Gregory E. Blomquist

Trade-off between age of first reproduction and survival in a female primate.

Trade-offs are central to life-history theory but difficult to document. Patterns of phenotypic and genetic correlations in rhesus macaques, Macaca mulatta—a long-lived, slow-reproducing primate—are used to test for a trade-off between female age of first reproduction and adult survival. A strong positive genetic correlation indicates that female macaques suffer reduced adult survival when they mature relatively early and implies primate senescence can be explained, in part, by antagonistic pleiotropy. Contrasts with a similar human study implicate the extension of parental effects to later ages as a potential mechanism for circumventing female life-history trade-offs in human evolution.

Fitness-related patterns of genetic variation in rhesus macaques.

The patterning of quantitative genetic descriptions of genetic and residual variation for 15 skeletal and six life history traits was explored in a semi-free-ranging group of rhesus macaques (Macaca mulatta Zimmerman 1780). I tested theoretical predictions that explain the magnitude of genetic and residual variation as a result of 1. strength of a trait’s association with evolutionary fitness, or 2. developmental and physiological relationships among traits. I found skeletal traits had higher heritabilities and lower coefficients of residual variation than more developmentally and physiologically dependent life history traits. Total lifetime fertility had a modest heritability (0.336) in this population, and traits with stronger correlations to fitness had larger amounts of residual variance. Censoring records of poorly-performing individuals on lifetime fertility and lifespan substantially reduced their heritabilities. These results support models for the fitness-related patterning of genetic variation based on developmental and physiological relationships among traits rather than the action of selection eroding variation.

Rank-Related Fitness Differences and Their Demographic Pathways in Semi-Free-Ranging Rhesus Macaques ( Macaca mulatta )

Researchers have explored the fitness consequences of female dominance hierarchies in many primate populations, with most studies highlighting differences in age of maturation, fertility, and offspring survival. We use resampling techniques and van Tienderen’s (2000) elasticity path analysis to identify rank-related differences in finite rate of increase (λ) and their demographic correlates among segments of a semi-free-ranging rhesus macaque population. Higher-ranking population segments grew at greater rates for some portions of the 40-yr study period. The female members of these segments achieved these lifetime fitness differences through higher fertility and especially higher adult survival rates. This is the first clear evidence that social rank influences female primate adult survival, and is a crucial fitness component for any long-lived, slow-reproducing animal. Traditional methods of comparing lifespans, and other life history variables, among rank categories fail to identify most of the rank-related differences primarily because they require completed life histories that are available only on a small number of the females known in the population.

Heritability and Fitness Correlates of Personality in the Ache, a Natural-Fertility Population in Paraguay

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.

Maternal effects on offspring mortality in rhesus macaques (Macaca mulatta).

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.

Environmental and genetic causes of maturational differences among rhesus macaque matrilines

Females of many cercopithecine primates live in stable dominance hierarchies that create long-term asymmetries among sets of female relatives (matrilines) in access to limiting resources and shelter from psychosocial stress. Rank-related differences in fitness components are widely documented, but their causes are unclear. Predicted breeding values from an animal model for female age of first reproduction are used to discriminate between shared additive genetic and shared environmental effects among the members of matrilines in a population of free-ranging rhesus macaques (Macaca mulatta). While age of first reproduction has a modest heritability (≈0.2), breeding values are distributed in a largely random fashion among matrilines and contribute little to the observed rank-related differences in average age of first reproduction. These results support the long-held, but previously unverified, contention that rank-related life history differences in female cercopithecine primates are the result of environmental rather than genetic differences among them.

Brief communication: Methods of sequence heterochrony for describing modular developmental changes in human evolution.

Interest in the developmental changes leading to apomorphic features of human anatomy is longstanding. Although most research has focused on quantitative measures of size and shape, additional information may be available in the sequence of events in development, including aspects of phenotypic integration. I apply two recently proposed techniques for analyzing developmental sequences to literature data on human and chimpanzee age of limb element ossification center appearance in radiographs. The event-pair cracking method of Jeffery et al. (Syst Biol 51 [2002] 478-491) offers little additional insight on sequence differences in this data set than a simpler difference of ranks. Both reveal shifts in timing that are likely related to locomotor differences between the two species. Poes (Evolution 58 [2004] 1852-1855) test for modularity in a sequence identifies the ankle, wrist, and hind limb as developmental modules, which may correspond to localized combinations of developmental genes. Ossification patterns of the rays of the hand and foot show little modularity. Integrating these and other methods of sequence analysis with traditional metrics of size and shape remains an underdeveloped area of inquiry.

Applying Quantitative Genetic Methods to Primate Social Behavior

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.

Demographic and Morphological Perspectives on Life History Evolution and Conservation of New World Monkeys

As an order, primates are distinguished by several features of their life histories from other mammals. These include late achievement of sexual maturity, low female reproductive rates and potentially very long lives (Martin 1990). New World primates present a diverse array of life histories and social organizations (Ross 1991; Garber and Leigh 1997). In this chapter we explore primate life history variation relative to demography and development. We also note how an appreciation of life history and particularly the relations between life history, morphology, and demography can contribute solutions to vexing conservation problems. Our interest in these questions comes at a critical moment in life history theory because much of this body of theory is undergoing important revisions. The traditional theoretical viewpoint arranges primate taxa along a continuum of “fast vs. slow” life histories. Primates with “fast” life histories bear young over short gestation periods. These young have brief infant and juvenile periods to begin reproducing at small sizes and young ages. Following these fleeting stages, animals with “fast” life history expect short adult lifespans. A “slow” life history species manifests an opposing set of attributes, with long pre- and postnatal developmental periods, large adult size, with few but protracted reproductive events. This paradigm or general theory of life history has been extremely productive in characterizing variation across the primate order. However, recent studies reveal serious deficiencies with this idea in understanding important variation in growth patterns and life history variables (Pereira and Leigh 2003). Furthermore, we maintain that a perspective of “fast” versus “slow” life histories is a heuristic that, unfortunately, inhibits the investigation and understanding of important variation in primate life histories and demography. This idea also hinders development of effective conservation programs.

Female Age of First Reproduction at Cayo Santiago: Heritability and Shared Environments

Sexual maturation is a major transition in mammalian life histories including relatively long-lived, late-maturing primates. Age of first reproduction (AFR) in female primates is widely documented to vary among population members and to correlate with population density and social dominance. Research with Cayo Santiago macaques was among the first to identify these patterns. While explanations for variation in female AFR have centered around priority of access to limited resources and avoidance of stress, less attention has been drawn to potential genetic variation for AFR. Furthermore, the “dual inheritance” of genes and dominance rank in nepotistic female macaques implies these effects may be confounded. Heritability estimates for AFR at Cayo Santiago are small (≈0.15), but significantly greater than zero implicating genetic variation in this life history trait. However, predicted breeding values for AFR are randomly distributed among rank-levels, which points to common environmental effects, rather than inter-matriline genetic differences, as the primary causes of rank-related variation in AFR. In addition, interannual variation in population density, climate, and colony management also result in strong cohort effects on AFR. Maternal identity explained no variance in AFR, although some maternal characteristics do influence AFR, which requires greater clarity in describing the presence or absence of maternal effects on this important life history trait.