Macaque Fertility Signals

Abstract

Females of many animal species exhibit signals of fertility, but few animal groups do so with such prevalence, diversity of signal types, and variability between closely related species, as anthropoid primates. An excellent group for studying the evolution of such signals is the macaques, a group of some 22 species of Old World monkey. The macaques exhibit the same general mating system, but a great amount of inter‐specific variation in the type and number of different signals they display. In this article, we discuss the evolution of these traits, including the types of variation in fertility that they may indicate and the hormonal mechanisms that underlie them. We discuss the different signals that macaques exhibit, and review the distribution and abundance of these signals across species. Even closely related species differ in the type and number of signals displayed, as well as in their apparent accuracy in reflecting the timing of female ovulation. We offer some potential explanations for this variation, though much is still poorly understood. We finish by discussing future directions for research that are likely to prove fruitful.

Key Concepts

  • Females of many anthropoid primates, including macaques, exhibit signals of fertility.
  • Macaque signals of fertility include swellings of the hindquarters, changes in facial colour, olfactory signals, and auditory oestrus and copulation calls.
  • Three types of variation in fertility might potentially be communicated to others: intra‐cycle variation in the probability of ovulation; inter‐cycle, intra‐female variation in the probability of conception in that cycle, and inter‐female differences in overall fecundity.
  • The expression of intra‐cycle signals of the probability of ovulation is linked to the hormones oestrogen (positively) and progesterone (negatively).
  • There is a great deal of inter‐specific variation in the presence and type of fertility signals shown, as well as in their apparent accuracy in reflecting ovulatory function.
  • Though we understand some of the evolutionary pressures that may have led to inter‐specific variation, the sources of much of the variation remain unclear.

Keywords: primate; macaque; reproduction; sexual behaviour; communication; signalling; colouration

Figure 1. Examples of the diversity of macaque signals that might potentially be informative about female fertility. Signals are often exhibited in multiple sensory modalities: (a) rhesus macaque (M. mulatta) face colouration (photo credit: Constance Dubuc); (b) crested macaque (M. nigra) sexual swelling, combined with female presentation (a behavioural signal), and with male inspection, potentially of olfactory signals (photo credit: Jerome Micheletta; Macaca Nigra Project); (c) sonogram of a Barbary macaque copulation call (photo credit: Stuart Semple).
Figure 2. Diversity in visual anogenital signals among macaques collected from different free‐ranging and wild populations: (a) Presumed ancestral state of sexual swelling exhibited by wild Barbary macaques (Macaca sylvanus) (photo credit: Laetitia Maréchal). (b,c) Large and colourful swellings exhibited by wild pig‐tailed macaques (M. nemestrina) (photo credit: Antje Engelhardt) and wild female crested macaques (M. nigra) (photo credit: Macaca Nigra Project). (d–f) Derived loss of sexual swelling in wild Assamese macaques (M. assamensis) (photo credit: Assamese Macaque Project Phu Khieo), wild long‐tailed macaques (M. fascicularis) (photo credit: Antje Engelhardt) and provisioned free‐ranging rhesus macaques (M. mulatta) (photo credit: Constance Dubuc). (g,h) In several species, sexual skin swells only or mainly in nulliparous and young females, here illustrated by long‐tailed (photo credit: Antje Engelhardt) and rhesus macaques (photo credit: Constance Dubuc).
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Further Reading

Darwin C (1872) The Descent of Man and Selection in Relation to Sex. London, UK: John Murray.

Dixson AF (2012b) Primate Sexuality: Comparative Studies of Prosimians, Monkeys, Apes, and Human Beings, 2nd edn. Oxford, UK: Oxford University Press.

Jones CB (ed) (2003) Sexual Selection and Reproductive Competition in Primates: New Perspectives and Directions. Norman, OK: American Society of Primatologists.

Kappeler P and van Schaik C (2004) Sexual Selection in Primates. Cambridge, MA: Cambridge University Press.

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Higham, James P, and Dubuc, Constance(May 2015) Macaque Fertility Signals. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0024968]