism changes through time, rather than simply focusing on the magnitude of size dimorphism in isolation.     

宁波滑蜥两性异形和雌性繁殖

蜥蜴的雌性繁殖特征对理解两性异形的进化原因起着重要作用。于2011年4月在安徽滁州采集宁波滑蜥(Scincella modesta),定量研究该种形态特征的两性异形和雌性繁殖特征,检验成体形态特征两性异形与雌性繁殖的相关性。研究共采集43条(17♀♀,26♂♂)宁波滑蜥,雄性和雌性个体的最大体长分别为47.4 mm和46.6 mm。雌雄两性在体长和头宽上没有差异,而在腹长和头长上差异显著,雄性有较大的头长,雌性有较大的腹长。宁波滑蜥年产单窝卵。窝卵数和窝卵重与雌体体长及腹长呈正相关,卵重与雌体体长无相关性。窝卵数及卵重的变异系数分别为0.20和0.12。卵长径与窝卵数呈负相关,而卵短径与窝卵数无关。雌体主要通过增加窝卵数来增加繁殖输出。这些结果表明,宁波滑蜥是雌雄个体大小同形的两性异形模式,性选择使得雄性有着较大的头长,以具有较高的交配成功率,生育力选择使得雌性有着较大的腹长,以具有较大的生育力和繁殖输出。