The seminal coagulum favours passage of fast-moving sperm into the uterus in the black-handed spider monkey

Abstract

In addition to gametes, mammalian internal fertilisation has required the evolution of assorted anatomical, physiological and biochemical devices to deal with intra-and inter-sexual conflict such as sperm competition and female cryptic choice respectively. The seminal coagulum of primates and other mammals is viewed as one of such devices. Among primates, the seminal coagulum characteristically occurs in multi-male and multi-female species, leading us to suppose that it intervenes in sperm competition. However, it can also provide cues to the female reproductive tract about male desired or undesired traits, and therefore deter or favour sperm survival and migration. The present work investigates whether the seminal coagulum of the black-handed spider monkey enhances sperm fertilisation chances by improving the female reproductive tract conditions, and if the female reproductive tract is 'blind' to semen or behaves selectively towards ejaculates of different males. A series of artificial inseminations were done in five females, using the ejaculates of three different males, one at a time, and measuring the presence of distinct types of sperm inside the uteri at 10, 30 and 60 min following the insemination. The presence of coagulum, menstrual phase, and male and female identity only affected fast, straightmoving sperm, with larger amounts of fast sperm appearing inside the uteri when ejaculates had seminal coagulum, as well as when in the periovulatory phase. There was great intra-uterine fast-sperm variation regarding which male's semen inseminated which female. The results provide evidence to account for sexual conflict in the spider monkey as well as a methodological approach to this kind of study.

Testicular volume and semen characteristics in the endangered southern muriqui (Brachyteles arachnoides)

“…The observed semen pH (7.7) was similar to that reported in other Neotropical primate species, in semen from C goeldii (7.61) and C jacchus (7.6), and lower than that described in A caraya (8.9 and 8.1) and A geoffroyi (8.0) . Semen pH is dictated by the balance between accessory glands secretions’ pH, mostly alkaline secretions from seminal vesicles and acidic secretions from prostate .…”

Copulatory and Postcopulatory Sexual Selection in Primates

“…Some caution is advisable, however, as it transpires that human vaginal pH is exceptionally low, averaging 4.5, as compared to pH values of 7.6 (Macaca nemestrina), 5.0-5.6 (Papio anubis), 5.5 (P. cynocephalus) and 6.5 (A. geoffroyi) at around the time of the oestrogen peak [Miller et al, 2016]. Nonetheless, in the last of the species listed (the black-handed spider monkey, A. geoffroyi), Hernández-López et al [2008] have demonstrated positive effects of the presence of a seminal coagulum upon vaginal pH (increased to 7.0) and the migration of fast linearly moving sperm into the uterus following intravaginal artificial insemination procedures. They concluded that "although still far from being compelling evidence of female cryptic choice in the spider monkey, our results acknowledge that sperm selection starts as early as the vagina, where females seemingly rely on cues provided by the seminal coagulum in favouring or opposing sperm migration."…”

“…For example, mouse lemurs, ring-tailed lemurs, lorises, black-handed spider monkeys, muriquis and chimpanzees all produce copulatory plugs, and all of these species have polygynandrous mating systems . Hernández-López et al [2008] have shown that, in black-handed spider monkeys (Ateles geoffroyi), the copulatory plug promotes the passage of highly motile, linearly moving sperm through the cervix. The plug also serves to buffer pH and to raise the temperature of the vagina.…”

Factors Affecting the Distribution of Copulatory Plugs in Rhesus Monkeys (Macaca mulatta) on Cayo Santiago

“…Poiani [2006] suggests that the female reproductive tract and seminal fluid act as a co-evolved system; the female reproductive tract may be both enabled and inhibited by the various molecular components of seminal fluid. Hernandez-Lopez et al [2008] found that among blackhanded spider monkeys, seminal fluid effectively changes vaginal chemistry, making the female reproductive tract more hospitable for sperm and therefore fertilization. As pregnancy advances, a large amount of cervical mucus blocks off the entrance to the cervix [Hafez and Jaszczak, 1972].…”

“…Although the evolutionary and physiological mechanisms are not fully understood, copulatory plugs are thought to facilitate the reproductive success of particular males [Dixson and Anderson, 2002] and may have evolved in response to intersexual conflict [Hernandez-Lopez et al, 2008]. Previous research on copulatory plugs has traditionally focused on the facilitation of fertilization by preventing sperm leakage, slowing sperm Distribution of Macaque Copulatory Plugs 265 Folia Primatol 2009;80:264-274 release and helping sperm to reach the cervix; other hypotheses have focused on male-male competition and reproductive strategies, suggesting that copulatory plugs may serve as an obstacle for subsequent males [for a review, see Voss, 1979].…”