Male age, dominance, and mating success among rhesus macaques

Some previous primate studies have found a positive correlation between male dominance and mating success when data from subadult males were included in the analyses. The information in this paper suggests that an unconscious bias may have been introduced when data on subadult males were included because of the lower dominance rank of these animals. Data from a study of rhesus monkeys on Cayo Santiago showed that subadult males mated significantly less than adults. Because these monkeys are not fully mature, data on them should not be used in any test for correlation between adult male dominance and mating success. The only significant correlation found for adult male mating success was an inverse one with relation to age. Based on behavioral data young, fully adult males have the best chance of fathering offspring regardless of their dominance rank.     

The measurement of form and variation in form: An application of three-dimensional quantitative morphology by finite-element methods

D'Arcy Thompson developed a method of coordinates which allowed for a geometrical presentation of form and form change. While his grid transformations have received much attention, little work in the geometry of form and form change has occurred since. We present a three-dimensional nonhomogeneous finite-element scaling method which allows for the mathematical and geometrical measurement of form change in addition to the graphical representation of these deformations as D'Arcy Thompson grids. This allows a reconciliation between geometrical and statistical methods for analyzing form. The method involves quantification of the transformation of one form into another in three dimensions without special registration and contains algorithms for obtaining a mean form. The method is applied to an analysis of variation in cranial form among adult male rhesus macaques from the Cayo Santiago skeletal collection. Variation was greatest in the superior-inferior direction, followed by the anterior-posterior and medial-lateral directions. The upper facial region is particularly variable. An analysis of allometry relative to local size variation shows that the larger any particular region is, the relatively greater its height, narrower its width, and shorter its length. An analysis of allometry relative to overall size showed that the upper face is positively allometric, the occipital region is strongly negatively allometric, and the other regions are isometric. After within-group variation is characterized, as described here, between-group studies, such as growth series and phylogenetic series, can be performed.     

Models of ontogenetic allometry in cladoceran morphology studies

Ontogenetic variation of morphological traits in cladocerans is usually analysed by a simple allometry function. We found that common cyclomorphic and inducible traits in Bosmina and Daphnia sometimes deviate from simple allometry, however. Consequently, simple allometric analysis may at times be inadequate since important aspects of the ontogenetic development may not be revealed. We suggest that other allometric models should be used more extensively in ontogenetic studies of cladocerans morphology. Especially, complex allometric functions may help analyse the effects of size-selective predation on morphological defence traits when predators prefer prey of intermediate size. Guest editor: Piet Spaak Cladocera: Proceedings of the 7th International Symposium on Cladocera     

Variance in intrinsic rates of growth among free-ranging rhesus monkey groups

Differential rates of intrinsic growth for the population of Macaca mulatta on Cayo Santiago partitioned by social group and dominance rank of genealogies indicate that the potential for increase is not uniformly distributed throughout the population. In the period from 1973 to 1974, high-ranking genealogies were growing at a faster rate than low-ranking genealogies. Large differences in r among the social groups indicate the possible existence of demographic, genetic, or social differences between groups. A random resampling procedure was employed to assess the statistical significance of differences in the intrinsic rate of growth among the 5 natural social groups and the 3 partitions formed by, respectively, lumping members of high-, middle-, and low-ranking genealogies across several social groups. Comparisons among social groups shows that there are significant differences in the rate of growth between Group J and Group M, and between Group J and Group F for the period from 1973 to 1974. Among dominance ranks of genealogies, significant differences in r were found between the partitions of the high- and middle-ranking genealogies. These findings suggest that differential reproductive success is influenced and maintained by underlying variations in the distribution of behavioral traits in the population.     

Postnatal ontogenetic size and shape changes in the craniums of plateau pika and woolly hare(Mammalia: Lagomorpha)

In the present study, postnatal ontogenetic size and shape changes in the cranium of two lagomorph species, the plateau pika(Ochotona curzoniae) and woolly hare(Lepus oiostolus), were investigated by geometric morphometrics. The ontogenetic size and shape changes of their cranium exhibited different growth patterns in response to similar environmental pressures on the Qinghai-Tibetan Plateau. The overall size change in the cranium of the plateau pika was slower than that of the woolly hare. The percentage of ontogenetic shape variance explained by size in the woolly hare was greater than that in the plateau pika. The overall shape of the cranium was narrowed in both species, and morphological components in relation to neural maturity showed negative allometry, while those responsible for muscular development showed isometric or positive allometry. The most remarkable shape variations in the plateau pika were associated with food acquisition(temporalis development), though other remarkable shape variations in the incisive and palatal foramen in the ventral view were also observed. The most important shape change in the woolly hare was demonstrated by the elongation of the nasal bones, expansion of the supra-orbital process and shape variation of the neurocranium.     

Sociometrics of Macaca mulatta: II. Decoupling centrality and dominance in rhesus monkey social networks

The concept of the linear dominance hierarchy and a much less precise notion of a central/peripheral ordering of individuals have been prominent among the ideas about social organization of monkey groups. Although the latter has seldom been quantified, the ranks of individuals in the two orders are usually assumed to be correlated. This paper reports on a longitudinal study of a free-ranging group of rhesus monkeys. The individual histories of progression of dominance rank and an independently determined measure of centrality in the social grooming network are compared among a set of males. Centrality is not a static correlate of dominance rank as implied by the findings of short-term studies. Rather, centrality is a more sensitive indicator of status than is dominance rank, to which it is related in a dynamic fashion. Small changes in dominance rank may be followed by large changes in centrality. An increase in centrality may facilitate rise in dominance rank. These findings suggest a complex psychology of status, rather than a simple causative relation between the two variables.     

Proceedings of the fifty-fourth Annual Meeting of the American Association of physical anthropologists to be held in Knoxville,Tennessee—Holiday Inn World's fair April 10–13, 1985

Empirical analyses and models of the lineal effects of fission indicate that considerable genetic differentiation may occur at the time of group formation, thus confusing the usual positive relationship between historical affiliation and genetic differentiation. We analyze the effects of fission pattern on variation in highly heritable morphological traits among eight social groups on Cayo Santiago. The analysis is performed using general network autocorrelation methods that quantitatively and directly measure the amount of variation in social group mean morphology that can be explained by fission. All of the fission autocorrelation coefficients are strongly negative, indicating that groups most recently formed by fission are most dissimilar. Also, most of the variation between groups can be explained by the fission pattern, indicating that lineal fission is the most important process generating between-group variation on Cayo Santiago.     

The evolution of static allometry in sexually selected traits

Although it has been the subject of verbal theory since Darwin, the evolution of morphological trait allometries remains poorly understood, especially in the context of sexual selection. Here we present an allocation trade-off model that predicts the optimal pattern of allometry under different selective regimes. We derive a general solution that has a simple and intuitive interpretation and use it to investigate several examples of fitness functions. Verbal arguments have suggested cost or benefit scenarios under which sexual selection on signal or weapon traits may favor larger individuals with disproportionately larger traits (i.e., positive allometry). However, our results suggest that this is necessarily true only under a precisely specified set of conditions: positive allometry will evolve when the marginal fitness gains from an increase in relative trait size are greater for large individuals than for small ones. Thus, the optimal allometric pattern depends on the precise nature of net selection, and simple examples readily yield isometry, positive or negative allometry, or polymorphisms corresponding to sigmoidal scaling. The variety of allometric patterns predicted by our model is consistent with the diversity of patterns observed in empirical studies on the allometries of sexually selected traits. More generally, our findings highlight the difficulty of inferring complex underlying processes from simple emergent patterns.     

Intersexual allometry differences and ontogenetic shifts of coloration patterns in two aquatic turtles,Graptemys oculifera and Graptemys flavimaculata

Coloration can play critical roles in a species' biology. The allometry of color patterns may be useful for elucidating the evolutionary mechanisms responsible for shaping the traits. We measured characteristics relating to eight aspects of color patterns from Graptemys oculifera and G. flavimaculata to investigate the allometric differences among male, female, and unsexed juvenile specimens. Additionally, we investigated ontogenetic shifts by incorporating the unsexed juveniles into the male and female datasets. In general, male color traits were isometric (i.e., color scaled with body size), while females and juvenile color traits were hypoallometric, growing in size more slowly than the increase in body size. When we included unsexed juveniles in our male and female datasets, our linear regression analyses found all relationships to be hypoallometric and our model selection analysis found support for nonlinear models describing the relationship between body size and color patterns, suggestive of an ontogenetic shift in coloration traits for both sexes at maturity. Although color is critical for many species' biology and therefore under strong selective pressure in many other species, our results are likely explained by an epiphenomenon related to the different selection pressures on body size and growth rates between juveniles and adults and less attributable to the evolution of color patterns themselves.     

Quantitative genetics of skeletal nonmetric traits in the rhesus macaques on Cayo Santiago. II. Phenotypic,genetic, and environmental correlations between traits

The general lack of phenotypic correlation among skeletal nonmetric traits has been interpreted as indicating a lack of genetic correlation among these traits. Nonmetric traits scored on animals in the skeletal collection of rhesus macaques from Cayo Santiago are used to calculate phenotypic, genetic, and environmental correlations between traits. The results show that even when phenotypic correlations are low, there may be large, significant genetic correlations among these traits. The genetic correlation pattern suggests that genes which affect nonmetric trait variation act primarily at a local level in the cranium, even though there are genes with pleiotropic effects on skeletal nonmetric traits throughout the cranium. Environmental and phenotypic correlations do not show this neighborhood pattern of correlation.     

Social group fission and the origin of intergroup genetic differentiation among the rhesus monkeys of Cayo Santiago.

The serum transferrin locus is used to investigate the roles of the lineal effect of fission, male migration effect of fission, and genetic drift in causing intergroup genetic differentiation among the rhesus macaques of Cayo Santiago. These three mechanisms prove sufficient to explain the degrees of differentiation between the newly formed social groups A, K, and L as of July 1, 1971. The lineal effect of fission provides a baseline of intergroup differentiation which is altered by forces leading to intragroup genetic change, the male migration effect and genetic drift. The importance of population dynamics for the distribution of alleles among subgroups of a population is recognized.     

Skull allometry in the marine toad,Bufo marinus

Scaling predictions pioneered by A.V. Hill state that isometric changes in kinematics result from isometric changes in size. These predictions have been difficult to support because few animals display truly isometric growth. An exception to this rule is said to be the toads in the genus Bufo, which can grow over three orders of magnitude. To determine whether skull shape increases isometrically, I used linear measurements and geometric morphometrics to quantify shape variation in a size series of 69 skulls from the marine toad, B. marinus. Toads ranged in body mass from 1.8 gm to a calculated 1,558.9 gm. Of all linear measurements (S/V length, skull width, skull length, levator mass, depressor mass, adductor foramen area), only the area of the adductor foramen increased faster than body mass; the remaining variables increased more slowly. In addition, modeling the lower jaw as a lever‐arm system showed that the lengths of the closing in‐ and out‐levers scaled isometrically with body mass despite the fact that the skull itself is changing allometrically. Geometric morphometrics discerned areas of greatest variability with increasing body mass at the rear of the skull in the area of the squamosal bone and the adductor foramen. This increase in area of the adductor foramen may allow more muscle to move the relatively greater mass of the lower jaw in larger toads, although adductor mass scales with body mass. If B. marinus feeds in a similar manner to other Bufo, these results imply that morphological allometry may still result in kinematic isometry. J. Morphol. 241:115–126, 1999. © 1999 Wiley‐Liss, Inc.     

A four-year study of the association between male dominance rank, residency status, and reproductive activity in rhesus macaques (Macaca mulatta)

Considerable controversy exists on the nature of the relationship between male dominance rank and reproductive activity. The nature of this relationship has important implications for understanding the manner in which males compete for access to limited resources. Behavioral data on mating patterns were collected over a four-year period from one social group of rhesus macaques on Cayo Santiago. Correlations between dominance rank and reproductive activity were not stable over a four-year period, but changed yearly. Positive, significant correlations were present in the first two years of the study while non-significant correlations were found in the second two years. The variation found in the correlations between rank and mating activity could be accounted for by changes in the mating frequencies of different classes of males. The long-term resident males had declines in ejaculation frequencies over the duration of the study. Males who immigrated into the group had yearly increases in reproductive behavior over three consecutive years. Maturing natal males also increased their levels of reproductive activity from year-to-year. Combining these mating patterns over time resulted in shifting the proportions of matings away from the long-term residents and in favor of the new males. High-ranking males had an advantage in reproductive activity over the first two years of the study, as measured by both the total number of ejaculations and the mean number of ejaculation per male. New males, comprised of recent immigrants and maturing natal males, had a greater level of reproductive activity over the last two years. These results suggest that the effect of rank on reproductive activity is variable and that males utilize alternative tactics to attain access to limited resources. Simple one-factor models explaining the relationship between rank and reproductive activity must be replaced with models explaining how alternate strategies affect male competition and reproductive success in primates.     

Sexual dimorphism and allometry in primate ossa coxae

Five measurements were taken on the ossa coxae of 454 adult primates representing Ceboidea, Cercopithecoidea and Hominoidea. Sex differences in these variables and their relationships to overall body size and sexual dimorphism were tested by means of Student's t-test and regression analysis. The study attempts to clarify the nature of primate pelvic sexual dimorphism, including allometric effects, and more specifically, test the assertion made by Mobb and Wood (1977) that sexual dimorphism in body size in not an important determinant in pelvic sex differences. Variables that contribute to the size of the birth canal tend to be larger in females than males in all taxa studied except two. In these, Hylobates and Alouatta, there were no significant differences between the sexes for any of the five variables. In general, sexual dimorphism in variables contributing to the size of the birth canal was correlated (r ? 0.8) with sexual dimorphism in body size. Furthermore, the coefficients of allometry underlying pelvic sex differences were shown to be moderately correlated (r ? 0.5) with sexual dimorphism in size. The influence of other adaptive factors on primate pelvic sexual dimorphism are also briefly discussed.     

The hemogram,serum biochemistry,and electrolyte profile of the free-ranging Cayo Santiago rhesus macaques (Macaca mulatta)

Sixty-four male and 33 female free-ranging rhesus monkeys (Macaca mulatta) from one of six social groups on the island of Cayo Santiago, Puerto Rico, were surveyed to establish normal values for the hemogram and serum biochemical and electrolytes for the colony. Mean values (± 1 SD) are reported by sex for each of three age groups (2–3, 4–9 and ≥ 10 years). All adult females (≥ 4 years) were pregnant. There were significant differences for a number of variables compared to the range reported in the existing literature, and among the age and sex groups in the sampled population.     

Spatial scaling of allometry for terrestrial,mammalian carnivores

A regression slope of –0.75 between log₁₀ density and log₁₀ body mass is thought to express equivalence of energy conversion among species' populations of similar taxonomic and trophic status. Using larger sample sizes than the usual 1–3 density estimates per species, we estimated a regression slope of –0.71 for terrestrial mammalian carnivores. We investigated the sampling variation in this estimate, and those derived from smaller intra-specific subsets, using 1000-iteration bootstrap analyses to obtain 90% confidence intervals. As expected, these widened as random subsets were reduced in size, but always contained the postulated –0.75. However, log₁₀ density also declined as 3/4 of the log₁₀ spatial extent of study area, and study area accounted for virtually all of the variation in density that was previously thought due to body mass. We removed the effect of study area by using the species-specific regression models between density and study area to predict density at a common scale of 400 km². These common-scale densities regressed against body mass with a slope of –0.16, but separated into body mass classes less than and greater than 11 kg, they produced slopes that were not significantly different from zero. We show that the allometry of density could be a case of circular logic, whereby body mass has influenced the investigator's choice of study area, and the resulting scale-dependent densities are related back to body mass. To test the allometry hypothesis, the effect of study area on density estimates needs to be removed. This requires conducting larger-scale studies of the smaller-bodied species so that all species compared are represented by an average study area that is near the common scale. Furthermore, study sites need to be selected and designed to represent more than the local detail in species' density.     

Epiphyseal union and dental eruption in Macaca mulatta

Age of dental eruption and epiphyseal fusion is estimated for the permanent dentition and long bone epiphyses of rhesus macaques (Macaca mulatta), with 299 skeletons of individuals with known age of death, from the Cayo Santiago skeletal collection. Epiphyses at a given joint tend to fuse at the same time. While males and females tend to have the same pattern of epiphyseal fusion, females' epiphyses fuse earlier than those of males, espeically at the elbow and knee joints. The order of epiphyseal fusion in rhesus macaques follows the general primate pattern. Times of dental eruption for males and females are generally the same, except for the relatively late eruption of the canine in the males. The order of eruption follows a common primate pattern (dm2?M1?I1?I2?M2?(P3,P4)?C?M3). Multiple regressions were calculated in order to allow determination of developmental state, or predictions of chronological age, from epiphyseal fusion and/or dental eruption scores in juvenile rhesus macaques. Standard deviations of residuals from these regressions indicate considerable variation in developmental state among aminals of the same chronological age. The lack of correlation between residuals from the separate skeletal and dental regressions, indicates that skeletal and dental development are largely independent.     

Age- and gender-related changes in body size, adiposity, and endocrine and metabolic parameters in free-ranging rhesus macaques.

Normative age- and gender-related changes in body composition, serum lipids, testosterone, and insulin-like growth factor (IGF-1) were examined in the Cayo Santiago free-ranging rhesus macaques. In both adult males and females, body weights, crown-rump lengths, and circumference of the limbs were lowest in the oldest group (20+ years of age) as compared with other adult age classes. Body fat, as reflected in subcutaneous fatfold thickness and waist/thigh ratios, were higher in adult females than adult males. This gender dimorphism was first detectable among the 6-9 year old age group. Greatest body fat among females was observed in the 10-14 age group, whereas in males the highest values were observed in the 15-19 age group. Differences in body composition were also observed with respect to reproductive status. Although there were no gender differences in overall cholesterol levels, there were age-related differences between males and females, and only in males were cholesterol values positively related to adiposity. There were no age- or gender-related differences in triglyceride values, but levels were significantly higher in pregnant females in comparison with other reproductive states. Levels of testosterone were not significantly related to any morphometric parameter and values did not decrease significantly with age. Levels of IGF-1 exhibited a significant age-related decrease among adult males, and females had higher levels independent of age. The similarities between the present findings and human studies suggest that further studies in the free-ranging rhesus macaques would provide a bridge between studies of laboratory-housed primates and studies of human beings with respect to the etiology of obesity and life-history changes in body composition and endocrine and metabolic parameters.