Evolution of genetically correlated traits: tooth size and body size in baboons

Within a population, only phenotypic variation that is influenced by genes will respond to selection. Genes with pleiotropic effects are known to influence numerous traits, complicating our understanding of their evolution through time. Here we use quantitative genetic analyses to identify and estimate the shared genetic effects between molar size and trunk length in a pedigreed, breeding population of baboons housed at the Southwest National Primate Research Center. While crown area has a genetic correlation with trunk length, specific linear measurements yield different results. We find that variation in molar buccolingual width and trunk length is influenced by overlapping additive genetic effects. In contrast, mesiodistal molar length appears to be genetically independent of body size. This is the first study to demonstrate a significant genetic correlation between tooth size and body size in primates. The evolutionary implications are discussed.     

Genetic integration of molar cusp size variation in baboons

Many studies of primate diversity and evolution rely on dental morphology for insight into diet, behavior, and phylogenetic relationships. Consequently, variation in molar cusp size has increasingly become a phenotype of interest. In 2007 we published a quantitative genetic analysis of mandibular molar cusp size variation in baboons. Those results provided more questions than answers, as the pattern of genetic integration did not fit predictions from odontogenesis. To follow up, we expanded our study to include data from the maxillary molar cusps. Here we report on these later analyses, as well as inter‐arch comparisons with the mandibular data. We analyzed variation in two‐dimensional maxillary molar cusp size using data collected from a captive pedigreed breeding colony of baboons, Papio hamadryas, housed at the Southwest National Primate Research Center. These analyses show that variation in maxillary molar cusp size is heritable and sexually dimorphic. We also estimated additive genetic correlations between cusps on the same crown, homologous cusps along the tooth row, and maxillary and mandibular cusps. The pattern for maxillary molars yields genetic correlations of one between the paracone–metacone and protocone–hypocone. Bivariate analyses of cuspal homologues on adjacent teeth yield correlations that are high or not significantly different from one. Between dental arcades, the nonoccluding cusps consistently yield high genetic correlations, especially the metaconid–paracone and metaconid–metacone. This pattern of genetic correlation does not immediately accord with the pattern of development and/or calcification, however these results do follow predictions that can be made from the evolutionary history of the tribosphenic molar. Am J Phys Anthropol, 2010. © 2009 Wiley‐Liss, Inc.     

Heritability of age at first birth in captive olive baboons

The evolution of life history traits is a topic of growing interest in primatology. Traits associated with fertility, such as age at menarche and age at first birth, have great significance for natural selection, and knowing the genetic basis of such demographic traits may improve our understanding of population dynamics. Knowledge of the heritability of reproductive traits may also have practical implications for the management of captive breeding colonies. A maximum likelihood method was used to estimate heritability of age at first birth for a sample of female olive baboons resident at the Southwest Foundation for Biomedical Research. Only animals born at the Foundation that were caged in mixed sex groups and that had previously given birth were included in the sample (n = 316). There were 117 independent individuals and 199 individuals in 35 pedigrees composed of 2 to 26 members. Age at first birth ranged from 3.85 years to 13.11 years. Age at first birth is highly heritable (h² = 0.87) with no evidence for maternal effects or a dominance genetic component. This level of genetic variability in a fitness-related trait is contrary to evolutionary expectation and may reflect the uniform environment of a captive breeding situation. Thus, the heritability observed in this population may be taken as an upper bound for that in natural populations. © 1995 Wiley-Liss, Inc.     

Genetic correlations between mandibular molar cusp areas in baboons

Primate evolutionary studies rely significantly on dental variation given the large role that teeth play in how an organism interacts with its environment (animal and plant) and conspecifics. Variation in cusp size has been shown to vary among primate taxa, although most studies to date focused on extant and extinct hominoids. Here we test the assumed hypothesis that a significant proportion of this variation in baboons is due to the additive effects of genes. We perform quantitative genetic analyses on variation in two-dimensional (2-D) mandibular molar cusp size in a captive pedigreed breeding population of baboons (Papio hamadryas) from the Southwest National Primate Research Center. These analyses show that variation in cusp size is heritable and sexually dimorphic. Additionally, we tested for genetic correlations between cusps on the same crown, between morphological homologues along the tooth row, and between cusp area and crown buccolingual width. We find that four of the six cusp pairs on the first molar have a genetic correlation of one, save for the metaconid-hypoconid and entoconid-hypoconid, which are not statistically different from zero. The second and third molars have lower genetic correlations, although the metaconid-hypoconid correlation is similarly estimated at zero and the entoconid-protoconid correlation is estimated to be one. This cross pattern of genetic and no genetic correlation does not immediately accord with the known pattern of development and/or calcification. We propose two explanative hypotheses.     

Genetics and the evolution of primate enamel thickness: a baboon model

The thickness of mammalian tooth enamel plays a prominent role in paleontology because it correlates with diet, and thicker enamel protects against tooth breakage and wear. Hominid evolutionary studies have stressed the importance of this character for over 30 years, from the identification of "Ramapithecus" as an early Miocene hominid, to the recent discovery that the earliest hominids display molar enamel intermediate in thickness between extant chimpanzees and Australopithecus. Enamel thickness remains largely unexplored for nonhominoid primate fossils, though there is significant variation across modern species. Despite the importance of enamel thickness variation to primate evolution, the mechanisms underlying variation in this trait have not yet been elucidated. We report here on the first quantitative genetic analysis of primate enamel thickness, an analysis based on 506 pedigreed baboons from a captive breeding colony. Computed tomography analysis of 44 Papio mandibular molars shows a zone of sufficiently uniform enamel thickness on the lateral surface of the protoconid. With this knowledge, we developed a caliper metric measurement protocol for use on baboon molars worn to within this zone, enabling the collection of a data set large enough for genetic analyses. Quantitative genetic analyses show that a significant portion of the phenotypic variance in enamel thickness is due to the additive effects of genes and is independent of sex and tooth size. Our models predict that enamel thickness could rapidly track dietary adaptive shifts through geological time, thus increasing the potential for homoplasy in this character. These results have implications for analyses of hominoid enamel thickness variation, and provide a foundation from which to explore the evolution of this phenotype in the papionin fossil record.     

Testing the function of reconciliation and third-party affiliation for aggressors in hamadryas baboons (Papio hamadryas hamadryas)

In social groups, agonistic conflicts can have different negative consequences. Several post-conflict interactions have been suggested as post-conflict management behaviors to mitigate those negative effects. In this study, we investigated the function of two post-conflict behaviors--reconciliation and aggressor-initiated third-party affiliation--on the aggressor's levels of post-conflict anxiety and aggression in a large colony of hamadryas baboons. We also examined variation in the aggressor's levels of post-conflict anxiety as a function of relationship quality between the opponents as predicted by the Integrated Hypothesis. We found that after conflicts hamadryas baboon aggressors showed increased rates of anxiety-related behaviors and that they were also more likely to be involved in renewed aggressive interactions. Although both reconciliation and aggressor-initiated third-party affiliation reduced the probability of receiving post-conflict aggression, only reconciliation reduced the rates of anxiety-related behaviors, suggesting that the aggressors' post-conflict anxiety might be owing mainly to the damage that the conflict causes to their relationship with the victim. Furthermore, aggressor's rates of post-conflict anxiety were higher after conflicts with individuals with whom they had a high-quality relationship, supporting the idea that levels of post-conflict anxiety mediate the occurrence of reconciliation depending on the quality of the relationship with former opponent as predicted by the Integrated Hypothesis.     

Microbial community analysis of rectal methanogens and sulfate reducing bacteria in two non-human primate species

Background  Methanogenesis by methanogenic Archaea and sulfate reduction by sulfate reducing bacteria (SRB) are the major hydrogenotrophic pathways in the human colon. Methanogenic status of mammals is suggested to be under evolutionary rather than dietary control. However, information is lacking regarding the dynamics of hydrogenotrophic microbial communities among different primate species.
Methods  Rectal swabs were collected from 10 sooty mangabeys ( Cercocebus atys ) and 10 baboons ( Papio hamadryas ). The diversity and abundance of methanogens and SRB were examined using PCR-denaturing gradient gel electrophoresis (DGGE) and real-time quantitative PCR (qPCR).
Results  The DGGE results revealed that intestinal Archaea and SRB communities differ between mangabeys and baboons. Phylogenetic analyses of Archaea DGGE bands revealed two distinct clusters with one representing a putative novel order of methanogenic Archaea. The qPCR detected a similar abundance of methanogens and SRB.
Conclusions  Intestinal Archaea and SRB coexist in these primates, and the community patterns are host species-specific.     

New methodology for measuring blood pressure in awake baboons with use of behavioral training techniques

Adult male baboons were behaviorally conditioned to extend an arm outside of the living cage and to accept repeated cuff inflations for manual auscultatory blood pressure measurements. Frequency distributions of systolic and diastolic blood pressure for both normotensive and renovascular hypertensive baboons generally were normally distributed. The procedure accurately tracked rapid changes in blood pressure after oral administration of antihypertensive drugs. Advantages over direct arterial cannulation for blood pressure measurement during extended, chronic experiments are discussed.     

Statistical genetics of molar cusp patterning in pedigreed baboons: implications for primate dental development and evolution

Gene expression and knock-out studies provide considerable information about the genetic mechanisms required for tooth organogenesis. Quantitative genetic studies of normal phenotypic variation are complementary to these developmental studies and may help elucidate the genes and mechanisms that contribute to the normal population-level phenotypic variation upon which selection acts. Here we present the first quantitative genetic analysis of molar cusp positioning in mammals. We analyzed quantitative measures of molar cusp position in a captive pedigreed baboon breeding colony housed at the Southwest National Primate Research Center in San Antonio, Texas. Our results reveal complete pleiotropy between antimeric pairs of traits--i.e., they are influenced by the same gene or suite of genes. Mandibular morphological homologues in the molar series also exhibit complete pleiotropy. In contrast, morphological homologues in maxillary molar series appear to be influenced by partial, incomplete pleiotropic effects. Variation in the mandibular mesial and distal molar loph orientation on the same molar crown is estimated to be genetically independent, whereas the maxillary molar mesial and distal loph orientation is estimated to have partially overlapping genetic affects. The differences between the maxillary and mandibular molar patterning, and the degree of genetic independence found between lophs on the same molar crown, may be indicative of previously unrecognized levels of modularity in the primate dentition.     

Heritability and genetic correlations of personality traits in a wild population of yellow‐bellied marmots (Marmota flaviventris)

Describing and quantifying animal personality is now an integral part of behavioural studies because individually distinctive behaviours have ecological and evolutionary consequences. Yet, to fully understand how personality traits may respond to selection, one must understand the underlying heritability and genetic correlations between traits. Previous studies have reported a moderate degree of heritability of personality traits, but few of these studies have either been conducted in the wild or estimated the genetic correlations between personality traits. Estimating the additive genetic variance and covariance in the wild is crucial to understand the evolutionary potential of behavioural traits. Enhanced environmental variation could reduce heritability and genetic correlations, thus leading to different evolutionary predictions. We estimated the additive genetic variance and covariance of docility in the trap, sociability (mirror image stimulation), and exploration and activity in two different contexts (open‐field and mirror image simulation experiments) in a wild population of yellow‐bellied marmots (Marmota flaviventris). We estimated both heritability of behaviours and of personality traits and found nonzero additive genetic variance in these traits. We also found nonzero maternal, permanent environment and year effects. Finally, we found four phenotypic correlations between traits, and one positive genetic correlation between activity in the open‐field test and sociability. We also found permanent environment correlations between activity in both tests and docility and exploration in the MIS test. This is one of a handful of studies to adopt a quantitative genetic approach to explain variation in personality traits in the wild and, thus, provides important insights into the potential variance available for selection.     

Taste difference thresholds for sucrose in two species of nonhuman primates

The purpose of this study was to determine taste difference thresholds for sucrose in frugivorous spider monkeys and omnivorous baboons. Using a two‐bottle preference test of brief duration, we presented four Ateles geoffroyi and four Papio hamdryas anubis with six different reference concentrations (RCs) of 25, 50, 100, 200, 300, and 400 mM sucrose and tested their ability to discriminate these from lower concentrations of this carbohydrate. The just noticeable differences (JNDs), expressed as Weber ratios (Δ/I), were found to range from 0.075–0.25 in the spider monkeys, with a tendency for lower values with higher Rcs. In contrast, the baboons showed the reverse trend, with the lowest Weber ratio of 0.10 at the two lowest Rcs and higher values of up to 0.25 with the highest RC tested. Thus, the JNDs were found to be generally similar in both species and at least as low as in humans. The results support the assumption that both spider monkeys and baboons may use sweetness as a criterion for food selection. The different patterns of differential sensitivity for sucrose across the range of concentrations tested suggest a correlation between the ability to discriminate between different concentrations of sucrose and the dietary habits of the two species. Am. J. Primatol. 48:153–160, 1999. © 1999 Wiley‐Liss, Inc.     

Correlational selection leads to genetic integration of body size and an attractive plumage trait in dark-eyed juncos

When a trait's effect on fitness depends on its interaction with other traits, the resultant selection is correlational and may lead to the integration of functionally related traits. In relation to sexual selection, when an ornamental trait interacts with phenotypic quality to determine mating success, correlational sexual selection should generate genetic correlations between the ornament and quality, leading to the evolution of honest signals. Despite its potential importance in the evolution of signal honesty, correlational sexual selection has rarely been measured in natural populations. In the dark-eyed junco (Junco hyemalis), males with experimentally elevated values of a plumage trait (whiteness in the tail or "tail white") are more attractive to females and dominant in aggressive encounters over resources. We used restricted maximum-likelihood analysis of a long-term dataset to measure the heritability of tail white and two components of body size (wing length and tail length), as well as genetic correlations between pairs of these traits. We then used multiple regression to assess directional, quadratic, and correlational selection as they acted on tail white and body size via four components of lifetime fitness (juvenile and adult survival, mating success, and fecundity). We found a positive genetic correlation between tail white and body size (as measured by wing length), which indicates past correlational selection. Correlational selection, which was largely due to sexual selection on males, was also found to be currently acting on the same pair of traits. Larger males with whiter tails sired young with more females, most likely due to a combination of female choice, which favors males with whiter tails, and male-male competition, which favors both tail white and larger body size. To our knowledge, this is the first study to show both genetic correlations between sexually selected traits and currently acting correlational sexual selection, and we suggest that correlational sexual selection frequently may be an important mechanism for maintaining the honesty of sexual signals.     

It takes two: Heritable male effects on reproductive timing but not clutch size in a wild bird population*

Within-population variation in the traits underpinning reproductive output has long been of central interest to biologists. Since they are strongly linked to lifetime reproductive success, these traits are expected to be subject to strong selection and, if heritable, to evolve. Despite the formation of durable pair bonds in many animal taxa, reproductive traits are often regarded as female-specific, and estimates of quantitative genetic variation seldom consider a potential role for heritable male effects. Yet reliable estimates of such social genetic effects are important since they influence the amount of heritable variation available to selection. Based on a 52-year study of a nestbox-breeding great tit (Parus major) population, we apply “extended” bivariate animal models in which the heritable effects of both sexes are modeled to assess the extent to which males contribute to heritable variation in seasonal reproductive timing (egg laying date) and clutch size, while accommodating the covariance between the two traits. Our analyses show that reproductive timing is a jointly expressed trait in this species, with (positively covarying) heritable variation for laydate being expressed in both members of a breeding pair, such that the total heritable variance is 50% larger than estimated by traditional models. This result was robust to explicit consideration of a potential male-biased environmental confound arising through sexually dimorphic dispersal. In contrast to laydate, males’ contribution to heritable variation in clutch size was limited. Our study thus highlights the contrasting extent of social determination for two major components of annual reproductive success, and emphasizes the need to consider the social context of what are often considered individual-level traits.     

A comparison of results obtained with two methods for assessing yield stability

Summary A major objective of the CIMMYT Maize Program is to develop open-pollinated varieties of maize (Zea mays L.) that are well adapted to a wide range of environments. To achieve this breeding goal, it is essential that the program use a stability technique that will identify high-yielding, stable genotypes accurately in international trials conducted under different environmental conditions. The objective of this study was to compare a spatial method with a modified conventional regression analysis method to determine the yield stability of 27 CIMMYT maize varieties evaluated at 37 locations. The methods also were compared on the basis of their consistency in assessing the stability of varieties when certain locations were omitted, and when subsets of varieties were analyzed. The varieties found to be stable by the spatial method with all sites included in the analysis were also stable (1) when the lowest and highest yielding sites were excluded from the analyses, and (2) when the varieties were considered, along with others, as a subset of the original group of materials. Stability parameters determined by regression analysis, however, varied for some varieties when (1) extreme sites were excluded, and (2) a subset of entries was considered in isolation. Because the spatial method was more consistent in identifying high-yielding stable varieties, it was considered the more useful of the two methods.     

The quantitative genetics of fluctuating asymmetry: a comparison of two models

The genetic basis of fluctuating asymmetry (FA), a measure of random deviations from perfect bilateral symmetry, has been the subject of much recent work. In this paper we compare two perspectives on the quantitative genetic analysis of FA and directional asymmetry (DA). We call these two approaches the character-state model and the environmental responsiveness model. In the former approach, the right and left sides are viewed as separate traits whose genetic coupling is manifested by the genetic correlation. This model leads to the relationship, h2(DA) = h2[(1-rA)/(1-rp)), where h2 is the heritability of each component trait (assumed to be the same), rA and rp are the genetic and phenotypic correlations between traits, respectively. Simulation shows that, under this model, the heritability of FA is considerably less than that of DA, except when heritabilities are very close to zero. The environmental responsiveness model permits genetic variance in FA even when the genetic correlation between traits is + 1. Simulation shows that under this model the heritability of FA can be uncoupled from that of DA. The additive and nonadditive components of the component (right and left) traits, their DA and FA values are estimated using a diallel cross of seven inbred lines of the sand cricket, Gryllus firmus. Four leg measurements were made and both the individual DA and FA values and the compound measures DASUM and CFA estimated. The heritabilities of the compound measures are slightly larger than the individual estimates. Dominance variance is observed in the individual traits but predicted to be an even smaller component of the phenotypic variance than the additive genetic variance. The estimated values confirm this, although a previous study has demonstrated that dominance variance is present. Because the heritabilities of FA are generally larger than those of DA, which never exceed 0.02, the environmental responsiveness model is more consistent with the data than the character-state model. A review of other data suggests that both sources of variation might be found in some species.