Sexual signalling in female crested macaques and the evolution of primate fertility signals

James Higham, Michael Heistermann, Carina Saggau, Muhammad Agil, Dyah Perwitasari-Farajallah, Antje Engelhardt

    Research output: Contribution to journalArticle

    Abstract

    Background: Female signals of fertility have evolved in diverse taxa. Among the most interesting study systems are those of multimale multifemale group-living primates, where females signal fertility to males through multiple signals, and in which there is substantial inter-specific variation in the composition and reliability of such signals. Among the macaques, some species display reliable behavioural and/or anogenital signals while others do not. One cause of this variation may be differences in male competitive regimes: some species show marked sexual dimorphism and reproductive skew, with males fighting for dominance, while others show low dimorphism and skew, with males queuing for dominance. As such, there is variation in the extent to which rank is a reliable proxy for male competitiveness, which may affect the extent to which it is in females interest to signal ovulation reliably. However, data on ovulatory signals are absent from species at one end of the macaque continuum, where selection has led to high sexual dimorphism and male reproductive skew. Here we present data from 31 cycles of 19 wild female crested macaques, a highly sexually dimorphic species with strong mating skew. We collected measures of ovarian hormone data from faeces, sexual swelling size from digital images, and male and female behaviour. Results: We show that both sexual swelling size and female proceptivity are graded-signals, but relatively reliable indicators of ovulation, with swelling size largest and female proceptive behaviours most frequent around ovulation. Sexual swelling size was also larger in conceptive cycles. Male mating behaviour was well timed to female ovulation, suggesting that males had accurate information about this. Conclusion: Though probabilistic, crested macaque ovulatory signals are relatively reliable. We argue that in species where males fight over dominance, male dominance rank is surrogate for competitiveness. Under these circumstances it is in the interest of females to increase paternity concentration and assurance in dominants beyond levels seen in species where such competition is less marked. As such, we suggest that it may in part be variation in male competitive regimes that leads to the evolution of fertility signalling systems of different reliability.

    Original languageEnglish (US)
    Article number89
    JournalBMC Evolutionary Biology
    Volume12
    Issue number1
    DOIs
    StatePublished - 2012

    Fingerprint

    Macaca
    primate
    fertility
    Primates
    swelling
    ovulation
    female behavior
    male behavior
    dominance (genetics)
    sexual dimorphism
    competitiveness
    interspecific variation
    mating behavior
    dimorphism
    paternity
    overdominance
    fighting
    digital image
    feces
    digital images

    Keywords

    • Fertility signals
    • Primate
    • Sexual selection
    • Sexual swellings

    ASJC Scopus subject areas

    • Ecology, Evolution, Behavior and Systematics

    Cite this

    Higham, J., Heistermann, M., Saggau, C., Agil, M., Perwitasari-Farajallah, D., & Engelhardt, A. (2012). Sexual signalling in female crested macaques and the evolution of primate fertility signals. BMC Evolutionary Biology, 12(1), [89]. https://doi.org/10.1186/1471-2148-12-89

    Sexual signalling in female crested macaques and the evolution of primate fertility signals. / Higham, James; Heistermann, Michael; Saggau, Carina; Agil, Muhammad; Perwitasari-Farajallah, Dyah; Engelhardt, Antje.

    In: BMC Evolutionary Biology, Vol. 12, No. 1, 89, 2012.

    Research output: Contribution to journalArticle

    Higham, J, Heistermann, M, Saggau, C, Agil, M, Perwitasari-Farajallah, D & Engelhardt, A 2012, 'Sexual signalling in female crested macaques and the evolution of primate fertility signals', BMC Evolutionary Biology, vol. 12, no. 1, 89. https://doi.org/10.1186/1471-2148-12-89
    Higham J, Heistermann M, Saggau C, Agil M, Perwitasari-Farajallah D, Engelhardt A. Sexual signalling in female crested macaques and the evolution of primate fertility signals. BMC Evolutionary Biology. 2012;12(1). 89. https://doi.org/10.1186/1471-2148-12-89
    Higham, James ; Heistermann, Michael ; Saggau, Carina ; Agil, Muhammad ; Perwitasari-Farajallah, Dyah ; Engelhardt, Antje. / Sexual signalling in female crested macaques and the evolution of primate fertility signals. In: BMC Evolutionary Biology. 2012 ; Vol. 12, No. 1.
    @article{796ce836c86e42d4888eb0ab3101ec2a,
    title = "Sexual signalling in female crested macaques and the evolution of primate fertility signals",
    abstract = "Background: Female signals of fertility have evolved in diverse taxa. Among the most interesting study systems are those of multimale multifemale group-living primates, where females signal fertility to males through multiple signals, and in which there is substantial inter-specific variation in the composition and reliability of such signals. Among the macaques, some species display reliable behavioural and/or anogenital signals while others do not. One cause of this variation may be differences in male competitive regimes: some species show marked sexual dimorphism and reproductive skew, with males fighting for dominance, while others show low dimorphism and skew, with males queuing for dominance. As such, there is variation in the extent to which rank is a reliable proxy for male competitiveness, which may affect the extent to which it is in females interest to signal ovulation reliably. However, data on ovulatory signals are absent from species at one end of the macaque continuum, where selection has led to high sexual dimorphism and male reproductive skew. Here we present data from 31 cycles of 19 wild female crested macaques, a highly sexually dimorphic species with strong mating skew. We collected measures of ovarian hormone data from faeces, sexual swelling size from digital images, and male and female behaviour. Results: We show that both sexual swelling size and female proceptivity are graded-signals, but relatively reliable indicators of ovulation, with swelling size largest and female proceptive behaviours most frequent around ovulation. Sexual swelling size was also larger in conceptive cycles. Male mating behaviour was well timed to female ovulation, suggesting that males had accurate information about this. Conclusion: Though probabilistic, crested macaque ovulatory signals are relatively reliable. We argue that in species where males fight over dominance, male dominance rank is surrogate for competitiveness. Under these circumstances it is in the interest of females to increase paternity concentration and assurance in dominants beyond levels seen in species where such competition is less marked. As such, we suggest that it may in part be variation in male competitive regimes that leads to the evolution of fertility signalling systems of different reliability.",
    keywords = "Fertility signals, Primate, Sexual selection, Sexual swellings",
    author = "James Higham and Michael Heistermann and Carina Saggau and Muhammad Agil and Dyah Perwitasari-Farajallah and Antje Engelhardt",
    year = "2012",
    doi = "10.1186/1471-2148-12-89",
    language = "English (US)",
    volume = "12",
    journal = "BMC Evolutionary Biology",
    issn = "1471-2148",
    publisher = "BioMed Central",
    number = "1",

    }

    TY - JOUR

    T1 - Sexual signalling in female crested macaques and the evolution of primate fertility signals

    AU - Higham, James

    AU - Heistermann, Michael

    AU - Saggau, Carina

    AU - Agil, Muhammad

    AU - Perwitasari-Farajallah, Dyah

    AU - Engelhardt, Antje

    PY - 2012

    Y1 - 2012

    N2 - Background: Female signals of fertility have evolved in diverse taxa. Among the most interesting study systems are those of multimale multifemale group-living primates, where females signal fertility to males through multiple signals, and in which there is substantial inter-specific variation in the composition and reliability of such signals. Among the macaques, some species display reliable behavioural and/or anogenital signals while others do not. One cause of this variation may be differences in male competitive regimes: some species show marked sexual dimorphism and reproductive skew, with males fighting for dominance, while others show low dimorphism and skew, with males queuing for dominance. As such, there is variation in the extent to which rank is a reliable proxy for male competitiveness, which may affect the extent to which it is in females interest to signal ovulation reliably. However, data on ovulatory signals are absent from species at one end of the macaque continuum, where selection has led to high sexual dimorphism and male reproductive skew. Here we present data from 31 cycles of 19 wild female crested macaques, a highly sexually dimorphic species with strong mating skew. We collected measures of ovarian hormone data from faeces, sexual swelling size from digital images, and male and female behaviour. Results: We show that both sexual swelling size and female proceptivity are graded-signals, but relatively reliable indicators of ovulation, with swelling size largest and female proceptive behaviours most frequent around ovulation. Sexual swelling size was also larger in conceptive cycles. Male mating behaviour was well timed to female ovulation, suggesting that males had accurate information about this. Conclusion: Though probabilistic, crested macaque ovulatory signals are relatively reliable. We argue that in species where males fight over dominance, male dominance rank is surrogate for competitiveness. Under these circumstances it is in the interest of females to increase paternity concentration and assurance in dominants beyond levels seen in species where such competition is less marked. As such, we suggest that it may in part be variation in male competitive regimes that leads to the evolution of fertility signalling systems of different reliability.

    AB - Background: Female signals of fertility have evolved in diverse taxa. Among the most interesting study systems are those of multimale multifemale group-living primates, where females signal fertility to males through multiple signals, and in which there is substantial inter-specific variation in the composition and reliability of such signals. Among the macaques, some species display reliable behavioural and/or anogenital signals while others do not. One cause of this variation may be differences in male competitive regimes: some species show marked sexual dimorphism and reproductive skew, with males fighting for dominance, while others show low dimorphism and skew, with males queuing for dominance. As such, there is variation in the extent to which rank is a reliable proxy for male competitiveness, which may affect the extent to which it is in females interest to signal ovulation reliably. However, data on ovulatory signals are absent from species at one end of the macaque continuum, where selection has led to high sexual dimorphism and male reproductive skew. Here we present data from 31 cycles of 19 wild female crested macaques, a highly sexually dimorphic species with strong mating skew. We collected measures of ovarian hormone data from faeces, sexual swelling size from digital images, and male and female behaviour. Results: We show that both sexual swelling size and female proceptivity are graded-signals, but relatively reliable indicators of ovulation, with swelling size largest and female proceptive behaviours most frequent around ovulation. Sexual swelling size was also larger in conceptive cycles. Male mating behaviour was well timed to female ovulation, suggesting that males had accurate information about this. Conclusion: Though probabilistic, crested macaque ovulatory signals are relatively reliable. We argue that in species where males fight over dominance, male dominance rank is surrogate for competitiveness. Under these circumstances it is in the interest of females to increase paternity concentration and assurance in dominants beyond levels seen in species where such competition is less marked. As such, we suggest that it may in part be variation in male competitive regimes that leads to the evolution of fertility signalling systems of different reliability.

    KW - Fertility signals

    KW - Primate

    KW - Sexual selection

    KW - Sexual swellings

    UR - http://www.scopus.com/inward/record.url?scp=84862266709&partnerID=8YFLogxK

    UR - http://www.scopus.com/inward/citedby.url?scp=84862266709&partnerID=8YFLogxK

    U2 - 10.1186/1471-2148-12-89

    DO - 10.1186/1471-2148-12-89

    M3 - Article

    C2 - 22708622

    AN - SCOPUS:84862266709

    VL - 12

    JO - BMC Evolutionary Biology

    JF - BMC Evolutionary Biology

    SN - 1471-2148

    IS - 1

    M1 - 89

    ER -