Ontogeny and the evolution of adult body size dimorphism in apes

This analysis investigates the ontogeny of body size dimorphism in apes. The processes that lead to adult body size dimorphism are illustrated and described. Potential covariation between ontogenetic processes and socioecological variables is evaluated. Mixed-longitudinal growth data from 395 captive individuals (representing Hylobates lar [gibbon], Hylobates syndactylus [siamang], Pongo pygmaeus [orangutan], Gorilla gorilla [gorilla], Pan paniscus [pygmy chimpanzee], and Pan troglodytes [“common” chimpanzee]) form the basis of this study. Results illustrate heterogeneity in the growth processes that produce ape dimorphism. Hylobatids show no sexual differentiation in body weight growth. Adult body size dimorphism in Pongo can be largely attributed to indeterminate male growth. Dimorphism in African apes is produced by two different ontogenetic processes. Both pygmy chimpanzees (Pan paniscus) and gorillas (Gorilla gorilla) become dimorphic primarily through bimaturism (sex differences in duration of growth). In contrast, sex differences in rate of growth account for the majority of dimorphism in common chimpanzees (Pan troglodytes). Diversity in the ontogenetic pathways that produce adult body size dimorphism may be related to multiple evolutionary causes of dimorphism. The lack of sex differences in hylobatid growth is consistent with a monogamous social organization. Adult dimorphism in Pongo can be attributed to sexual selection for indeterminate male growth. Interpretation of dimorphism in African apes is complicated because factors that influence female ontogeny have a substantial effect on the resultant adult dimorphism. Sexual selection for prolonged male growth in gorillas may also increase bimaturism relative to common chimpanzees. Variation in female growth is hypothesized to covary with foraging adaptations and with differences in female competition that result from these foraging adaptations. Variation in male growth probably corresponds to variation in level of sexual selection. © 1995 Wiley-Liss, Inc.     

Correlates of sexual dimorphism in primates: Ecological and size variables

The effects of a series of ecological and size factors on the degree of sexual dimorphism in body weight and canine size were studied among subsets of 70 primate species. Variation in body-weight dimorphism can be almost entirely attributed to body weight (83% of variance R² of weight dimorphism). Much smaller amounts of the variation can be attributed to mating system (R² =6.8%,polygynous species being more dimorphic than monogamous ones) and diet (R² = 2.5%,frugivorous species being more dimorphic than folivorous ones). Habitat (arboreal vs. terrestrial) and activity rhythm (nocturnal vs. diurnal) have only an indirect effect on weight dimorphism. Variation in canine-size dimorphism can be explained in terms of canine size (R² =49%),activity rhythm (R² = 20%,diurnal species being more dimorphic than nocturnal ones), and mating system (R² = 10%).Habitat and diet do not play a significant role in canine-size dimorphism. The unexpectedly high contribution of size to sexual dimorphism coupled with the observation of increased sexual dimorphism with increased size leads us to formulate a new selection model for the evolution of sexual dimorphism. We suggest that if there is selection for size increase, whatever its cause, directional selection in both males and females will lead to an increase in sexual dimorphism based on differences in genetic variance between the sexes. Sexual selection, resource division between the sexes, or lopsided reproductive selection need not play a role in such a model.     

Cranial morphology and adaptations in Eocene Adapidae. I. Sexual dimorphism in Adapis magnus and Adapis parisiensis

Adapis is one of the best known lemuriform fossil primates. Quantitative analysis of all well-preserved crania of Adapis magnus (n = 8) and Adapis parisiensis (n = 12) together with maxillary and mandibular dentitions preserving canines corroborates Stehlin's hypothesis that Adapis was sexually dimorphic. Males are from 13% to 16% larger than females in cranial length, corresponding to a weight dimorphism estimated at 44% to 56%, and have relatively broader skulls with more prominent sagittal and nuchal crests. Canine dimorphism ranges from 13% to 19%, which is equal to or only slightly greater than that expected as a result of body size dimorphism (i.e., relative canine dimorphism is slight or nonexistent). By comparison with living primates, the observed body size dimorphism in Adapis implies a polygynous breeding system. Cebus apella is a diurnal arboreal living primate with moderate body size dimorphism and slight relative canine dimorphism and one can speculate that Adapis lived in polygynous multimale troops of moderate size like those of C. appella. Adapis extends the geological history of sexual dimorphism and polygyny in primates back to the Eocene. Extant lemuriform primates are generally not dimorphic or polygynous and they clearly do not adequately represent the range of social adaptations present in Eocene primates. The evolutionary lineage from Adapis magnus to Adapis parisiensis exhibits reduction in body size and in relative canine size, and phyletic dwarfing in Adapis is possibly an adaptive response to increasing climatic seasonality and environmental instability in the late Eocene and early Oligocene.     

Canine Dimorphism and Interspecific Canine Form in Cebus

I investigated canine dimorphism and interspecific canine form in adult specimens from 4 capuchin species (Cebus albifrons, C. apella, C. capucinus, and C. olivaceus). I used various univariate and multivariate statistics, which are based on 6 variables, to test several hypotheses that are based upon the finding that canine dimorphism is strongly associated with intermale competition in platyrrhines (Kay et al., 1988), Greenfield (1992a), Plavcan and van Schaik (1992, 1994). Results from the indices of canine dimorphism and the unpaired t-tests corroborate the prediction that males of each species possess significantly larger canines than those of females. Large male canines are especially prominent in 2 variables, maxillary and mandibular canine height. Greene's t-test (1989) does not support the prediction that Cebus apella and C. olivaceus possess a larger degree of canine dimorphism relative to C. albifrons and C. capucinus. No interspecific differences in degree of canine dimorphism are indicated by this test. Results of the discriminant function analyses (DFA) do not find that Cebus apella and C. olivaceus possess different canine form relative to C. albifrons and C. capucinus as predicted. However, Cebus apella is differentiated from the untufted capuchins (C. albifrons, C. capucinus, and C. olivaceus) by the DFA. I suggest that intermale competition is the primary selective force underlying the observed morphological patterns; however, it does not explain all the variation associated with canine dimorphism in Cebus.     

Metric variability in the anterior dentition of African colobines

The anterior dentition of three species of African colobines (Colobus polykomos, C. badius, and C. verus) was investigated metrically and the results analyzed for three characters: (1) intraspecific tooth size relations, (2) sexual dimorphism, and (3) interspecific relations. Based on incisor size sequences C. polykomos and C. badius appear to be more closely related to each other than either is to C. verus. However, incorporating the results of a previous study on postcanine dentition the three species appear to be equally closely related. The magnitude of sexual dimorphism in canine size decreases from C. badius to C. verus to C. polykomos. Interspecific differences in the degree of canine size dimorphism may be attributed to differential intensities of male intrasexual selection; however, the interspecific differences in canine size dimorphism do not correspond to the interspecific differences in body size dimorphism.     

Sexual dimorphism in the skull geometry of newt species of <Emphasis Type="Italic">Ichthyosaura,Triturus</Emphasis> and <Emphasis Type="Italic">Lissotriton</Emphasis> (Salamandridae,Caudata, Amphibia)

In this study, we applied geometric morphometrics to explore variations in the level and pattern of sexual size dimorphism (SSD) and sexual shape dimorphism (SShD) of the ventral cranium in three different Modern Eurasian newt taxa (Ichthyosaura alpestris, Triturus species group and Lissotriton vulgaris). The ventral cranium is the part of the skull that is more directly related to foraging and feeding. Our results indicate that the level and pattern of sexual dimorphism in the ventral cranium differ among Modern Eurasian newt taxa. Regarding sexual dimorphism in skull size, Ichthyosaura alpestris and Triturus species show female-biased patterns (females are larger than males), whereas Lissotriton vulgaris appears to be non-dimorphic in skull size. In I. alpestris and Triturus species, SShD is mostly absent, whereas in L. vulgaris, SShD is more pronounced. A high level of variation between populations in both SSD and SShD indicates that local conditions may have a profound effect on the magnitude and direction of sexual dimorphism. The significant sexual differences in ventral cranium size and shape indicate possible subtle intersexual differences in ecological demands due to diet specialisation, in spite of similar general ecological settings.     

Cranial ontogeny and sexual dimorphism in two new world monkeys: Alouatta caraya (Atelidae) and Cebus apella (Cebidae)

Pattern of skull development and sexual dimorphism was studied in Cebus apella and Alouatta caraya using univariate, bivariate, and multivariate statistics. In both species, sexual dimorphism develops because the common growth trajectory in males extends and because of differences in growth rates between sexes. The expectation that the ontogenetic bases of adult dimorphism vary interspecifically is well substantiated by this study. A. caraya exhibits transitional dimorphism in its subadult stage, although the condylobasal length, zygomatic breadth, and rostrum length are strongly dimorphic in the final adult stage, being greater in males. Most cranial measurements in C. apella exhibit significant dimorphism in the adult stage, being strongly influenced by a faster rate of growth in males. Sexual dimorphism is also evidenced through sex differences in growth rates in several cranial measurements. These results also indicate that different ontogenetic mechanisms are acting in C. apella and A. caraya and reveal differences in the way through which neotropical primates attain adult sexual dimorphism. J. Morphol. 2011. © 2011 Wiley‐Liss, Inc.     

Sexual Dimorphism and Mortality Bias in a Small Miocene North American Rhino, <Emphasis Type="Italic">Menoceras arikarense</Emphasis>: Insights into the Coevolution of Sexual Dimorphism and Sociality in Rhinos

Rhinos are the only modern perissodactyls that possess cranial weapons similar to the horns, antlers and ossicones of modern ruminants. Yet, unlike ruminants, there is no clear relationship between sexual dimorphism and sociality. It is possible to extend the study of the coevolution of sociality and sexual dimorphism into extinct rhinos by examining the demographic patterns in large fossil assemblages. An assemblage of the North American early Miocene (∼22 million years ago) rhino, Menoceras arikarense, from Agate Springs National Monument, Nebraska, exhibits dimorphism in incisor size and nasal bone size, but there is no detectible dimorphism in body size. The degree of dimorphism of the nasal horn is greater than the degree of sexual dimorphism of any living rhino and more like that of modern horned ruminants. The greater degree of sexual dimorphism in Menoceras horns may relate to its relatively small body size and suggests that the horn had a more sex-specific function. It could be hypothesized that Menoceras evolved a more gregarious type of sociality in which a fewer number of males were capable of monopolizing a larger number of females. Demographic patterns in the Menoceras assemblage indicate that males suffered from a localized risk of elevated mortality at an age equivalent to the years of early adulthood. This mortality pattern is typical of living rhinos and indicates that young males were susceptible to the aggressive behaviors of dominant individuals in areas conducive to fossilization (e.g., ponds, lakes, rivers). Menoceras mortality patterns do not suggest a type of sociality different from modern rhinos although a group forming type of sociality remains possible. Among both living and extinct rhinos, the severity of socially mediated mortality seems unrelated to the degree of sexual dimorphism. Thus, sexual dimorphism in rhinos is not consistent with traditional theories about the co-evolution of sexual dimorphism and sociality.     

The differential expression of dental sexual dimorphism in subspecies ofColobus guereza

Data on dental sex differences in seven of the eight currently recognized subspecies of Colobus guerezareveals a range of expression of sexual dimorphism. Males of most subspecies are larger than females throughout the dentition and this is especially pronounced for the canines and P ₃ For C. g. guerezaand C. g. gallarum,however, sex differences in the canines and P ₃ are less pronounced and females are often slightly larger than males in noncanine dental measurements. C. guerezasspp. occupying comparable habitats express similarities in the degree of maxillary canine dimorphism. In addition, for those subspecies distributed above the equator, there is also a cline of decreasing maxillary canine dimorphism from west to east in a progressively more northern direction. This cline corresponds to the occupation of increasingly more arid habitats, and reduced dimorphism is the result of larger maxillary canine size in females. We propose that this pattern of sexual dimorphism is related to differences in the relative intensity of predation pressure, guereza social organization, and energetic considerations. That the mandibular canine does not exhibit a similar trend of sexual dimorphism suggests that larger maxillary canines in females may function as weapons.     

Degrees of sexual dimorphism in Cebus and other new world monkeys

Sexual dimorphism in primate species expresses the effects of phylogeny, life history, behavior, and ontogeny. The causes and implications of sexual dimorphism have been studied in several different primates using a variety of morphological databases such as body weight, canine length, and coat color and ornamentation. In addition to these different patterns of dimorphism, the degree to which a species is dimorphic results from a variety of possible causes. In this study we test the general hypothesis that a species highly dimorphic for one size-based index of dimorphism will be equally dimorphic (relative to other species) for other size-based indices. Specifically, the degree and pattern of sexual dimorphism in Cebus and several other New World monkey species is measured using craniometric data as a substitute for the troublesome range of variation in body weight estimates. In general, the rank ordering of species for dimorphism ratios differs considerably across neural vs. non-neural functional domains of the cranium. The relative degree of sexual dimorphism in different functional regions of the cranium is affected by the independent action of natural selection on those regions. Regions of the cranium upon which natural selection is presumed to have acted within a species show greater degrees of dimorphism than do the same regions in closely related taxa. Within Cebus, C. apella is consistently more dimorphic than other Cebus species for facial measurements, but not for neural or body weight measurements. The pattern in C. apella indicates no single best measurement of the degree of dimorphism in a species; rather, the relative degree of dimorphism applies only to the region being measured and may be enhanced by other selective pressures on morphology. Am J Phys Anthropol 107:243–256, 1998. © 1998 Wiley-Liss, Inc.     

Sexual dimorphism in the snub-nosed langurs (Colobinae: Rhinopithecus)

Sexual dimorphism in the dentition and skeleton of the four extant species of snub-nosed langurs, Rhinopithecus (R.) bieti, R. (R.) brelichi, R. (R.) roxellana and R. (Presbytiscus) avunculus, was studied. The species shared a similar general pattern of sexual dimorphism, but were found to differ in respects that appear to reflect the influence of disparate socioecological and environmental factors. All the species showed marked canine dimorphism, but the very high degree of canine dimorphism in R. bieti appeared to be due to the intensity of intermale competition for mates during a temporally restricted breeding season, and possibly also to the intensity of competition between males for other resources during other times of the year. Sexual dimorphism in the postcranial skeleton of Rhinopithecus species was also most pronounced in R. bieti and may be related to the relatively higher frequency of terrestrial locomotion in males of the species. © 1995 Wiley-Liss, Inc.     

Sexual dimorphism in the face of Australopithecus africanus

Recently discovered crania of Australopithecus africanus from Sterkfontein Member 4 and Makapansgat enlarge the size range of the species and encourage a reappraisal of both the degree and pattern of sexual dimorphism. Resampling methodology (bootstrapping) is used here to establish that A. africanus has a greater craniofacial size range than chimpanzees or modern humans, a range which is best attributed to a moderately high degree of sexual dimorphism. Compared to other fossil hominins, this variation is similar to that of Homo habilis (sensu lato) but less than that of A. boisei. The finding of moderately high dimorphism is corroborated by a CV-based estimate and ratios between those specimens considered to be male and those considered to be female. Inferences about the pattern of craniofacial dimorphism in the A. africanus face currently rely on the relationship of morphology and size. Larger specimens, particularly Stw 505, show prominent superciliary eminences and glabellar regions, but in features related in part to canine size, such as the curvature of the infraorbital surface, large and small specimens of A. africanus are similar. In this respect, the pattern resembles that of modern humans more so than chimpanzees or lowland gorillas. A. africanus may also show novel patterns of sexual dimorphism when compared to extant hominines, such as in the form of the anterior pillar. However, males of the species do not exhibit characteristics of more derived hominins, such as A. robustus. Am J Phys Anthropol 108:97–127, 1999. © 1999 Wiley-Liss, Inc.     

Sexual dimorphism in relative sacral breadth among catarrhine primates

As the sacrum contributes to the size and shape of the birth canal, the sexually dimorphic sacrum of humans is frequently interpreted within obstetric contexts. However, while the human sacrum has been extensively studied, comparatively little is known about sacral morphology in nonhuman primates. Thus, it remains unclear whether sacral sexual dimorphism exists in other primates, and whether potential dimorphism is primarily related to obstetrics or other factors such as body size dimorphism. In this study, sacra of Homo sapiens, Hylobates lar, Nasalis larvatus, Gorilla gorilla, Pongo pygmaeus, Pan troglodytes, and Pan paniscus were evaluated for sexual dimorphism in relative sacral breadth (i.e., the ratio of overall sacral breadth to first sacral vertebral body breadth). Homo sapiens, H. lar, N. larvatus, and G. gorilla exhibit dimorphism in this ratio. Of these, the first three species have large cephalopelvic proportions, whereas G. gorilla has small cephalopelvic proportions. P. pygmaeus, P. troglodytes, and P. paniscus, which all have small cephalopelvic proportions, were not dimorphic for relative sacral breadth. We argue that among species with large cephalopelvic proportions, wide sacral alae in females facilitate birth by increasing the pelvic inlet's transverse diameter. However, given the small cephalopelvic proportions among gorillas, an obstetric basis for dimorphism in relative sacral breadth appears unlikely. This raises the possibility that sacral dimorphism in gorillas is attributable to selection for relatively narrow sacra in males rather than relatively broad sacra in females. Accordingly, these results have implications for interpreting pelvic dimorphism among fossil primates, including hominins. Am J Phys Anthropol 152:435–446, 2013. © 2013 Wiley Periodicals, Inc.     

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.     

Leptin's Sexual Dimorphism Results from Genotype by Sex Interactions Mediated by Testosterone

Objective: Recent studies have reported the existence of marked sexual dimorphism in serum leptin levels in humans, with women having approximately three times the levels of men. As we have shown for other measures of adiposity, such sexual dimorphism can arise from a special case of genotype by environment interaction, that of genotype by sex interaction. Research Methods and Procedures: Using maximum likelihood-based variance decomposition techniques, we examined the genetic and environmental architecture of sexual dimorphism in serum leptin levels in 1147 Mexican Americans from the San Antonio Family Heart Study. Results: Both the genetic and environmental variances for this trait differed significantly between the sexes (p < 0.001 and p < 0.01, respectively), with women displaying larger values for both components. We found significant evidence that different genes influence variation in serum leptin levels between the two sexes (p = 0.05). Furthermore, this pattern of sexual dimorphism in serum leptin levels persisted even after accounting for the effects of either the percentage of body fat or total body fat. However, this pattern of sexual dimorphism was eliminated after accounting for the effects of testosterone. Discussion: These findings suggest that the sexual dimorphism seen in leptin levels is not simply explained as differences in total adiposity between the sexes. We conclude that the genes, which influence variation in serum leptin levels, are differentially expressed depending on sex, and that the sexes also show differences in response of the expression of this obesity-related trait to unmeasured residual effects.     

SEX CHROMOSOME LINKED GENETIC VARIANCE AND THE EVOLUTION OF SEXUAL DIMORPHISM OF QUANTITATIVE TRAITS

Theory predicts that sex chromsome linkage should reduce intersexual genetic correlations thereby allowing the evolution of sexual dimorphism. Empirical evidence for sex linkage has come largely from crosses and few studies have examined how sexual dimorphism and sex linkage are related within outbred populations. Here, we use data on an array of different traits measured on over 10,000 individuals from two pedigreed populations of birds (collared flycatcher and zebra finch) to estimate the amount of sex‐linked genetic variance (h²_z). Of 17 traits examined, eight showed a nonzero h²_Z estimate but only four were significantly different from zero (wing patch size and tarsus length in collared flycatchers, wing length and beak color in zebra finches). We further tested how sexual dimorphism and the mode of selection operating on the trait relate to the proportion of sex‐linked genetic variance. Sexually selected traits did not show higher h²_Z than morphological traits and there was only a weak positive relationship between h²_Z and sexual dimorphism. However, given the relative scarcity of empirical studies, it is premature to make conclusions about the role of sex chromosome linkage in the evolution of sexual dimorphism.     

Sexual size dimorphism in the great tit (Parus major) in relation to history and current selection

We investigated the possible causes of the evolution of sexual size and shape dimorphism in the great tit (Parus major) by using two different approaches. First, we used the equilibrium approach, i.e. analysing current selection to see whether it was possible to find directional selection in the direction of the dimorphism, or stabilising selection maintaining dimorphism at its current level. Second, we used the historical approach, i.e. putting the degree of dimorphism in a phylogenetic perspective to analyse what kind of changes (if any) have occurred. This was carried out in the following way: (i) we described the level of sexual dimorphism in a population of Swedish great tits by means of path model. (ii) We used the path model design to analyse survival and reproductive selection in this population. (iii) We compared the level of dimorphism in relation to size in the great tit with that of the closest congener, the blue tit P. caeruleus. (iv) We compared the amount of interspecific morphological variation with that which would be expected under a drift model. We found no evidence of either stabilising or directional survival or reproductive selection. Size and shape variation in the great tit seemed unrelated to fitness in adults. Dimorphism was somewhat greater in the great tit compared to the blue tit, but only with an amount predictable by its larger size. In terms of phenotypic standard deviations, the great tit was not more dimorphic than the blue tit, although it was larger. The amount of interspecific variance with regard to size was lower or equal to that expected by the drift model, showing that long-term directional selection for an increase in size and dimorphism is improbable. These results agree with recent theoretical findings that size and dimorphism should be related and that strong conservatism with regard to dimorphism is to be expected. They also agree with the view that in equilibrium populations, fitness components (if there are many of them) should appear neutral with regard to total fitness.     

An APETALA3 homolog controls both petal identity and floral meristem patterning in Nigella damascena L. (Ranunculaceae)

Flower architecture mutants provide a unique opportunity to address the genetic origin of flower diversity. Here we study a naturally occurring floral dimorphism in Nigella damascena (Ranunculaceae), involving replacement of the petals by numerous sepal‐like and chimeric sepal/stamen organs. We performed a comparative study of floral morphology and floral development, and characterized the expression of APETALA3 and PISTILLATA homologs in both morphs. Segregation analyses and gene silencing were used to determine the involvement of an APETALA3 paralog (NdAP3–3) in the floral dimorphism. We demonstrate that the complex floral dimorphism is controlled by a single locus, which perfectly co‐segregates with the NdAP3–3 gene. This gene is not expressed in the apetalous morph and exhibits a particular expression dynamic during early floral development in the petalous morph. NdAP3–3 silencing in petalous plants perfectly phenocopies the apetalous morph. Our results show that NdAP3–3 is fully responsible for the complex N. damascena floral dimorphism, suggesting that it plays a role not only in petal identity but also in meristem patterning, possibly through regulation of perianth organ number and the perianth/stamen boundary.     

Morphological Variation in Populations of <Emphasis Type="Italic">Eulemur albocollaris</Emphasis> and <Emphasis Type="Italic">E. fulvus rufus</Emphasis>

Sexual dimorphism in body size and canine weaponry is commonly associated with high levels of male-male competition. When group living species do not rely heavily on male-male competition for access to females, sperm competition may represent a viable alternative strategy. Unlike most haplorhine primates, lemurs are typically monomorphic in body weight and canine height. We assessed variability of body mass dimorphism and canine size dimorphism in brown lemurs using morphometric data from 3 populations in southeastern Madagascar: Eulemur fulvus rufus, E. albocollaris, and hybrids of the species. We found significant male-biased canine dimorphism in E. albocollaris in conjunction with body-size monomorphism. We observed similar patterns in the hybrids, but E. fulvus rufus exhibited significant female-biased size dimorphism and canine monomorphism. Testes volume was relatively high across study populations. Thus, sperm competition appears to be strong in brown lemurs. E. albocollaris males combine sperm competition with large canines, but not higher body mass, indicating a difference in sexual strategy from most lemurs. Patterns of body mass and canine size dimorphism are not uniform across brown lemur populations, indicating that future work on these populations can explicitly test models that predict relationships between size dimorphism and various types of competition.