Intrasexual competition and body weight dimorphism in anthropoid primates

Body weight dimorphism in anthropoid primates has been thought to be a consequence of sexual selection resulting from male-male competition for access to mates. However, while monogamous anthropoids show low degrees of weight dimorphism, as predicted by the sexual selection hypothesis, polygynous anthropoids show high variation in weight dimorphism that is not associated with measures of mating system or sex ratio. This observation has led many to debate the role of other factors such as dietary constraints, predation pressure, substrate constraints, allometric effects, and phylogeny in the evolution of anthropoid weight dimorphism. Here, we re-evaluate variation in adult body weight dimorphism in anthropoids, testing the sexual selection hypothesis using categorical estimates of the degree of male-male intrasexual competition (“competition levels”). We also test the hypotheses that interspecific variation in body weight dimorphism is associated with female body weight and categorical estimates of diet, substrate use, and phylogeny. Weight dimorphism is strongly associated with competition levels, corroborating the sexual selection hypothesis. Weight dimorphism is positively correlated with increasing female body weight, but evidence suggests that the correlation reflects an interaction between overall size and behavior. Arboreal species are, on average, less dimorphic than terrestrial species, while more frugivorous species tend to be more dimorphic than folivorous or insectivorous species. Several alternative hypotheses can explain these latter results. Weight dimorphism is correlated with taxonomy, but so too are competition levels. We suggest that most taxonomic correlations of weight dimorphism represent “phylogenetic niche conservatism”; however, colobines show consistently low degrees of weight dimorphism for reasons that are not clear. Am J Phys Anthropol 103:37–68, 1997. © 1997 Wiley-Liss, Inc.     

Ontogenetic bases of canine dimorphism in anthropoid primates

This study tests hypotheses regarding the ontogeny of canine tooth size dimorphism in five anthropoid primate species (Saguinus fuscicollis, Macaca mulatta, Cercocebus atys, Papio hamadryas, and Mandrillus sphinx). Canine measurements and chronological age data are analyzed to determine if bimaturism, a sex difference in the age at which eruption ceases, accounts for canine tooth sexual dimorphism. Canine height measurements are evaluated through a variety of regression techniques. Results show a lack of sexual dimorphism in Saguinus. While size dimorphism is absent in the deciduous teeth of all species analyzed, the adult teeth in cercopithecines become increasingly dimorphic through ontogeny. Female adult tooth eruption regularly precedes male tooth eruption, and regression-based eruption trajectories for both sexes intersect at about the age at which the female tooth reaches adult size. Males erupt the tooth later and more rapidly than females. Males also reach a larger adult size than females by erupting the tooth for much longer periods of time. Bimaturism is primary in the production of dimorphism, but rates of eruption show modest variation. These results point to the scheduling of sexual selection through intermale competition as a primary factor determining male eruption timing, rates of eruption, and adult size. Life history factors may play a role in determining the relations between the scheduling of intrasexual competition and canine eruption. Female contributions to sexual dimorphism are apparent in these species, suggesting that similar levels of dimorphism can be attained through diverse ontogenetic pathways.     

Intrasexual competition and canine dimorphism in anthropoid primates.

A number of factors, including sexual selection, body weight, body-weight dimorphism, predation, diet, and phylogenetic inertia have been proposed as influences on the evolution of canine dimorphism in anthropoid primates. Although these factors are not mutually exclusive, opinions vary as to which is the most important. The role of sexual selection has been questioned because mating system, which should reflect its strength, poorly predicts variation in canine dimorphism, particularly among polygynous species. Kay et al. (1988) demonstrate that a more refined estimate of intermale competition explains a large proportion of the variation in canine dimorphism in platyrrhine primates. We expand their analysis, developing a more generalized measure of intermale competition based on the frequency and intensity of male-male agonism. We examine the relative influences of predation (inferred by substrate use), female body weight, body-weight dimorphism, diet, and sexual selection on the evolution of anthropoid canine dimorphism. Intermale competition is very strongly associated with canine dimorphism. Predation also has a marked effect on canine dimorphism, in that savanna-dwelling species consistently show greater canine dimorphism than other species, all other factors being held equal. Body-weight dimorphism is also strongly associated with canine dimorphism, though apparently through a common selective basis, rather than through allometric effects. Body weight seems to play only a minor, indirect role in the evolution of canine dimorphism. Diet plays no role. Likewise, we find little evidence that phylogenetic inertia is a constraint on the evolution of canine dimorphism.     

Sexual dimorphism of body size and shell shape in European tortoises

Adult body size and shape were examined in almost 1400 individuals of the tortoises Testudo graeca , T. hermanni and T. marginata from Greece. The size at maturity was greater in females than in males in all three species. Maximum and mean adult sizes were also greater in females than in males in T. graeca and T. hermanni . Males grew to a larger size than females in T. marginata , and mean adult size was similar in the sexes in this species. Sexual dimorphism of shape (adjusted for size covariate) was shown in most of the characters examined, and the degree of this dimorphism differed significantly among the three species. Differences were related to their contrasting courtship behaviours: horizontal head movements and severe biting in T. marginata , vertical head bobs and carapace butting in T. graeca , and mounting and tail thrusting in T. hermanni . There was no difference in the frequency of observations of courtship or fighting among the three species, but courtship was about 10 times more common than combat in males. All species showed greatest courtship activity in autumn; copulation was rarely observed in T. hermanni (only 0.36% of courting males) and not seen in the other species in the field. Observations made throughout the activity season indicated that feeding was equally common in males and females in all three species. Differences in shape were more likely to be the result of sexual selection than of natural selection for fecundity. Detailed predictions are made for sexual dimorphism of other characters in these species.     

Sexual dimorphism in lizard body shape: the roles of sexual selection and fecundity selection

Sexual dimorphism is widespread in lizards, with the most consistently dimorphic traits being head size (males have larger heads) and trunk length (the distance between the front and hind legs is greater in females). These dimorphisms have generally been interpreted as follows: (1) large heads in males evolve through male-male rivalry (sexual selection); and (2) larger interlimb lengths in females provide space for more eggs (fecundity selection). In an Australian lizard (the snow skink, Niveoscincus microlepidotus), we found no evidence for ongoing selection on head size. Trunk length, however, was under positive fecundity selection in females and under negative sexual selection in males. Thus, fecundity selection and sexual selection work in concert to drive the evolution of sexual dimorphism in trunk length in snow skinks.     

Sexual selection on skeletal shape in Carnivora

Lifetime reproductive success of males is often dependent upon the ability to physically compete for mates. However, species variation in social structure leads to differences in the relative importance of intraspecific aggression. Here, we present a large comparative dataset on sexual dimorphism in skeletal shape in Carnivora to test the hypotheses that carnivorans exhibit sexual dimorphism in skeletal anatomy that is reflective of greater specialization for physical aggression in males relative to females and that this dimorphism is associated with the intensity of sexual selection. We tested these hypotheses using a set of functional indices predicted to improve aggressive performance. Our results indicate that skeletal shape dimorphism is widespread within our sample. Functional traits thought to enhance aggressive performance are more pronounced in males. Phylogenetic model selection suggests that the evolution of this dimorphism is driven by sexual selection, with the best‐fitting model indicating greater dimorphism in polygynous versus nonpolygynous species. Skeletal shape dimorphism is correlated with body size dimorphism, a common indicator of the intensity of male–male competition, but not with mean body size. These results represent the first evidence of sexual dimorphism in the primary locomotor system of a large sample of mammals.     

Sexual conflict in primates

Sexual conflict is increasingly recognized as a major force for evolutionary change and holds great potential for delineating variation in primate behavior and morphology. The goals of this review are to highlight the rapidly rising field of sexual conflict and the ongoing shift in our understanding of interactions between the sexes. We discuss the evidence for sexual conflict within the Order Primates, and assess how studies of primates have illuminated and can continue to increase our understanding of sexual conflict and sexual selection. Finally, we introduce a framework for understanding the behavioral, anatomical, and genetic expression of sexual conflict across primate mating systems and suggest directions for future research.     

Sexual dimorphism and dental variability in platyrrhine primates

Leutenegger and Cheverud (1982, 1985) propose a hypothesis to explain why larger primates are more sexually dimorphic in body weight and canine size. Their hypothesis states that any factor selecting for an evolutionary increase in body size will produce an increase in sexual dimorphism in any character if either heritability or phenotypic variability is greater in males than in females for that character. They cite no evidence for heritability but give some data to suggest that males are, in fact, more variable than females. We test the latter proposition more fully using measurements on the dentitions of platyrrhine primates. Male and female phenotypic variances are not significantly different in most cases. Cases of greater male phenotypic variance are not limited to sexually dimorphic species. We conclude that the hypothesis of Leutenegger and Cheverud does not explain the observed patterns of dental sexual dimorphism, at least in platyrrhines.     

Sexual dimorphism in weight among the primates: The relative impact of allometry and sexual selection

In this paper, we examine allometric and sexual-selection explanations for interspecific differences in the amount of sexual dimorphism among 60 primate species. Based on evidence provided by statistical analyses, we reject Leutenegger and Cheverud’s [(1982). Int. J. Primatol.3:387-402] claim that body size alone is the major factor in the evolution of sexual dimorphism. The alternative proposed here is that sexual selection due to differences in the reproductive potential of males and females is the primary cause of sexual dimorphism. In addition, we propose that the overall size of a species determines whether the dimorphism will be expressed as size dimorphism,rather than in some other form.     

Sexual size dimorphism in parasitoid wasps

Sexual dimorphism in body length and proportion of overlap between the ranges of body length for males and females were estimated for 361 species of parasitoid wasps from 21 families. In most species, females are generally larger than males, though the range of male and female sizes overlap. Species in the family Ichneumonidae differ significantly from species in other families in three ways: (1) ichneumonids on average are larger, (2) in most species, females are generally smaller than males, and (3) on average, proportion overlap between the ranges of body length for males and females is greater. At present, there is a paucity of life history data on parasitoid wasp species for which size dimorphism is known. Thus it is not clear why ichneumonids differ from species in other families. Possible evolutionary explanations for variation in dimorphism among parasitoid wasp species are discussed.     

Sexual dimorphism of head morphology in three‐spined stickleback Gasterosteus aculeatus

This study examined sexual dimorphism of head morphology in the ecologically diverse three‐spined stickleback Gasterosteus aculeatus. Male G. aculeatus had longer heads than female G. aculeatus in all 10 anadromous, stream and lake populations examined, and head length growth rates were significantly higher in males in half of the populations sampled, indicating that differences in head size increased with body size in many populations. Despite consistently larger heads in males, there was significant variation in size‐adjusted head length among populations, suggesting that the relationship between head length and body length was flexible. Inter‐population differences in head length were correlated between sexes, thus population‐level factors influenced head length in both sexes despite the sexual dimorphism present. Head shape variation between lake and anadromous populations was greater than that between sexes. The common divergence in head shape between sexes across populations was about twice as important as the sexual dimorphism unique to each population. Finally, much of the sexual dimorphism in head length was due to divergence in the anterior region of the head, where the primary trophic structures were found. It is unclear whether the sexual dimorphism was due to natural selection for niche divergence between sexes or sexual selection. This study improves knowledge of the magnitude, growth rate divergence, inter‐population variation and location of sexual dimorphism in G. aculeatus head morphology.     

Sexual dimorphism of cranial suture complexity in wild sheep (Ovis orientalis)

Sutural complexity (the degree of interdigitation) of 13 cranial sutures was compared between male and female wild sheep ( Ovis orientalis ) to investigate a morphological feature that is potentially important with respect to stress transmission in the skulls of males during fighting. Most facial sutures (four of six) were not sexually dimorphic, but two sutures, the maxillojugal and jugolacrimal, had greater complexity in males than in females, suggesting that significant forces may be transmitted through the facial region of rams, most likely during horn clashing. Most of the braincase sutures (five of seven) were more complex in males than in females, and different factors appear to underlie this sexual dimorphism. In females, increased complexity of sutures during ontogeny was predicted best by variables measuring growth of the skull, brain or face, while in males, changes in complexity were predicted best by variables representing mechanical loading and frontal bone growth.     

Sexual size dimorphism and sexual selection in primates

1. In most animals, females are larger than males. Paradoxically, sexual size dimorphism is biased towards males in most mammalian species. An accepted explanation is that sexual dimorphism in mammals evolved by intramale sexual selection. I tested this hypothesis in primates, by relating sexual size dimorphism to seven proxies of sexual selection intensity: operational sex ratio, mating system, intermale competition, group sex ratio, group size, maximum mating percentage (percentage of observed copulations involving the most successful male), and total paternity (a genetic estimate of the percentage of young sired by the most successful male).
2. I fitted phylogenetic generalised least squares models using sexual size dimorphism as the dependent variable and each of the seven measures of intensity of sexual selection as independent variables. I conducted this comparative analysis with data from 50 extant species of primates, including Homo sapiens, Pan troglodytes, and Gorilla spp.
3. Sexual dimorphism was positively related to the four measures of female monopolisation (operational sex ratio, mating system, intermale competition, and group sex ratio) and in some cases to group size, but was not associated with maximum mating percentage or total paternity. Additional regression analyses indicated that maximum mating percentage and total paternity were negatively associated with group size.
4. These results are predicted by reproductive skew theory: in large groups, males can lose control of the sexual behaviour of the other members of the group or can concede reproductive opportunities to others. The results are also consistent with the evolution of sexual size dimorphism before polygyny, due to the effects of natural, rather than sexual, selection. In birds, the study of molecular paternity showed that variance in male reproductive success is much higher than expected by behaviour. In mammals, recent studies have begun to show the opposite trend, i.e. that intensity of sexual selection is lower than expected by polygyny.
5. Results of this comparative analysis of sexual size dimorphism and sexual selection intensity in primates suggest that the use of intramale sexual selection theory to explain the evolution of polygyny and sexual dimorphism in mammals should be reviewed, and that natural selection should be considered alongside sexual selection as an evolutionary driver of sexual size dimorphism and polygyny in mammals.

     

Sexual size dimorphism and timing of spring migration in birds

Sexually selected traits are limited by selection against those traits in other fitness components, such as survival. Thus, sexual selection favouring large size in males should be balanced by higher mortality of larger males. However, evidence from red-winged blackbirds (Agelaius phoeniceus) indicates that large males survive better than small males. A survival advantage to large size could result from males migrating north in early spring, when harsh weather favours large size for energetic reasons. From this hypothesis we predicted that, among species, sex differences in body size should be correlated with sex differences in timing of spring migration. The earlier males migrate relative to females, the larger they should be relative to females. We tested this prediction using a comparative analysis of data collected from 30 species of passerine birds captured on migration. After controlling for social mating system, we found that sexual size dimorphism and difference in arrival dates of males and females were significantly positively correlated. This result is consistent with the hypothesis that selection for survival ability promotes sexual size dimorphism (SSD), rather than opposes SSD as is the conventional view. If both natural selection and sexual selection favour large adult males, then limits to male size must be imposed before males become adults.     

Sexual selection and sexual size dimorphism in animals

Sexual selection is often considered as a critical evolutionary force promoting sexual size dimorphism (SSD) in animals. However, empirical evidence for a positive relationship between sexual selection on males and male-biased SSD received mixed support depending on the studied taxonomic group and on the method used to quantify sexual selection. Here, we present a meta-analytic approach accounting for phylogenetic non-independence to test how standardized metrics of the opportunity and strength of pre-copulatory sexual selection relate to SSD across a broad range of animal taxa comprising up to 95 effect sizes from 59 species. We found that SSD based on length measurements was correlated with the sex difference in the opportunity for sexual selection but showed a weak and statistically non-significant relationship with the sex difference in the Bateman gradient. These findings suggest that pre-copulatory sexual selection plays a limited role for the evolution of SSD in a broad phylogenetic context.     

Sexual dimorphism and allometry of external morphology in Oreochromis mossambicus

Sexual dimorphism in growth of conventional morphometric characters was investigated in juveniles and young adults (size range: 31 to 91 mm) of Oreochromis mossambicus . A closely associated set of traits was identified that shows sexually dimorphic growth, which was positively allometric in the males. These traits correspond to two different morphological complexes: jaw structure and anal/dorsal fins. The best sex discriminators among this set of traits were premaxilla width, anal fin height and snout length. These findings may be explained in terms of intra– and inter–sexual selection acting together and favouring males with strong and large mouths and high dorsal and anal fins, traits that are important in agonistic displays (jaw and fins), fighting and nest digging (jaw).     

Sexual size dimorphism and assortative mating in Carolina Wrens

ABSTRACT.   Sexual size dimorphism (SSD) may be due to sexual and natural selection, but identifying specific mechanisms that generate such dimorphism in a species is difficult. I examined SSD in Carolina Wrens ( Thryothorus ludovicianus ) by examining (1) the degree of SSD in the population and between pairs using five morphometrics, (2) assortative mating patterns based on size and age, and (3) relationships between size and longevity. Analysis revealed that males were significantly larger than females in all body measurements. For example, mass, bill, and wing measurements yielded a canonical variable that permitted separation of the sexes and linear classification functions correctly determined the sex of 95% (238/250) of all wrens measured. No evidence was found to suggest that SSD was related to resource partitioning. However, assortative mating trends based on morphometrics (e.g., wing length), positive associations between longevity and morphometrics (e.g., wing length in females and body size in males), and intense male-male contests for territorial resources year-round provide evidence that sexual selection may contribute to SSD in Carolina Wrens.     

Sex and Weapons: Contrasting Sexual Dimorphisms in Weaponry and Aggression in Snapping Shrimp

Sexual dimorphisms in weaponry and aggression are common in species in which one sex (usually males) competes for access to mates or resources necessary for reproduction – sexually dimorphic weaponry and aggression, in other words, are frequently the result of intrasexual selection. In snapping shrimp, the major chela (snapping claw) can be a deadly weapon, and males of many species have larger chelae than females, a pattern readily interpreted as resulting from intrasexual selection. Thus, males might be expected to show more sex‐specific aggression than females, and be more aggressive overall. We tested these predictions in two species of snapping shrimp in a territorial defense context. Neither of these predictions was supported: in both species, females, but not males, engaged in sex‐specific aggression and females were more aggressive than males overall. These contrasting sexual dimorphisms – larger weaponry in males but higher aggression in females – highlight the importance of considering the function of weaponry and aggression in contexts other than direct competitions over mates. In addition, species differences in the degree of sexual dimorphism in chela size were due to differences in female, not male, chela size, and the species with greater sexual dimorphism in weaponry was significantly less aggressive overall; also, while paired and solitary males did not differ in residual chela size, for the species with greater sexual dimorphism, females carrying embryos had smaller residual chela sizes. These results suggest that understanding the sexual dimorphisms in weaponry and aggression in snapping shrimp requires understanding the relative costs and benefits of both in females as well as males.