Abstract
The role of multiple sexual signals in indicating the timing of female ovulation, and discrimination of this timing by males, has been particularly well studied among primates. However the exhibition of pregnancy signals, and how such signals might modulate male post-conception mating decisions, is still poorly understood. Here we aimed to determine if Japanese macaque males use changes in female sexual signals (behavioral, visual and auditory) to discriminate pregnancy and adjust their socio-sexual behaviors. We combined behavioral observations, digital photography and endocrinological (progestogen and estrogen) data, collected systematically during three one-month periods: the pre-conceptive period, the 1st month of pregnancy and the 2nd month of pregnancy. We analyzed variation in the probability of detecting male and female socio-sexual behaviors and estrus calls, as well as changes in female face color parameters, in relation to female reproductive state. Based on our focal observations, we found that males did not copulate during the pregnancy period, and that female socio-sexual behaviors generally decreased from the pre-conceptive to post-conceptive periods. Female face luminance decreased from the pre-conceptive month to the pregnancy period whereas face color only varied between the 1st and 2nd month of gestation. Our results suggest that Japanese macaque females display sexual cues of pregnancy that males might use to reduce energy wasted on non-reproductive copulations with pregnant females. We hypothesize that females advertize their pregnancy through changes in behavioral, visual and potential auditory signals that males can use to adjust their mating behaviors. We finish by discussing implications for male and female post-conception strategies.
Highlights
Primate males usually concentrate their reproductive efforts towards females during the period of highest conception probability, i.e. the peri-ovulatory or fertile phase of the menstrual cycle [1,2,3,4,5]
The E1C/PdG ratio depended on pregnancy status (LRT: X2 = 11.59,Δdf = 4, P < 0.001, see Table A in S1 File for further details), increasing significantly during the second month of pregnancy compared to the first (GLMM: t = 3.49, P < 0.001, see Table B in S1 File for further details)
Further analyses showed that while progestogen concentrations were significantly different according to reproductive status (LRT: X2 = 7.78, Δdf = 4, P = 0.006), decreasing from the first month of pregnancy to the second month (GLMM: t = -2.06, P = 0.045), concentrations of E1C did not differ (LRT: X2 = 1.71, Δdf = 2, P = 0.43)
Summary
Primate males usually concentrate their reproductive efforts towards females during the period of highest conception probability, i.e. the peri-ovulatory or fertile phase of the menstrual cycle [1,2,3,4,5]. Non-reproductive copulations during pregnancy are not unusual among New World (capuchins: [1]) and Old World (sooty mangabeys: [2,] Hanuman langurs: [3], Phayre’s langurs: [4], rhesus macaques: [5], pig-tailed macaques: [6], stumptailed macaques: [7], Japanese macaques: [8], long-tailed macaques: [9], Assamese macaques: [10], Barbary macaques: [11], chimpanzees: [12], bonobos: [13]) primates Many of these reports were based on observations of mounts, either with or without intromission and ejaculation, collected unsystematically, with inferences made about female reproductive state in the absence of endocrinological confirmation of pregnancy. Without a better understanding of the potential communication of pregnancy status and the potential causes of post-conception mating (i.e. variations in female sexual signals between pre- and post-conception, and their use by males to discriminate the female reproductive state), drawing clear conclusions is impossible
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