OBJECTIVE Early life interindividual variation in hypothalamic-pituitary-adrenal (HPA) reactivity to stress is predictive of later life psychological and physical well-being, including the development of many pathological syndromes that are often sex-biased. A complex and interactive set of environmental and genetic causes for such variation has been implicated by previous studies, though little attention has been paid to nonadditive effects (e.g. dominance, X-linked) or sex-specific genetic effects. METHOD We used a large pedigreed sample of captive 3-4 months old infant rhesus macaques (N = 2,661, 54% female) to fit univariate and multivariate linear mixed quantitative genetic models for four longitudinal blood cortisol samples and three reliable ratings of infant temperament (nervousness, gentleness, confidence) during a mother-infant separation protocol. RESULTS Each trait had a moderate narrow-sense heritability (h², 0.26-0.46), but dominance effects caused the first two cortisol samples to have much larger broad-sense heritabilities (H², 0.57 and 0.77). We found no evidence for X-linked variance or common maternal environment variance. There was a sex difference in heritability of the first cortisol sample (hf² < hm²), suggesting differing genetic architecture of perception of maternal separation and relocation during infancy. Otherwise, genetic covariance matrices for the sexes were very similar. Genetic correlations between cortisol levels and temperament were weak (< |0.4|) but stronger than residual or phenotypic correlations. CONCLUSIONS HPA reactivity and temperament had a primarily additive genetic basis in infant macaques, but there were important complexities to the genetic architecture of including genetic dominance and sex differences in heritability at this early life stage. (PsycInfo Database Record (c) 2021 APA, all rights reserved).
Recent studies have shown that global variation in body proportions is more complex than previously thought as some traits formerly associated with climate adaptation are better explained by geographic proximity and neutral evolutionary forces. While the recent incorporation of quantitative genetic methodologies has improved understanding of patterns related to climate in Africa, Europe, and the Americas, Asia remains underrepresented in recent and historic studies of body form. As ecogeographic studies tend to focus on male morphology, potential sex differences in features influenced by climate remain largely unexplored. Skeletal measurements encompassing the dimensions of the skull, pelvis, limbs, hands, and feet were collected from male (n = 459) and female (n = 442) remains curated in 13 collections across seven countries in East Asia (n = 901). Osteological data were analyzed with sex and minimum temperature as covariates adjusted by autosomal single-nucleotide polymorphism population genetic distance using univariate Bayesian linear mixed models, and credible intervals were calculated for each trait. Analysis supports a relationship between specific traits and climate as well as providing the magnitude of response in both sexes. After accounting for genetic distance between populations, greater association between climate and morphology was found in postcranial traits, with the relationship between climate and the skull limited primarily to breadth measurements. Larger body size is associated with colder climates with most measurements increasing with decreased temperature. The same traits were not always associated with climate for males and females nor correlated with the same intensity for both sexes. The varied directional association with climate for different regions of the skeleton and between the sexes underscores the necessity of future ecogeographic research to holistically evaluate body form and to look for sex-specific patterns to better understand population responses to environmental stresses.
Abstract Organisms use color for camouflage, sexual signaling, or as a warning sign of danger. Primates are one of the most vibrantly colored Orders of mammals. However, the genetics underlying their coat color are poorly known, limiting our ability to study molecular aspects of its evolution. The role of the melanocortin 1 receptor (MC1R) in color evolution has been implicated in studies on rocket pocket mice (Chaetodipus intermediusi), toucans (Ramphastidae), and many domesticated animals. From these studies, we know that changes in MC1R result in a yellow/red or a brown/black morphology. Here, we investigate the evolution of MC1R in Lorisidae, a monophyletic nocturnal primate family, with some genera displaying high contrast variation in color patterns and other genera being monochromatic. Even more unique, the Lorisidae family has the only venomous primate: the slow loris (Nycticebus). Research has suggested that the contrasting coat patterns of slow lorises are aposematic signals for their venom. If so, we predict the MC1R in slow lorises will be under positive selection. In our study, we found that Lorisidae MC1R is under purifying selection (ω = 0.0912). In Lorisidae MC1R, there were a total of 75 variable nucleotides, 18 of which were nonsynonymous. Six of these nonsynonymous substitutions were found on the Perodicticus branch, which our reconstructions found to be the only member of Lorisidae that has predominantly lighter coat color; no substitutions were associated with Nycticebus. Our findings generate new insight into the genetics of pelage color and evolution among a unique group of nocturnal mammals and suggest putative underpinnings of monochromatic color evolution in the Perodicticus lineage.
The Caribbean is a genetically diverse region with heterogeneous admixture compositions influenced by local island ecologies, migrations, colonial conflicts, and demographic histories. The Commonwealth of Dominica is a mountainous island in the Lesser Antilles historically known to harbor communities with unique patterns of migration, mixture, and isolation. This community-based population genetic study adds biological evidence to inform post-colonial narrative histories in a Dominican horticultural village. High density single nucleotide polymorphism data paired with a previously compiled genealogy provide the first genome-wide insights on genetic ancestry and population structure in Dominica. We assessed family-based clustering, inferred global ancestry, and dated recent admixture by implementing the fastSTRUCTURE clustering algorithm, modeling graph-based migration with TreeMix, assessing patterns of linkage disequilibrium decay with ALDER, and visualizing data from Dominica with Human Genome Diversity Panel references. These analyses distinguish family-based genetic structure from variation in African, European, and indigenous Amerindian admixture proportions, and analyses of linkage disequilibrium decay estimate admixture dates 5–6 generations (~160 years) ago. African ancestry accounts for the largest mixture components, followed by European and then indigenous components; however, our global ancestry inferences are consistent with previous mitochondrial, Y chromosome, and ancestry marker data from Dominica that show uniquely higher proportions of indigenous ancestry and lower proportions of African ancestry relative to known admixture in other French- and English-speaking Caribbean islands. Our genetic results support local narratives about the community’s history and founding, which indicate that newly emancipated people settled in the steep, dense vegetation along Dominica’s eastern coast in the mid-19 th century. Strong genetic signals of post-colonial admixture and family-based structure highlight the localized impacts of colonial forces and island ecologies in this region, and more data from other groups are needed to more broadly inform on Dominica’s complex history and present diversity.
OBJECTIVES:Body size and composition vary widely among individuals and populations, and long-term research in diverse contexts informs our understanding of genetic, cultural, and environmental impacts on this variation. We analyze longitudinal measures of height, weight, and body mass index (BMI) from a Caribbean village, estimating the extent to which these anthropometrics are shaped by genetic variance in a small-scale population of mixed ancestry.MATERIALS AND METHODS:Longitudinal data from a traditionally horticultural village in Dominica document height and weight in a non-Western population that is transitioning to increasingly Westernized lifestyles, and an 11-generation pedigree enables us to estimate the proportions of phenotypic variation in height, weight, and BMI attributed to genetic variation. We assess within-individual variation across growth curves as well as heritabilities of these traits for 260 individuals using Bayesian variance component estimation.RESULTS:Age, sex, and secular trends account for the majority of anthropometric variation in these longitudinal data. Independent of age, sex, and secular trends, our analyses show high repeatabilities for the remaining variation in height, weight, and BMI growth curves (>0.75), and moderate heritabilities (h2height = 0.68, h2weight = 0.64, h2BMI = 0.49) reveal clear genetic signals that account for large proportions of the variation in body size observed between families. Secular trends show increases of 6.5% in height and 16.0% in weight from 1997 to 2017.DISCUSSION:This horticultural Caribbean population has transitioned to include more Westernized foods and technologies over the decades captured in this analysis. BMI varies widely between individuals and is significantly shaped by genetic variation, warranting future exploration with other physiological correlates and associated genetic variants.
OBJECTIVES:Ratios of weight to height, especially body mass index (BMI = kg/m2 ), are often used in epidemiological and genetic studies of health, but the limitations of quantitative genetic analysis of ratios are not widely known. The heritability of these ratios can be closely approximated from a bivariate quantitative genetic model of weight and height which clarifies how BMI heritabilities change.METHODS:I explored this bivariate approximation and alternative measures through simulated datasets fit with linear mixed models. Simulated data were based on published heritabilities and other statistics for BMI and related anthropometric dimensions from four human samples.RESULTS:Inspection of the bivariate approximation and analysis of simulated data show the heritability of weight/height crucially depends on the phenotypic (rP ) and genetic correlations (rA ) between weight and height. Changes in these correlations can have dramatic effects on the heritability of BMI. For example, when rP ≪ rA heritability of BMI is reduced to 35-50% of its value when the correlations are equal.DISCUSSION:Increasing adiposity likely decreases the phenotypic correlations more than the genetic correlation resulting in reduced heritability of the ratio. This contrasts with the commonly reported stability or increase of BMI heritability and implies it may result from increased genetic variance in weight in obesogenic environments. The bivariate model offers other advantages over ratios, including estimating the conditional genetic variance or heritability of weight that is unassociated with height, which may prove useful in quantitative and molecular genetic studies.
Background Milk is a complicated chemical mixture often studied through macronutrient concentrations of fat, protein, and sugar. There is a long-standing natural history tradition describing interspecific diversity in these concentrations. However, recent work has shown little influence of ecological or life history variables on them, aside from maternal diet effects, along with a strong phylogenetic signal. Methods I used multivariate phylogenetic comparative methods to revisit the ecological and life history correlates of milk macronutrient composition and elaborate on the nature of the phylogenetic signal using the phylogenetic mixed model. I also identified clades with distinctive milks through nonparametric tests (KSI) and PhylogeneticEM evolutionary modeling. Results In addition to the previously reported diet effects, I found increasingly aquatic mammals have milk that this is lower in sugar and higher in fat. Phylogenteic heritabilities for each concentration were high and phylogenetic correlations were moderate to strong indicating coevolution among the concentrations. Primates and pinnipeds had the most outstanding milks according to KSI and PhylogeneticEM, with perissodactyls and marsupials as other noteworthy clades with distinct selection regimes. Discussion Mammalian milks are diverse but often characteristic of certain higher taxa. This complicates identifying the ecological and life history correlates of milk composition using common phylogenetic comparative methods because those traits are also conservative and clade-specific. Novel methods, careful assessment of data quality and hypotheses, and a “phylogenetic natural history” perspective provide alternatives to these traditional tools.
Extensive phylogenetic studies have found robust phylogenies are modeled by using a mull-gene approach and sampling from the majority of the taxa of interest. Yet, molecular studies focused on the lorises, a cryptic primate family, have often relied on one gene, or just mitochondrial DNA, and many were unable to include all four genera in the analyses, resulting in inconclusive phylogenies. Past phylogenetic loris studies resulted in lorises being monophyletic, paraphyletic, or an unresolvable trichotomy with the closely related galagos. The purpose of our study is to improve our understanding of loris phylogeny and evolutionary history by using a multi-gene approach. We used the mitochondrial genes cytochrome b, and cytochrome c oxidase subunit 1, along with a nuclear intron (recombination activating gene 2) and nuclear exon (the melanocortin 1 receptor). Maximum Likelihood and Bayesian phylogenetic analyses were conducted based on data from each locus, as well as on the concatenated sequences. The robust, concatenated results found lorises to be a monophyletic family (Lorisidae) (PP >= 0.99) with two distinct subfamilies: the African Perodictinae (PP >= 0.99) and the Asian Lorisinae (PP >= 0.99). Additionally, from these analyses all four genera were all recovered as monophyletic (PP >= 0.99). Some of our single-gene analyses recovered monophyly, but many had discordances, with some showing paraphyly or a deep-trichotomy. Bayesian partitioned analyses inferred the most recent common ancestors of lorises emerged similar to 42 +/- 6 million years ago (mya), the Asian Lorisinae separated similar to 30 +/- 9 mya, and Perodictinae arose similar to 26 +/- 10 mya. These times fit well with known historical tectonic shifts of the area, as well as with the sparse loris fossil record. Additionally, our results agree with previous mull-gene studies on Lorisidae which found lorises to be monophyletic and arising similar to 40 mya (Perelman el al., 2011; Pozzi el al., 2014). By taking a mull-gene approach, we were able to recover a well-supported, monophyletic loris phylogeny and inferred the evolutionary history of this cryptic family.
Evolutionary allometry describes size and shape differences across taxa matched for developmental stage (e.g., adulthood). Allometric studies can identify subtle differences among species, and therefore help researchers interested in small-bodied, cryptic species such as tarsiers. Recent taxonomic revision has emphasized size differences among three possible tarsier genera inhabiting different island regions: Sulawesi (genus: Tarsius), Borneo (genus: Cephalopachus), and the Philippines (genus: Carlito). We examined seven craniodental measures of 102 museum specimens of adult tarsiers representing these three regions. We found that the allometric patterns within groups do not predict the observable differences among groups. Crania of the largest-bodied genus, Cephalopachus, are characterized by relatively short skulls and small orbits, with wider palates and molars than predicted by allometric increase from the smaller-bodied Tarsius. Overall, we found tarsier skulls stay the same shape as they increase in size. This may reflect shared developmental and biomechanical adaptations across tarsier groups filling an extreme leaping, faunivorous niche with hypertrophied orbits and subtle dietary differences in prey selection. These shared adaptations of tarsiers may severely limit the range of body sizes in tarsiers and impose further constraints on cranial shape. Despite their deep divergence times in the Miocene, living tarsier groups are united by a common craniodental form across a limited size range. Adaptations to extreme niches might result in a hyperconservatism of the cranium. Future primate allometric studies should explore cranial variation in other taxa to determine how adaptations to specific niches affect the size and shape of the cranium.
Uncovering sources of variation in gorilla infant mortality informs conservation and life history research efforts. The international studbook for the western lowland gorilla provides information on a sample of captive gorillas large enough for which to analyze genetic, maternal, and various other effects on early life mortality in this critically endangered species. We assess the importance of variables such as sex, maternal parity, paternal age, and hand rearing with regard to infant survival. We also quantify the proportions of variation in mortality influenced by heritable variation and maternal effects from these pedigree and survival data using variance component estimation. Markov chain Monte Carlo simulations of generalized linear mixed models produce variance component distributions in an animal model framework that employs all pedigree information. Two models, one with a maternal identity component and one with both additive genetic and maternal identity components, estimate variance components for different age classes during the first 2 years of life. This is informative of the extent to which mortality risk factors change over time during gorilla infancy. Our results indicate that gorilla mortality is moderately heritable with the strongest genetic influence just after birth. Maternal effects are most important during the first 6 months of life. Interestingly, hand-reared infants have lower mortality for the first 6 months of life. Aside from hand rearing, we found other predictors commonly used in studies of primate infant mortality to have little influence in these gorilla data. Am. J. Primatol. 77:666–678, 2015. © 2015 Wiley Periodicals, Inc.
Increasingly, behavioral ecologists have applied quantitative genetic methods to investigate the evolution of behaviors in wild animal populations. The promise of quantitative genetics in unmanaged populations opens the door for simultaneous analysis of inheritance, phenotypic plasticity, and patterns of selection on behavioral phenotypes all within the same study. In this article, we describe how quantitative genetic techniques provide studies of the evolution of behavior with information that is unique and valuable. We outline technical obstacles for applying quantitative genetic techniques that are of particular relevance to studies of behavior in primates, especially those living in noncaptive populations, e.g., the need for pedigree information, non-Gaussian phenotypes, and demonstrate how many of these barriers are now surmountable. We illustrate this by applying recent quantitative genetic methods to spatial proximity data, a simple and widely collected primate social behavior, from adult rhesus macaques on Cayo Santiago. Our analysis shows that proximity measures are consistent across repeated measurements on individuals (repeatable) and that kin have similar mean measurements (heritable). Quantitative genetics may hold lessons of considerable importance for studies of primate behavior, even those without a specific genetic focus.
Offspring size is often an intimate link between the fitness of parents and offspring. Among mammals, neonate mass is also related to adult levels of dimorphism and intrasexual competitive mating. We describe the sex-specific genetic architecture of neonate mass in captive squirrel monkeys (Saimiri boliviensis), a small Neotropical primate. Best fitting quantitative genetic models show strong maternal genetic effects with little difference between sexes offering limited opportunity for neonatal dimorphism to respond to observed or hypothetical selection. Heritabilities that are approximately zero also imply it is unlikely that neonatal dimorphism can evolve as a correlated response to selection on adult size. However, male mass is also more dependent on maternal condition (age and parity) making dimorphism plastic. Finally, we hypothesize that large maternal genetic effects reflect income breeding and tightly synchronized seasonal reproduction in squirrel monkeys, both of which require strong maternal control of offspring growth and timing of birth.
The genetics of primate life histories are poorly understood, but quantitative genetic patterns in other mammals suggest phenotypic differences among individuals early in life can be strongly affected by interactions with mothers or other caretakers. I used generalized linear mixed model extensions of complex pedigree quantitative genetic techniques to explore regression coefficients and variance components for infant and juvenile mortality rates across prereproductive age classes in the semifree ranging Cayo Santiago rhesus macaques. Using a large set of records (maximum n = 977 mothers, 6,240 offspring), strong maternal effects can be identified early in development but they rapidly “burn off” as offspring age and mothers become less consistent buffers from increasingly prominent environmental variation. The different ways behavioral ecologists and animal breeders have defined and studied maternal effects can be subsumed, and even blended, within the quantitative genetic framework. Regression coefficients identify loss of the mother, maternal age, and offspring age within their birth cohort as having significant maternal effects on offspring mortality, while variance components for maternal identity record significant maternal influence in the first month of life. Am. J. Primatol. 75:238‐251, 2013. © 2013 Wiley Periodicals, Inc.
The current study assessed the heritability of personality in a traditional natural-fertility population, the Ache of eastern Paraguay. Self-reports (n = 110) and other-reports (n = 66) on the commonly used Big Five Personality Inventory (i.e., extraversion, agreeableness, conscientiousness, neuroticism, openness) were collected. Self-reports did not support the Five Factor Model developed with Western samples, and did not correlate with other-reports for three of the five measured personality factors. Heritability was assessed using factors that were consistent across self-and other-reports and factors assessed using other-reports that showed reliabilities similar to those found in Western samples. Analyses of these items in combination with a multi-generation pedigree (n = 2,132) revealed heritability estimates similar to those found in most Western samples, although we were not able to separately estimate the influence of the common environment on these traits. We also assessed relations between personality and reproductive success (RS), allowing for a test of several mechanisms that might be maintaining heritable variation in personality. Phenotypic analyses, based largely on other-reports, revealed that extraverted men had higher RS than other men, but no other dimensions of personality predicted RS in either sex. Mothers with more agreeable children had more children, and parents mated assortatively on personality. Of the evolutionary processes proposed to maintain variation in personality, assortative mating, selective neutrality, and temporal variation in selection pressures received the most support. However, the current study does not rule out other processes affecting the evolution and maintenance of individual differences in human personality.