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Reproductive Suppression in Female Primates: a Review

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Reproductive Suppression in Female Primates: a Review Evolutionary Anthropology 22:226–238 (2013) ARTICLE Reproductive Suppression in Female Primates: A Review JACINTA C. BEEHNER AND AMY LU Reproductive performance is the currency of evolution. All things being equal, A comprehensive review of the an organism should reproduce as often as possible. The puzzling questions in evo- reproductive suppression model is lutionary biology, therefore, are not how and why an organism does reproduce, not possible here. Therefore, we but rather how and why an organism does not reproduce. It is difficult to under- restrict this review in three impor- stand why any individual, particularly a female, might forestall reproduction when tant ways. First, we focus on within- one of the biggest limitations for female mammalian reproduction is time (that is, population comparisons and exam- reproductive lifespan).1 The answer, now widely cited throughout behavioral ecol- ine why one female might reproduce ogy is quite simple: Reproductive suppression can be an adaptive strategy.2 successfully while another in the same population might not. Between-species comparisons that Mammalian female reproduction females may increase their lifetime explore life-history evolution across is a costly endeavor that may have a reproductive success by restricting taxa have received excellent coverage 1 high chance of failure under subopti- reproduction to coincide with favor- elsewhere. mal circumstances. Therefore, over able conditions. Thus, the general Second, although we briefly review evolutionary time, natural selection rule of thumb is this: If prevailing the energetic causes of reproductive should have favored females that are conditions are poor, delay reproduc- suppression, we focus primarily on sensitive to environmental cues and tion to preserve energy for future social causes (Fig. 1). Certainly, a able to suppress their own reproduc- reproduction; if conditions are likely female’s physiology should be sensi- tion when current prospects for to remain the same or get worse, tive to all cues that indicate harsh reproductive success are poor. This carry on with reproduction. reproductive conditions: their own idea, known as the reproductive sup- Several assumptions are associated energy balance and health, the physi- pression model,2 maintains that with this model.2 First, female repro- cal and genetic status of their embryo or fetus, and the local envi- duction should be sensitive to all 3 cues that are predictive of poor ronmental conditions. But social reproductive outcomes and natural pressures are among the most dra- Jacinta C. Beehner is an Associate Pro- selection should favor females that matic and least understood factors fessor in the Departments of Anthropol- are able to translate these cues cor- affecting female reproduction. ogy and Psychology at the University of Third, in the spirit of this special Michigan. She is broadly interested in rectly into reproductive decisions. the interactions between hormones and Second, females should suppress issue, we would like to highlight the animal behavior, with a particular empha- work by Jeanne Altmann and Sarah sis on reproductive strategies in female reproduction as soon as a cue is primates. available because the earlier the loss, Hrdy, who have substantially furth- Amy Lu is a postdoctoral fellow in the the less it affects a female’s subse- ered our understanding of reproduc- Department of Anthropology at the Uni- tive suppression. In her versity of Illinois Urbana-Champaign. quent reproduction. Third, females She is interested in socioendocrinology, should use only cues that reliably groundbreaking work with wild yel- sexual selection, and development. Her low baboons in Amboseli National current research focuses on socially predict poor reproductive perform- mediated maturation and associated life- ance because it is costly to suppress Park, Kenya, Jeanne Altmann has history tradeoffs in wild geladas. a reproductive event that would oth- demonstrated that living in a erwise have been successful. Fourth, resource-poor and unpredictable Key words: anovulation; energetic suppression; reproductive suppression should be environment can have dramatic con- fertility; ovulatory suppression; pregnancy loss; regulated by the female herself, and sequences on female fitness across 4–9 reproductive failure; social suppression thus differs from the more general the life span. Similarly, Sarah Hrdy term “reproductive failure,” which has established much of the ground- VC 2013 Wiley Periodicals, Inc. also includes externally imposed work for testing hypotheses related to DOI: 10.1002/evan.21369 sources of loss, such as disease, social suppression in female primates Published online in Wiley Online Library (wileyonlinelibrary.com). injury, or infanticide. through her empirical work with the ARTICLE Reproductive Suppression in Female Primates 227 ENERGETIC SUPPRESSION Mammalian female reproduction requires a great deal of energy.16 When food is limited or entails high acquisition costs, organisms must make allocation decisions to priori- tize the partitioning of metabolic fuels. For many long-lived organisms, individual survival is paramount thus, when energy is at a minimum, basic cellular processes critical for survival take precedence over proc- esses that can be compromised, such as reproduction.17 However, even when survival is not at stake, females should abandon reproductive efforts as soon as they detect that they do not have enough energy to complete them. Energetic suppression is defined as the self-imposed inhibition of reproductive physiology in other- wise fertile individuals in response to an internal metabolic cue that indi- Figure 1. Routes to reproductive suppression. It has been notoriously difficult to separate cates a poor reproductive outcome. rank-related reproductive dysfunction caused directly by elevated levels of social stress To be clear, “self-imposed inhibition” from that caused indirectly by nutritional insufficiencies. Here, we focus mainly on empiri- does not involve any conscious deci- cal studies in primates that have demonstrated a direct link between the social environ- sion by the female, but is mediated by ment and female reproductive failure (red arrow). Note that although dominance rank a metabolic signal triggered in is a component of the social environment, it can mediate fitness in two ways: through the ecological environment (for example, by restricting energy intake, increasing energy response to an appropriate cue. The expenditure, or both) and through the social environment (for example, via social stress specifics that underlie this metabolic or social suppression of subordinates). [Color figure can be viewed in the online issue, pathway have yet to be fully identi- which is available at wileyonlinelibrary.com.] fied, but it is becoming increasingly clear that integrative control of energy balance and reproduction is Hanuman langurs of Mt. Abu, pression via neuroendocrine mecha- carried out by multiple metabolic and India,10,11 and her theoretical ideas nisms. In some cases, these are one neuroendocrine signals. Research on about infanticide.12–14 and the same; the factors that serve how females suppress reproduction In what follows, we provide an as proximate cues indicating a sub- in response to energetic signals is still overview of reproductive suppres- optimal environment are the same rapidly developing, and we refer read- sion in female primates, paying ones that trigger reproductive sup- ers to recent reviews of this topic.17,18 particular attention to two different pression (for example, poor ener- The question of why females sup- levels of analysis: an ultimate (func- getic condition). In most cases, press reproduction in response to tional) and a proximate (mechanis- however, the cues that reliably pre- limited energy is easier to tackle. tic) perspective (Fig. 2). From a dict reproductive failure are not Energetic suppression is common in functional perspective, we ask why inherently linked to reproductive females suppress their own repro- suppression (for example, the species in which physical condition arrival of a new male). In the inter- must meet a threshold before initiat- duction. That is, what are the fit- 19 ness benefits? To answer this est of bridging function and mecha- ing reproduction (capital breeders). question, we review the consequen- nism, we focus on both the cues as This energetic threshold presumably ces of reproducing under conditions well as the specific neuroendocrine indicates whether a mother will be in which the prospects for success mechanisms. We ask “why” and able to partition the necessary are poor. Second, from a proximate “how” questions as two related lines energy to reproduction on an perspective, we ask how females of inquiry. Just as the blind man ongoing basis. In contrast, other spe- suppress their own reproduction. cannot completely describe an ele- cies exclusively rely on external cues That is, what mechanisms are phant by holding onto its tail, we to initiate reproduction (income involved? There are two ways to specifically hope to emphasize how breeders). These external cues enable answer this question. We can integrating answers at different lev- females to schedule more energeti- explore the cues themselves or how els can help us emerge with a bet- cally demanding stages of reproduc- we can examine these cues are ter understanding of reproductive tion with a reliable and predictable translated into reproductive sup- suppression in female primates. abundance
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