Papers by Alexander Georgiev
Background and objectives Life history theory predicts resource allocation trade-offs between com... more Background and objectives Life history theory predicts resource allocation trade-offs between competing functions and processes. We test the hypothesis that relative investment towards innate versus acquired immunity in humans is subject to such trade-offs and that three types of early developmental exposures are particularly salient in shaping adult immunophenotype: (i) pathogen exposure, (ii) nutritional resources; and (iii) extrinsic mortality cues.
Methodology We quantified one aspect each of innate and acquired immune function, via C-reactive protein and Epstein–Barr virus antibodies, respectively, in a sample of 1248 men and women from the Philippines (ca. 21.5 years old). Early developmental exposures were assessed via long-term data collected prospectively since participants’ birth (1983–4). We calculated a standardized ratio to assess relative bias towards acquired versus innate immune function and examined its relationship to a suite of predictors via multiple regression.
Results In partial support of our predictions, some of the measures of higher pathogen exposure, greater availability of nutritional resources, and lower extrinsic mortality cues in early life were associated with a bias toward acquired immunity in both men and women. The immune profile of women, in particular, appeared to be more sensitive to early life pathogen exposures than those of men. Finally, contrary to prediction, women exhibited a greater relative investment toward innate, not acquired, immunity.
Conclusions and implications Early environments can exert considerable influence on the development of immunity. They affect trade-offs between innate and acquired immunity, which show adaptive plasticity and may differ in their influence in men and women.
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Explaining intraspecific variation in reproductive tactics hinges on measuring associated costs a... more Explaining intraspecific variation in reproductive tactics hinges on measuring associated costs and benefits. Yet, this is difficult if alternative (purportedly less optimal) tactics remain unobserved. We describe a rare alpha-position takeover by an immigrant male rhesus macaque in a population where males typically gain rank via succession. Unusually, male aggressiveness after the takeover correlated with rank and mating success. The new alpha achieved the highest mating and reproductive success. Nevertheless, he sired only 4 infants due to high extra-group paternity (59.3%). The costs of his immigration tactic were high: after the mating season ended, unable to deter coali-tionary attacks by resident males, he was overthrown. The following year he had the highest relative annual weight loss and levels of immune activation among males in the group. Succession-based rank-acquisition in large, provisioned groups of macaques thus appears to be actively maintained by resident males, who impose high costs on challengers.
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Immune defenses provide resistance against infectious disease that is critical to survival. But i... more Immune defenses provide resistance against infectious disease that is critical to survival. But immune defenses are costly, and limited resources allocated to immunity are not available for other physiological or developmental processes. We propose a framework for explaining variation in patterns of investment in two important subsystems of anti-pathogen defense: innate (non-specific) and acquired (specific) immunity. The developmental costs of acquired immunity are high, but the costs of maintenance and activation are relatively low. Innate immunity imposes lower upfront developmental costs, but higher operating costs. Innate defenses are mobilized quickly and are effective against novel pathogens. Acquired responses are less effective against novel exposures, but more effective against secondary exposures due to immunological memory. Based on their distinct profiles of costs and effectiveness, we propose that the balance of investment in innate versus acquired immunity is variable, and that this balance is optimized in response to local ecological conditions early in development. Nutritional abundance, high pathogen exposure and low signals of extrinsic mortality risk during sensitive periods of immune development should all favor relatively higher levels of investment in acquired immunity. Undernutrition, low pathogen exposure, and high mortality risk should favor innate immune defenses. The hypothesis provides a framework for organizing prior empirical research on the impact of developmental environments on innate and acquired immunity, and suggests promising directions for future research in human ecological immunology.
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Circulating testosterone (T) follows a diurnal pattern with high waking levels that decline acros... more Circulating testosterone (T) follows a diurnal pattern with high waking levels that decline across the day. The hypothalamic-pituitary-adrenal axis produces cortisol in a similar manner but also undergoes an abrupt increase in hormone secretion immediately upon waking (a cortisol awakening response, CAR). Whether the hypothalamic-pituitary-gonadal axis, and circulating T levels, exhibit a similar post-waking response is unclear. Here we describe post-waking T changes in a sample of 108 young adult males from metropolitan Cebu City, the Philippines. As expected, salivary T was higher at waking than in the evening but, remarkably, 60 % of this diurnal decline occurred within 30 min of awakening. There was a strong inverse linear relationship between waking T and the post-waking T decline, such that men with higher waking T experienced a more rapid decline in the hormone. Even though fathers had lower waking T, they experienced a greater post-waking decline than non-fathers. Men with a larger positive CAR had modestly attenuated post-waking T declines. We speculate that these findings reflect a testosterone awakening response (TAR) that helps partition the target tissue effects of T by time of day. T rises overnight to facilitate muscle anabolism at a time when the hormone’s impacts on social behavior are limited. Upon waking, the rapid drop in T helps shift from anabolic to catabolic processes in support of physical activity, while also calibrating T levels in line with the competing social priorities of the individual, as determined by the current balance of behavioral investment towards mating and parental effort.
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Nature Communications, 2014
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Sex differences in longevity may reflect sex-specific costs of intra-sexual competition and repro... more Sex differences in longevity may reflect sex-specific costs of intra-sexual competition and reproductive effort. As male rhesus macaques experience greater intrasexual competition and die younger, we predicted that males would experience greater oxidative stress than females and that oxidative stress would reflect sex-specific measures of reproductive effort. Males, relative to females, had higher concentrations of 8-OHdG and malondialdehyde, which are markers of DNA oxidative damage and lipid peroxidation, respectively. Older macaques had lower 8-OHdG levels than younger ones, suggesting that oxidative stress decreases in parallel with known age-related declines in reproductive investment. Among males, a recent period of social instability affected oxidative status: males who attacked others at higher rates had higher 8-OHdG levels. Multiparous lactating females with daughters had higher 8-OHdG levels than those with sons. No differences in antioxidant capacity were found. These results lend initial support for the use of oxidative stress markers to assess trade-offs between reproductive effort and somatic maintenance in primates.
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Research with the rhesus macaque population on Cayo Santiago can provide a unique perspective on ... more Research with the rhesus macaque population on Cayo Santiago can provide a unique perspective on the costs of sociality and reproduction in primates. Because the Cayo macaques live in unusually large groups and in a predator-free environment, in which their artificial food source lacks seasonal variation in abundance or quality, these monkeys constitute a semi-experimental study of the costs and benefits of group living. Here we review several long- and short-term studies that have focused on female life history and stress physiology. Long-term demographic data have shown that rhesus macaque females of middle- and low-ranking matrilines have lower adult survival probabilities than females of high-ranking matrilines. Costs of reproductive effort are also evident: adult females were more likely to die during the birth than during the mating season and they experienced higher cortisol levels when lactating. Lower-ranking females, in particular, experienced greater relative increase in cortisol production during lactation, in comparison to middle- and high-ranking females. Older high-ranking females had lower plasma cortisol levels than younger ones but cortisol levels were similarly high among young and old middle- and low-ranking females. Higher plasma cortisol levels and/or fecal glucocorticoid concentrations are associated with higher plasma concentrations of some proinflammatory cytokines. High cortisol, in turn, may be associated with chronic inflammation, and perhaps also with immunosuppression. In sum, the studies reviewed here provide multiple lines of evidence that sociality and reproductive effort impose measurable costs on female rhesus macaques. In line with socio-ecological theory, female dominance rank consistently emerges as an important modulator of variation in female life histories and physiology. The Cayo Santiago macaques are therefore a valuable model for elucidating the mechanisms by which within-group competition and reproduction impact health and survival in nonhuman primates and in humans. Am. J. Primatol. © 2015 Wiley Periodicals, Inc.
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International Journal of Primatology
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International Journal of Primatology
Costs of mating effort can affect the reproductive strategies and lifetime fitness of male primat... more Costs of mating effort can affect the reproductive strategies and lifetime fitness of male primates, but interspecific and interindividual variation in the magnitude and distribution of costs is poorly understood. Male costs have primarily been recognized in seasonally breeding species that experience concentrated periods of mating competition. Here, we examine foraging costs associated with male mating effort in chimpanzees (Pan troglodytes schweinfurthii), a polygynandrous species, in which mating opportunities occur intermittently throughout the year. To quantify male feeding, aggression, and mating, we conducted focal follows on 12 males in a wild community (Kanyawara, Kibale National Park, Uganda) for 11 mo. Males fed less on days when high-value mating opportunities (estrous parous females) were available than on days without any mating opportunities. Reductions in feeding time were related to increased rates of aggression and copulation, indicating that the proximate cause of changes in male foraging was mating effort. Surprisingly, however, there was no relationship between dominance rank and the extent to which feeding time was reduced. High costs of mating effort may reduce the degree of reproductive skew and limit the use of possessive tactics in chimpanzees. We suggest that male bonding in chimpanzees may be favored not only for its benefits but because intragroup competition is so costly. Our results complement the available data on mammals, and primates in particular, by showing that mating effort can have measurable foraging costs even in species, in which breeding is aseasonal and only moderately skewed.
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We compared the feeding ecology of the Hali–Hali community of bonobos (Pan paniscus) at Kokolopor... more We compared the feeding ecology of the Hali–Hali community of bonobos (Pan paniscus) at Kokolopori, a new field site in the Democratic Republic of the Congo, between two periods 5 months apart. During the first study period (SP1), bonobos relied heavily on the dry seeds of Guibourtia (Caesalpiniaceae), mostly eaten from the ground. The second period (SP2) was characterized by high consumption of ripe tree fruit. Terrestrial herbaceous vegetation (THV) contributed little to the diet in either study period. The low amount of ripe fruit and the high reliance on seeds in the diet during SP1 were associated with high cortisol production and low levels of urinary C-peptide in females, suggesting nutritional stress. However, female gregariousness was not constrained during the fruit-poor period, probably because high seed abundance on the ground ameliorated scramble feeding competition. This is the first description of extensive seed predation by bonobos. It suggests that bonobo feeding ecology may be more similar to that of chimpanzees than previously recognized.
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African Journal of Ecology, 2010
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Nature communications, 2014
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Nature, Sep 23, 2010
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Papers by Alexander Georgiev
Methodology We quantified one aspect each of innate and acquired immune function, via C-reactive protein and Epstein–Barr virus antibodies, respectively, in a sample of 1248 men and women from the Philippines (ca. 21.5 years old). Early developmental exposures were assessed via long-term data collected prospectively since participants’ birth (1983–4). We calculated a standardized ratio to assess relative bias towards acquired versus innate immune function and examined its relationship to a suite of predictors via multiple regression.
Results In partial support of our predictions, some of the measures of higher pathogen exposure, greater availability of nutritional resources, and lower extrinsic mortality cues in early life were associated with a bias toward acquired immunity in both men and women. The immune profile of women, in particular, appeared to be more sensitive to early life pathogen exposures than those of men. Finally, contrary to prediction, women exhibited a greater relative investment toward innate, not acquired, immunity.
Conclusions and implications Early environments can exert considerable influence on the development of immunity. They affect trade-offs between innate and acquired immunity, which show adaptive plasticity and may differ in their influence in men and women.
Methodology We quantified one aspect each of innate and acquired immune function, via C-reactive protein and Epstein–Barr virus antibodies, respectively, in a sample of 1248 men and women from the Philippines (ca. 21.5 years old). Early developmental exposures were assessed via long-term data collected prospectively since participants’ birth (1983–4). We calculated a standardized ratio to assess relative bias towards acquired versus innate immune function and examined its relationship to a suite of predictors via multiple regression.
Results In partial support of our predictions, some of the measures of higher pathogen exposure, greater availability of nutritional resources, and lower extrinsic mortality cues in early life were associated with a bias toward acquired immunity in both men and women. The immune profile of women, in particular, appeared to be more sensitive to early life pathogen exposures than those of men. Finally, contrary to prediction, women exhibited a greater relative investment toward innate, not acquired, immunity.
Conclusions and implications Early environments can exert considerable influence on the development of immunity. They affect trade-offs between innate and acquired immunity, which show adaptive plasticity and may differ in their influence in men and women.