In group living animals, especially among primates, there is consistent evidence that high-ranking males gain a higher reproductive output than low-ranking males. Primate studies have shown that male coalitions and sociality can impact male fitness; however, it remains unclear whether males could potentially increase their fitness by preferentially supporting and socializing with females. Here we investigate patterns of male interventions and the effect of coalitions and sociality on male fitness in rhesus macaques (Macaca mulatta) with particular focus on male-female interactions. We combined behavioral collected on Cayo Santiago with genetic data analyzed for male reproductive output and relatedness. Our results revealed that the ten top-ranking males provided the majority of all male support observed. In contrast to other primates, male rhesus macaques mainly formed all-down coalitions suggesting that coalitions are less likely used to enhance male dominance. Males supporting females during and before their likely conception were not more likely to fertilize those females. We also found no evidence that males preferably support their offspring or other close kin. Interestingly, the most important predictor of male support was sociality, since opponents sharing a higher sociality index with a given male were more likely to be supported. Furthermore, a high sociality index of a given male-female dyad resulted in a higher probability of paternity. Overall, our results strengthen the evidence that sociality affects fitness in male primates, but also suggest that in species in which males queue for dominance, it is less likely that males derive fitness benefits from coalitions.
male rhesus macaques; interventions; coalitions; fitness; sociality
Although the proximate mechanisms behind the formation of copulatory plugs are well understood, their distribution and function among primates remain largely unstudied. During a study of female rhesus macaque (Macaca mulatta) mating behaviour on Cayo Santiago, we examined the pattern of the distribution of visible copulatory plugs among females and their potential relationship to female reproductive traits and sexual skin colouration. Our results indicate that non-pregnant females were observed more frequently with visible copulatory plugs than were pregnant females. Female parity status, age and rank were unrelated to copulatory plug observation. Genital colouration components were higher among females observed with copulatory plugs. We suggest that although copulatory plugs are generally thought of in terms of male physiology, plug observation may also be affected by female reproductive status.
Rhesus macaques; Copulatory plugs; Colouration; Sperm competition; Sexual skin
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.
life history; quantitative genetics; genetic correlation; maturation; senescence; primate
The present case report provides a description of the emergence of an innovative, highly beneficial for- aging behavior in a single rhesus monkey (Macaca mulatta) on the island of Cayo Santiago, Puerto Rico. Selectively choosing the island’s cement dock and nearby surrounding rocky terrain, our focal subject (ID: 84 J) opens coconuts using two types of underhand tosses: (1) a rolling motion to move it, and (2) a throwing motion up in the air to crack the shell. We discuss this innovative behavior in light of species-specific behavioral propensities.
Innovation; behavioral repertoire; foraging; Rhesus macaques
In contrast to most mammalian species, female sexual activity is not limited to the fertile phase of the ovarian cycle in anthropoid primates, which has long been proposed to conceal the timing of ovulation to males. It is now generally believed that females are still most attractive during the fertile phase, leading to high-ranking males successfully mate-guarding them specifically during this period. While studies conducted in species exhibiting exaggerated sexual swellings (probabilistic signal of the fertile phase) have generally supported this hypothesis, mixed support comes from others. Here, we investigated whether high-ranking males timed mate-guarding effort towards female fertile phases in rhesus macaques (Macaca mulatta). In this species, adult females do not exhibit sexual swellings, but undergo facial skin colour variation, an alternative oestrogens-dependent graded-signal of female reproductive status. We collected behavioural, hormonal and genetic paternity data during two mating seasons for one group of the free-ranging population of Cayo Santiago. Our results show that mate-guarding by top-ranking males did not completely cover the entire female fertile phase and that this tactic accounted for only 30-40% of all fertilisations observed. Males tended to prolong mate-guarding into the luteal phase (null probability of fertilisation), which mirrors the pattern of male attraction to female facial colour reported in an earlier study. These findings suggest that males may have limited knowledge regarding the exact timing of females’ fertile phase in rhesus macaques, which presumably allows females to gain more control over reproduction relative to other anthropoid primate species.
Prolonged sexual receptivity; concealed ovulation; mate-guarding; fecal steroids; reproductive strategies; fertile phase; genetic paternity analysis; primates; rhesus macaques
Reproductive effort in female ungulates originates from gestation and lactation and has been studied extensively; however, no comparable studies of reproductive effort in males (due to fighting for access to mates) have, to our knowledge, previously been reported. Here, we report on weight loss of male red deer during the annual mating season--a direct measure of male reproductive effort (or somatic reproductive costs). The 'terminal investment' hypothesis predicts that reproductive effort should increase with age, given that costs remain stable. We also propose the 'mating strategy-effort' hypothesis, which predicts that reproductive effort peaks in prime-aged males, since they are most often the harem holders. Consistent with the mating strategy-effort hypothesis, relative weight loss during the rutting season peaked at prime age and was lower in younger and senescent males. Weight loss during the rut was relatively smaller as density increased and more so for older males. This is probably primarily due to males (particularly senescent males) starting their rut in poorer condition at high density. The pattern of reproductive effort in males with regard to age and density therefore differs markedly from the pattern reported for females.
There is growing interest in studying oxytocin biology in the context of social functioning in human and non-human primates. Studies of human subjects are typically restricted to peripheral oxytocin assessments because opportunities to collect cerebrospinal fluid (CSF) are rare. A few studies have examined CSF oxytocin levels in captive adult primates, but none to our knowledge have been conducted under free-ranging conditions and inclusive of young infants. The main goal of the present study was to establish feasibility of quantifying CSF oxytocin levels in free-ranging adult female and infant rhesus monkeys living on the island of Cayo Santiago, Puerto Rico. CSF oxytocin levels were examined in relation to individuals’ demographic and reproductive characteristics, as well as in relation to plasma cortisol levels. CSF oxytocin concentrations ranged from 36.02 to 134.41 pg/ml in adult females (ages 7–26 years; N = 31) and 35.94 to 77.3 pg/ml in infants (ages 38–134 days; N = 17). CSF oxytocin levels were positively correlated with adult female age and negatively correlated with infant age. The former correlation was driven by reproductive status. CSF oxytocin levels were unrelated to dominance rank or plasma cortisol levels. In contrast to a previous study of plasma oxytocin concentrations in this population, CSF oxytocin levels did not differ significantly between lactating and non-lactating females. In summary, these findings: 1) provide feasibility data for examining CSF oxytocin biology in free-ranging nonhuman primates and 2) indicate that CSF oxytocin levels may be a biomarker of age-related central nervous system changes across lifespan development. Although our study did not report significant associations between CSF oxytocin levels and socially-relevant demographic variables, the relationships between CSF oxytocin levels and assessments of social functioning warrant future investigation.
Age; CSF; infant; cortisol; free-ranging; oxytocin; rhesus monkey
Most primates are both highly visual and highly social. These qualities predict that visual cues to social variables, such as identity, sex, social status, and reproductive quality, would be intrinsically valuable and systematically attract attention. Supporting this idea, thirsty male rhesus macaques (Macaca mulatta) will forego fluid reward to view images of the faces of high-ranking males and the sexual skin of females. Whether female rhesus macaques, who experience dramatically different social pressures and reproductive costs than male macaques, also systematically and spontaneously value visual cues to social information remains untested experimentally. We probed the preferences of female rhesus macaques, given the opportunity to display an image from a known class of social stimuli or touch a second target to display a blank screen. We found that females preferred faces of high-status males and also images of the perinea of both males and females, but were not motivated to display images of subordinate males or control stimuli. These findings endorse the view that both male and female rhesus macaques—and presumably other highly social primates—seek information about other individuals in a way that matches the adaptive value of that information for guiding social behavior.
Macaca mulatta; Social; Dominant; Subordinate; Status; Hierarchy
A fundamental life history question is how individuals should allocate resources to reproduction optimally over time (reproductive allocation). The reproductive restraint hypothesis predicts that reproductive effort (RE; the allocation of resources to current reproduction) should peak at prime-age, whilst the terminal investment hypothesis predicts that individuals should continue to invest more resources in reproduction throughout life, owing to an ever-decreasing residual reproductive value. There is evidence supporting both hypotheses in the scientific literature.
We used an uncommonly large, 38 year dataset on Alpine chamois (Rupicapra rupicapra) shot at various times during the rutting period to test these two hypotheses. We assumed that body mass loss in rutting males was strongly related to RE and, using a process-based approach, modelled how male relative mass loss rates varied with age. For different regions of our study area, we provide evidence consistent with different hypotheses for reproductive allocation. In sites where RE declined in older age, this appears to be strongly linked to declining body condition in old males. In this species, terminal investment may only occur in areas with lower rates of body mass senescence.
Our results show that patterns of reproductive allocation may be more plastic than previously thought. It appears that there is a continuum from downturns in RE at old age to terminal investment that can be manifest, even across adjacent populations. Our work identifies uncertainty in the relationship between reproductive restraint and a lack of competitive ability in older life (driven by body mass senescence); both could explain a decline in RE in old age and may be hard to disentangle in empirical data. We discuss a number of environmental and anthropogenic factors which could influence reproductive life histories, underlining that life history patterns should not be generalised across different populations.
Theories of ageing predict a trade-off between metabolism, reproduction, and maintenance. Species with low investment in early reproduction are thus expected to be able to evolve more efficient maintenance and repair mechanisms, allowing for a longer potential life span (intrinsic longevity). The erosion of telomeres, the protective caps at the ends of linear chromosomes, plays an important role in cellular and organismal senescence, signalling the onset of age-related disease due to accumulation of unrepaired somatic damage. Using extensive longitudinal data from a long-term study of a natural population of barnacle geese Branta leucopsis, we investigated individual rates of telomere length changes over two years in 34 birds between 0 and 22 years of age, covering almost 80% of the species’ lifespan.
We show that telomeres in this long-lived bird are very well maintained, as theoretically expected, with an average loss rate of only 5 base pairs per year among adults. We thus found no significant relationship between change in telomere length and age. However, telomeres tended to shorten at a faster pace in juveniles compared to adults. For the first time, we demonstrate a faster telomere attrition rate in females compared to males. We found no correlation between telomere loss rate and adult survival or change in body mass.
Our results add further support for a link between longevity and telomere maintenance, and highlight the complexities of telomere dynamics in natural populations.
Individual telomere rate of change; Longitudinal data; Rate of ageing; Senescence; Survival; Telomere maintenance
This study reports an experimental confirmation of the terminal investment hypothesis, a longstanding theoretical idea that animals should increase their reproductive effort as they age and their prospects for survival and reproduction decline. Previous correlational and experimental attempts to test this hypothesis have yielded contradictory results. In the blue-footed booby, Sula nebouxii, a long-lived bird, after initial increase, male reproductive success declines progressively with age. Before laying, males of two age classes were challenged with lipopolysaccharide to elicit an immune response, which induced symptoms of declining survival prospects. Reproductive success of immune-challenged mature males fell, while that of immune-challenged old males showed a 98% increase. These results demonstrate that senescent males with poor reproductive prospects increase their effort when those prospects are threatened, whereas younger males with good reproductive prospects do not.
senescence; life history; immune response; plasticity; reproductive success; lipopolysaccharide
Nonhuman primates, particularly rhesus macaques (Macaca mulatta), provide important model systems for studying human reproductive infectious diseases such as human immunodeficiency virus, human papillomavirus, and Chlamydia spp. An understanding of the spectrum of spontaneous cervical disease provides essential context for interpreting experimental disease outcomes in the female reproductive tract. This retrospective study characterizes the incidence of inflammatory and/or proliferative cervicovaginal lesions seen over a 14-year period in a multispecies nonhuman primate colony, focusing on rhesus macaques. The most common observations included a spectrum of lymphocytic accumulation from within normal limits to lymphoplasmacytic cervicitis, and suppurative inflammation with occasional squamous metaplasia or polyp formation. These inflammatory spectra frequently occurred in the context of immunosuppression following experimental simian immunodeficiency virus (SIV) infection. Cervical neoplasias were uncommon and included leiomyomas and carcinomas. Cervical sections from 13 representative cases, with an emphasis on proliferative and dysplastic lesions, were surveyed for leukocyte infiltration, abnormal epithelial proliferation, and the presence of papillomavirus antigens. Proliferative lesions showed sporadic evidence of spontaneous papillomavirus infection and variable immune cell responses. These results under-score the importance of pre screening potential experimental animals for the presence of preexisting reproductive tract disease, and the consideration of normal variability within cycling reproductive tracts in interpretation of cervical lesions.
animal models; female reproduction; primate pathology; immunohistochemistry; histopathology
Dietary caloric restriction (CR) slows aging, extends lifespan, and reduces the occurrence of age-related diseases in short-lived species. However, it is unclear whether CR can exert similar beneficial effects in long-lived species, like primates. Our objective was to determine if CR could attenuate purported age-related changes in the 24-h release of adrenal steroids. To this end, we examined 24-hour plasma profiles of cortisol, and dehydroepiandrosterone sulfate (DHEAS) in young and old, male and female rhesus macaques (Macaca mulatta) subjected to either ad libitum (AL)-feeding or CR (70% of AL) for 2–4 years. Hormone profiles from young monkeys showed pronounced 24-h rhythms. Cortisol concentrations were higher in old males but not females, whereas DHEAS rhythms were dampened with age in both sexes. The cortisol rhythms of old CR males resembled that of young control males. However, CR failed to prevent age-related declines in DHEAS and further dampened DHEAS rhythms in both sexes. Apart from the partial attenuation of the age-related cortisol elevation in the old males, 24-h adrenal steroid rhythms did not benefit from late-onset CR.
Adrenal steroids; Aging; Caloric restriction; Circadian; Cortisol; DHEAS; Endocrine rhythms; Primate
Reproductive investment decisions form an integral part of life-history biology. Selection frequently favours plasticity in investment that can generate maternal effects on offspring development. For example, if females differentially allocate resources based on mate attractiveness or quality, this can create a non-genetic link between mate attractiveness and offspring fitness with potential consequences for ecological and evolutionary dynamics. It is therefore important to understand under what conditions differential investment into offspring in relation to male quality is expected to occur and the direction of the effect. Two opposite predictions, increased investment into offspring produced with high-quality mates (differential allocation (DA)) and increased investment with low-quality males (reproductive compensation (RC)) have been suggested but no formal theoretical treatment justifying the assumptions underlying these two hypotheses has been conducted to date. Here, we used a state-based approach to investigate the circumstances under which the variation in mate quality results in differential female investment into offspring and how this interacts with female energetic resource levels. We found that a pattern of increased investment when mating with high-quality mates (i.e. DA) was the most common optimal investment strategy for females in our model. By contrast, increased investment when mating with low-quality mates (i.e. RC) was predicted only when the relative impact of parental investment on offspring quality was low. Finally, we found that the specific pattern of investment in relation to male quality depends on female energetic state, the likelihood for future mating opportunities and the expected future distribution of mate quality. Thus, the female's age and body condition should be important factors mediating DA and RC, which may help to explain the equivocal results of empirical studies.
dynamic program; differential allocation; compensation hypothesis; sexual selection; mate choice; maternal effects
The disposable soma hypothesis predicts that when reproduction is reduced, life span is increased because more nutrients are invested in the soma, increasing somatic repair. Rigorously testing the hypothesis requires tracking nutrients from ingestion to allocation to the soma or to reproduction. Fruit flies on life-extending dietary restriction increase allocation to the soma “relative” to reproduction, suggesting that allocation of nutrients can be associated with extension of life span. Here, we use stable isotopes to track ingested nutrients in ovariectomized grasshoppers during the first oviposition cycle. Previous work has shown that ovariectomy extends life span, but investment of protein in reproduction is not reduced until after the first clutch of eggs is laid. Because ovariectomy does not affect investment in reproduction at this age, the disposable soma hypothesis would predict that ovariectomy should also not affect investment in somatic tissues. We developed grasshopper diets with distinct signatures of 13C and 15N, but that produced equivalent reproductive outputs. These diets are, therefore, appropriate for the reciprocal switches in diet needed for tracking ingested nutrients. Incorporation of stable isotopes into eggs showed that grasshoppers are income breeders, especially for carbon. Allocation to the fat body of nitrogen ingested as adults was slightly increased by ovariectomy; this was our only result that was not consistent with the disposable soma hypothesis. In contrast, ovariectomy did not affect allocation of nitrogen to femoral muscles. Further, allocation of carbon to the fat body or femoral muscles did not appear to be affected by ovariectomy. Total anti-oxidant activities in the hemolymph and femoral muscles were not affected by ovariectomy. These experiments showed that allocation of nutrients was altered little by ovariectomy in young grasshoppers. Additional studies on older individuals are needed to further test the disposable soma hypothesis.
Evolutionary theory predicts that differential reproductive effort and rate of reproductive senescence will evolve under different rates of external mortality. We examine the evolutionary divergence of age-specific reproduction in two life-history ecotypes of the western terrestrial garter snake, Thamnophis elegans. We test for the signature of reproductive senescence (decreasing fecundity with age) and increasing reproductive effort with age (increasing reproductive productivity per gram female) in replicate populations of two life-history ecotypes: snakes that grow fast, mature young and have shorter lifespans, and snakes that grow slow, mature late and have long lives. The difference between life-history ecotypes is due to genetic divergence in growth rate. We find (i) reproductive success (live litter mass) increases with age in both ecotypes, but does so more rapidly in the fast-growth ecotype, (ii) reproductive failure increases with age in both ecotypes, but the proportion of reproductive failure to total reproductive output remains invariant, and (iii) reproductive effort remains constant in fast-growth individuals with age, but declines in slow-growth individuals. This illustration of increasing fecundity with age, even at the latest ages, deviates from standard expectations for reproductive senescence, as does the lack of increases in reproductive effort. We discuss our findings in light of recent theories regarding the phenomenon of increased reproduction throughout life in organisms with indeterminate growth and its potential to offset theoretical expectations for the ubiquity of senescence.
reproductive effort; garter snake; life history; senescence
Sociality is believed to have evolved as a strategy for animals to cope with their environments. Yet the genetic basis of sociality remains unclear. Here we provide evidence that social network tendencies are heritable in a gregarious primate. The tendency for rhesus macaques, Macaca mulatta, to be tied affiliatively to others via connections mediated by their social partners - analogous to friends of friends in people - demonstrated additive genetic variance. Affiliative tendencies were predicted by genetic variation at two loci involved in serotonergic signalling, although this result did not withstand correction for multiple tests. Aggressive tendencies were also heritable and were related to reproductive output, a fitness proxy. Our findings suggest that, like humans, the skills and temperaments that shape the formation of multi-agent relationships have a genetic basis in nonhuman primates, and, as such, begin to fill the gaps in our understanding of the genetic basis of sociality.
Nonhuman primates have been used for biomedical research for several decades. The high level of genetic homology to humans coupled with their outbred nature has made nonhuman primates invaluable preclinical models. In this review, we summarize recent advances in our understanding of the nonhuman primate immune system, with special emphasis on studies carried out in rhesus macaque (Macaca mulatta). We highlight the utility of nonhuman primates in the characterization of immune senescence and the evaluation of new interventions to slow down the aging of the immune system. Antioxid. Redox Signal. 14, 261–273.
The ability to recognize kin is an important social skill for primates. Humans are adept at using facial similarity to recognize likely kin, and there is evidence that nonhuman primates are also able to use facial similarity to make judgments about kinship. However, if and how nonhuman primate faces actually contain kinship information remains unclear. To test whether there is objectively measurable facial similarity in related nonhuman primates, we compared facial measurements from related (paternal half-sisters) and unrelated adult female rhesus macaques (Macaca mulatta). Facial measurements were first summarized into 5 factors using a principal component analysis. Differences in these factors between the faces of related macaques were compared with differences between the faces of random unrelated macaques and of age-matched unrelated macaques. The difference in facial measurements between related macaques was significantly smaller than the difference in facial measurements of either group of unrelated macaques, constituting an objective measure of facial similarity in macaque kin. These results indicate that kinship information is contained in the rhesus macaque face and suggest that nonhuman primates may rely in part on facial similarity to distinguish kin.
kin recognition; facial similarity; rhesus macaque; principal component analysis
We investigated the effects of population fluctuation on the offspring’s sex allocation by a weakly polygynous mouse, Apodemus argenteus, for 3 years. In acorn-poor seasons, heavier mothers invested more in sons, and lighter mothers invested more in daughters. In acorn-rich seasons, heavier mothers invested more in daughters, and lighter mothers invested more in sons. Maternal body condition and litter size affected the sex allocation. Furthermore, there was a maternal investment trade-off between a son’s birth mass and the number of daughters. Based upon the effect of population fluctuation on the lifetime reproductive success of each sex, we proposed the new “safe bet hypothesis”. This hypothesis predicts that frequent and unpredictable change in female distribution, which is often caused by abrupt fall in food condition, favors female-biased maternal investment to offspring by polygynous mammals and is applicable to many small mammals inhabiting in unstable environments.
Apodemus argenteus; Trivers and Willard’s hypothesis; Sex allocation; Maternal investment trade-off; Safe bet hypothesis
We develop a model for somatic growth in fishes that explicitly allows for the energy demand imposed by reproduction. We show that the von Bertalanffy (VB) equation provides a good description of somatic growth after maturity, but not before. We show that the parameters of the VB equation are simple functions of age at maturity and reproductive investment. We use this model to show how the energy demands for both growth and reproduction trade off to determine optimal life-history traits. Assuming that both age at maturity and reproductive investment adapt to variations in adult mortality to maximize lifetime offspring production, our model predicts that: (i) the optimal age of maturity is inversely related to adult mortality rate; (ii) the optimal reproductive effort is approximately equal to adult mortality rate. These predictions are consistent with observed variations in the life-history traits of a large sample of iteroparous freshwater fishes.
Linear dominance hierarchies organize and maintain stability in female rhesus macaque (Macaca mulatta) social groups regardless of group size. As a consequence of their low social status, subordinate females suffer from an array of adverse outcomes including reproductive compromise, impaired immune function, and poor cardiovascular health. However, data that differentiate limbic-hypothalamic-pituitary adrenal axis (LHPA) parameters between dominant from subordinate female monkeys are inconsistent, bringing into question whether social subordination alters the LHPA axis in female macaques. One difficulty in examining LHPA function in macaques may be the confounding effects of cycling ovarian steroids that are known to modulate LHPA activity. The current study used ovariectomized dominant and subordinate female rhesus monkeys to examine the effect that social subordination has on LHPA function by measuring morning and diurnal serum cortisol levels, dexamethasone (Dex) suppression of cortisol, metabolic clearance of Dex, and ACTH stimulation of adrenal cortisol release and cortisol response following exposure to acute social isolation. Compared to dominant females, subordinate females showed diminished morning peak cortisol secretion, weakened glucocorticoid negative feedback, and decreased adrenal cortisol response to an ACTH challenge as well as a restrained cortisol response following social isolation. However, the metabolism of Dex did not account for differences in Dex suppression between dominant and subordinate females. These results indicate that the ability to mount and limit glucocorticoid release is significantly reduced by psychosocial stress in female rhesus macaques, suggesting a hyporesponsive LHPA phenotype which resembles that observed in several human psychopathologies.
social subordination; dexamethasone; cortisol; ACTH; psychosocial stress; monkeys
Evolutionary explanations for life history diversity are based on the idea of costs of reproduction, particularly on the concept of a trade-off between age-specific reproduction and parental survival, and between expenditure on current and future offspring. Such trade-offs are often difficult to detect in population studies of wild mammals. Terminal investment theory predicts that reproductive effort by older parents should increase, because individual offspring become more valuable to parents as the conflict between current versus potential future offspring declines with age. In order to demonstrate this phenomenon in females, there must be an increase in maternal expenditure on offspring with age, imposing a fitness cost on the mother. Clear evidence of both the expenditure and fitness cost components has rarely been found. In this study, we quantify costs of reproduction throughout the lifespan of female antechinuses. Antechinuses are nocturnal, insectivorous, forest-dwelling small (20–40 g) marsupials, which nest in tree hollows. They have a single synchronized mating season of around three weeks, which occurs on predictable dates each year in a population. Females produce only one litter per year. Unlike almost all other mammals, all males, and in the smaller species, most females are semelparous. We show that increased allocation to current reproduction reduces maternal survival, and that offspring growth and survival in the first breeding season is traded-off with performance of the second litter in iteroparous females. In iteroparous females, increased allocation to second litters is associated with severe weight loss in late lactation and post-lactation death of mothers, but increased offspring growth in late lactation and survival to weaning. These findings are consistent with terminal investment. Iteroparity did not increase lifetime reproductive success, indicating that terminal investment in the first breeding season at the expense of maternal survival (i.e. semelparity) is likely to be advantageous for females.
Because most studies of AIDS pathogenesis in nonhuman primates have been performed in Indian-origin rhesus macaques (Macaca mulatta), little is known about lentiviral pathogenicity and control of virus replication following infection of alternative macaque species. Here, we report the consequences of simian-human immunodeficiency virus SHIV-89.6P and SIVmac251 infection in cynomolgus (Macaca fascicularis) and rhesus macaques of Chinese origin. Compared to the pathogenicity of the same viruses in Indian rhesus macaques, both cynomolgus and Chinese rhesus macaques showed lower levels of plasma virus. By 9 to 10 months after infection, both viruses became undetectable in plasma more frequently in cynomolgus than in either Chinese or Indian rhesus macaques. Furthermore, after SHIV-89.6P infection, CD4+ T-cell numbers declined less and survival was longer in cynomolgus and Chinese rhesus macaques than in Indian rhesus macaques. This attenuated pathogenicity was associated with gamma interferon ELISPOT responses to Gag and Env that were generated earlier and of higher frequency in cynomolgus than in Indian rhesus macaques. Cynomolgus macaques also developed higher titer neutralizing antibodies against SHIV-89.6 at 10 and 20 weeks postinoculation than Indian rhesus macaques. These studies demonstrate that the pathogenicity of nonhuman primate lentiviruses varies markedly based on the species or geographic origin of the macaques infected and suggest that the cellular immune responses may contribute to the control of pathogenicity in cynomolgus macaques. While cynomolgus and Chinese rhesus macaques provide alternative animal models of lentiviral infection, the lower levels of viremia in cynomolgus macaques limit the usefulness of infection of this species for vaccine trials that utilize viral load as an experimental endpoint.
In many taxa, reproductive performance increases throughout the lifespan and this may occur in part because older adults invest more in reproduction. The mechanisms that facilitate an increase in reproductive performance with age, however, are poorly understood. In response to stressors, vertebrates release glucocorticoids, which enhance survival but concurrently shift investment away from reproduction. Consequently, when the value of current reproduction is high relative to the value of future reproduction and survival, as it is in older adults, life history theory predicts that the stress response should be suppressed. In this study, we tested the hypothesis that older parents would respond less strongly to a stressor in a natural, breeding population of common terns (Sterna hirundo). Common terns are long-lived seabirds and reproductive performance is known to increase throughout the lifespan of this species. As predicted, the maximum level of glucocorticoids released in response to handling stress decreased significantly with age. We suggest that suppression of the stress response may be an important physiological mechanism that facilitates an increase in reproductive performance with age.
age; common tern (Sterna hirundo); corticosterone; life history evolution; parental care; stress response