Maternal effects are widespread in living organisms though little is known about whether they shape individual affiliative social behavior in primates. Further, it remains a question whether maternal effects on affiliative behavior differ by offspring sex, as they do in other physiological systems, especially in species with high levels of adult sexual dimorphism and divergence in social niches. We explored how direct and indirect experiences of maternal affiliative behavior during infancy predicted affiliative behavior approximately 1–6 years later during the juvenile period, using behavioral data from 41 wild blue monkey juveniles and their 29 mothers, and controlling for individual age, sex, and maternal rank. Female juveniles spent less time grooming with any partner and with peers the more maternal grooming they received during infancy, whereas males groomed more with any partner and with peers. Similarly, the more that mothers groomed with other adult females during subjects’ infancy, female subjects played less with peers, and male subjects played more as juveniles. Further, this maternal effect on social behavior appears specific to early life, as the same aspects of mothers’ sociality measured throughout subjects’ development did not predict juvenile behavior. Overall, our results suggest that both direct and indirect experience of mother's affiliative behavior during infancy influence an individual's affiliation later in life that sexes respond differently to the maternal affiliation, and that the first year of life is a critical window.
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Much is known about how the maternal environment can shape offspring traits via intergenerational effects. It is less clear, however, whether such effects may reach adult offspring sexual traits, with potential consequences for sexual selection and speciation. Here, we report effects of adult female aggregation density on the mating signals and mate preferences of their offspring in an insect that communicates via plant-borne vibrational signals. We experimentally manipulated the density of aggregations experienced by egg-laying mothers, reared the offspring in standard densities, and tested for corresponding differences in their signals and preferences. We detected a strong effect in male signals, with sons of mothers that experienced low aggregation density signalling more. We also detected a weak effect on female mate preferences, with daughters of mothers that experienced low aggregation density being less selective. These adjustments may help males and females find mates and secure matings in low densities, if the conditions they encounter correspond to those their mothers experienced. Our results thus extend theory regarding adjustments to the social environment to the scale of intergenerational effects, with maternal social environments influencing the expression of the sexual traits of adult offspring.
more » « less- Award ID(s):
- 1855962
- PAR ID:
- 10565573
- Publisher / Repository:
- Proceedings of the Royal Society B
- Date Published:
- Journal Name:
- Proceedings of the Royal Society B: Biological Sciences
- Volume:
- 291
- Issue:
- 2028
- ISSN:
- 0962-8452
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract -
Understanding the relationship between the environment parents experience during reproduction and the environment embryos experience in the nest is essential for determining the intergenerational responses of populations to novel environmental conditions. Thermal stress has become commonplace for organisms inhabiting areas affected by rising temperatures. Exposure to body temperatures that approach, but do not exceed, upper thermal limits often induces adverse effects in organisms, but the propensity for these temperatures to have intergenerational consequences has not been explored in depth. Here, we quantified the effects of thermal stress on the reproductive physiology and development of brown anoles (Anolis sagrei) when thermal stress is experienced by mothers and by eggs during incubation.Mothers exposed to thermal stress produced smaller eggs and smaller offspring with reduced growth rates, while egg stress reduced developmental time and offspring mass. Hatchling survival and growth were negatively affected by thermal stress experienced by mothers but not by thermal stress experienced as eggs. We found mixed evidence for an additive effect of thermal stress on offspring; rather, thermal stress had specific (and most often negative) effects on different components of offspring phenotypes and fitness proxies when experienced either by mothers or by eggs. Stressful body temperatures therefore can function in a similar manner to other types of maternal effects in reptiles; however, this maternal effect has predominantly negative consequences on offspring.more » « less
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BACKGROUND Charles Darwin’s Descent of Man, and Selection in Relation to Sex tackled the two main controversies arising from the Origin of Species: the evolution of humans from animal ancestors and the evolution of sexual ornaments. Most of the book focuses on the latter, Darwin’s theory of sexual selection. Research since supports his conjecture that songs, perfumes, and intricate dances evolve because they help secure mating partners. Evidence is overwhelming for a primary role of both male and female mate choice in sexual selection—not only through premating courtship but also through intimate interactions during and long after mating. But what makes one prospective mate more enticing than another? Darwin, shaped by misogyny and sexual prudery, invoked a “taste for the beautiful” without speculating on the origin of the “taste.” How to explain when the “final marriage ceremony” is between two rams? What of oral sex in bats, cloacal rubbing in bonobos, or the sexual spectrum in humans, all observable in Darwin’s time? By explaining desire through the lens of those male traits that caught his eyes and those of his gender and culture, Darwin elided these data in his theory of sexual evolution. Work since Darwin has focused on how traits and preferences coevolve. Preferences can evolve even if attractive signals only predict offspring attractiveness, but most attention has gone to the intuitive but tenuous premise that mating with gorgeous partners yields vigorous offspring. By focusing on those aspects of mating preferences that coevolve with male traits, many of Darwin’s influential followers have followed the same narrow path. The sexual selection debate in the 1980s was framed as “good genes versus runaway”: Do preferences coevolve with traits because traits predict genetic benefits, or simply because they are beautiful? To the broader world this is still the conversation. ADVANCES Even as they evolve toward ever-more-beautiful signals and healthier offspring, mate-choice mechanisms and courter traits are locked in an arms race of coercion and resistance, persuasion and skepticism. Traits favored by sexual selection often do so at the expense of chooser fitness, creating sexual conflict. Choosers then evolve preferences in response to the costs imposed by courters. Often, though, the current traits of courters tell us little about how preferences arise. Sensory systems are often tuned to nonsexual cues like food, favoring mating signals resembling those cues. And preferences can emerge simply from selection on choosing conspecifics. Sexual selection can therefore arise from chooser biases that have nothing to do with ornaments. Choice may occur before mating, as Darwin emphasized, but individuals mate multiple times and bias fertilization and offspring care toward favored partners. Mate choice can thus occur in myriad ways after mating, through behavioral, morphological, and physiological mechanisms. Like other biological traits, mating preferences vary among individuals and species along multiple dimensions. Some of this is likely adaptive, as different individuals will have different optimal mates. Indeed, mate choice may be more about choosing compatible partners than picking the “best” mate in the absolute sense. Compatibility-based choice can drive or reinforce genetic divergence and lead to speciation. The mechanisms underlying the “taste for the beautiful” determine whether mate choice accelerates or inhibits reproductive isolation. If preferences are learned from parents, or covary with ecological differences like the sensory environment, then choice can promote genetic divergence. If everyone shares preferences for attractive ornaments, then choice promotes gene flow between lineages. OUTLOOK Two major trends continue to shift the emphasis away from male “beauty” and toward how and why individuals make sexual choices. The first integrates neuroscience, genomics, and physiology. We need not limit ourselves to the feathers and dances that dazzled Darwin, which gives us a vastly richer picture of mate choice. The second is that despite persistent structural inequities in academia, a broader range of people study a broader range of questions. This new focus confirms Darwin’s insight that mate choice makes a primary contribution to sexual selection, but suggests that sexual selection is often tangential to mate choice. This conclusion challenges a persistent belief with sinister roots, whereby mate choice is all about male ornaments. Under this view, females evolve to prefer handsome males who provide healthy offspring, or alternatively, to express flighty whims for arbitrary traits. But mate-choice mechanisms also evolve for a host of other reasons Understanding mate choice mechanisms is key to understanding how sexual decisions underlie speciation and adaptation to environmental change. New theory and technology allow us to explicitly connect decision-making mechanisms with their evolutionary consequences. A century and a half after Darwin, we can shift our focus to females and males as choosers, rather than the gaudy by-products of mate choice. Mate choice mechanisms across domains of life. Sensory periphery for stimulus detection (yellow), brain for perceptual integration and evaluation (orange), and reproductive structures for postmating choice among pollen or sperm (teal). ILLUSTRATION: KELLIE HOLOSKI/ SCIENCEmore » « less
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ABSTRACT In oviparous vertebrates, maternal androgens can alter offspring immune function, particularly early in development, but the potential for negative health effects of maternal androgens in mammals remains unclear. We investigated the relation between maternal androgens, particularly in late gestation, and offspring health in the meerkat (
Suricata suricatta ) by comparing offspring from (a) normative dominant and subordinate matrilines, whose dams naturally express high versus lower circulating androgen concentrations, respectively, and (b) normative dominant and antiandrogen‐treated dominant matrilines, whose dams' androgen function was intact versus blocked owing to experimental antagonism of the latter's androgen receptors (using Flutamide). Foetal offspring thus experienced three different endocrine environments (‘high’, ‘lower’ and ‘blocked’ androgens) late in prenatal development. We assessed parasitism, immune function, sex steroid concentrations and survivorship in these three offspring groups, both during juvenility and early adulthood. The juvenile offspring of subordinate control and dominant treated dams generally had lower intensities of parasite infections and greater immune function than did their peers from dominant control dams—patterns not found in adult offspring, or in relation to the offspring's concurrent hormone concentrations. Survivorship to adulthood was greatest in the progeny of treated dams. Descendants of dominant female meerkats—those in the ‘high’ prenatal androgen category—suffered increased parasitism and decreased immunocompetence as juveniles, as well as reduced survivorship relative to antiandrogen‐exposed peers, providing evidence in mammals that maternal androgens can negatively impact offspring health and survival. These intergenerational, androgen‐mediated, health effects represent early costs imposed by female intrasexual competition and its associated selection pressures. -
Primate offspring often depend on their mothers well beyond the age of weaning, and offspring that experience maternal death in early life can suffer substantial reductions in fitness across the life span. Here, we leverage data from eight wild primate populations (seven species) to examine two underappreciated pathways linking early maternal death and offspring fitness that are distinct from direct effects of orphaning on offspring survival. First, we show that, for five of the seven species, offspring face reduced survival during the years immediately preceding maternal death, while the mother is still alive. Second, we identify an intergenerational effect of early maternal loss in three species (muriquis, baboons, and blue monkeys), such that early maternal death experienced in one generation leads to reduced offspring survival in the next. Our results have important implications for the evolution of slow life histories in primates, as they suggest that maternal condition and survival are more important for offspring fitness than previously realized.more » « less
