In species with giant females, small males are more abundant and have high mortality rates while searching for females7,8. In theory, this leads to increased sperm competition and to male adaptations to monopolize females9. We show that, as predicted from biology of other extremely sexually size-dimorphic spiders, C. darwini males avoid cannibalism by opportunistically mating with teneral females and by mate-binding22,23 (see Supporting Material 1 for review of the evidence in spiders). Furthermore, males engage in strategies to monopolize females via mate guarding, genital mutilation and plugging and emasculation23. However, C. darwini males also engage in oral sexual contact with female genitalia, a hitherto poorly known behavior in spiders whose significance we discuss below.

Female monopolization avoidance mechanisms in spiders include mate choice through precopulatory sexual aggression and cannibalism24, post-copulatory cryptic female choice25 and genital morphologies that decrease male plug effectiveness26. Male genital plugs in C. darwini are deemed inefficient because females readily remate and genital plugs can be removed by subsequent males. Thus, C. darwini males are mono- or at most bigynous, while females likely have a polyandrous mating strategy.

While several phenotypes uncovered by our study fit the predicted evolutionary correlates of female biased sexual size dimorphism, we also found a surprising behavior. Our results suggest that oral sexual contact is an obligate sexual repertoire performed before, between and after copulation with females of any adult stage and condition. With the data at hand, it seems premature to establish a precise adaptive significance of oral sexual contact, but several possibilities are plausible.

Oral sexual contact may function as a cannibalism avoidance mechanism equivalent to mate binding, opportunistic mating with teneral females and remote copulation12,22,27. This seems an unlikely function of oral sexual contact because males perform it with all females regardless of their aggressiveness, including the defenseless teneral ones.

Alternatively, oral sexual contact may function as assessment or manipulation of preexisting mating plugs. An assessment function, however, appears to be unlikely because the behavior is not only performed prior to copulation but also in between bouts and after copulation. A manipulation of plugs is also unlikely because males perform it regardless of females being plugged or not.

We find the following two explanations the most plausible. Oral sexual contact may signal male quality. This would imply the existence of cryptic female choice mechanisms, where females may bias paternity in favor of better quality males25. Additionally, enzymes in the saliva could provide physiological advantage to the donor’s over rival’s sperm. This would be an adaptation for lowering sperm competition and would function analogously to seminal toxins and aggressive sperm known in insects28,29. These two possibilities are intriguing but they require testing that was outside of the scope of this report.

Sexual activities involving the contact of the mouth or mouth parts of one individual with genitals of another, is rare in the animal kingdom. While fellatio-like behaviors were observed in several mammal groups, e.g. macaques, lemurs, bonobos, hyenas, cheetahs, lions, dolphins and bats30,31, cunnilingus-like behaviors are rarer still. In birds, dunnock males peck out rival male’s sperm from the female cloaca32 and among mammals, cunnilingus-like behaviors have been observed in bonobos and have been demonstrated to play an important role in mating of fruit bats33. Males of fruit flies lick female genitals as part of the courtship34,35, which does not influence paternity, but influences the duration of copulation36.

The only other spiders known to exhibit oral sexual encounters are the size dimorphic widows (Latrodectus), where nothing is known about the phenomenon apart from its occurrence, i.e. reports of oral contact and salivation37,38,39. The evidence for precise adaptive function of oral sexual encounters in spiders is currently elusive and therefore specifically designed experiments are to be employed for more precise future tests. Nevertheless, our discovery adds to a more general understanding of how spider sexual dimorphism relates to extreme sexual phenotypes, including male strategies to monopolize females10,40.