Homosexual acts may help impair reproduction by rivals --- for example, a male imitating a female

Male reproductive suppression: not a social affair- Z. Valentina Zizzari, Andrea Jessen, and Joris M. Koene. Current Zoology, Volume 63, Issue 5, 1 October 2017, Pages 573–579, https://doi.org/10.1093/cz/zow089

Abstract: In the animal kingdom there are countless strategies via which males optimize their reproductive success when faced with male–male competition. These male strategies typically fall into two main categories: pre- and post-copulatory competition. Within these 2 categories, a set of behaviors, referred to as reproductive suppression, is known to cause inhibition of reproductive physiology and/or reproductive behavior in an otherwise fertile individual. What becomes evident when considering examples of reproductive suppression is that these strategies conventionally encompass reproductive interference strategies that occur between members of a hierarchical social group. However, mechanisms aimed at impairing a competitor’s reproductive output are also present in non-social animals. Yet, current thinking emphasizes the importance of sociality as the primary driving force of reproductive suppression. Therefore, the question arises as to whether there is an actual difference between reproductive suppression strategies in social animals and equivalent pre-copulatory competition strategies in non-social animals. In this perspective paper we explore a broad taxonomic range of species whose individuals do not repeatedly interact with the same individuals in networks and yet, depress the fitness of rivals. Examples like alteration of male reproductive physiology, female mimicry, rival spermatophore destruction, and cementing the rival’s genital region in non-social animals, highlight that male pre-copulatory reproductive suppression and male pre-copulatory competition overlap. Finally, we highlight that a distinction between male reproductive interference in animals with and without a social hierarchy might obscure important similarities and does not help to elucidate why different proximate mechanisms evolved. We therefore emphasize that male reproductive suppression need not be restricted to social animals.

Keywords: indirect sperm transfer, offensive strategies, male pre-copulatory competition, male reproductive suppression, reproductive strategies

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The examples of reproductive interference in Table 1 show that males of non-social animals are able to depress the fitness of a rival, though some behaviors are more harmful than others. For instance, nematodes of the genus Steinernema remove a rival from the reproductive population by killing him (Zenner et al. 2014). Less extreme examples are provided by males of acanthocephalans and some nematodes, whose males have been observed to perform a homosexual rape or place a cement plug on the rivals’ reproductive organ making them incapable of reproducing at least temporarily (Hassanine and Al-Jahdali 2008; Gems and Riddle 2000; Coomans et al. 1988). Although several instances of same-sex sexual behaviour are suspected of being related to male dominance in vertebrates, such behaviours are often attributed to cases of mistaken identity in invertebrates (see review by Bailey and Zuk 2009). Yet, Preston-Mafham (2006) excluded that the homosexual mounting behaviour he observed in the scatophagid fly Hydromyza livens occurred through mistaken identity. Male-male sexual behaviour is a widespread phenomenon that needs certainly a more accurate analysis because there might be species where this represents a strategy to increase male reproductive success, as suggested in the hemipteran Xylocoris maculipennis (Carayon 1974) and in the flour beetle Tribolium castaneum (Levan et al. 2009). Males of X. maculipennis have been reported to traumatically inseminate other males and it has been hypothesized that the injected ejaculate (i.e., seminal fluid plus sperm) mixes up with the ejaculate of the inseminated male (Carayon 1974), although this remains to be demonstrated. So, while it remains unknown whether sperm from both males actually inseminate the female in the latter case, the transferred seminal fluid proteins could also act on the reproductive physiology of the inseminated male, similarly to what was discovered in L. stagnalis (Nakadera et al. 2014). More information is available for T. castaneum. Levan et al. (2009) showed that male homosexual copulatory behaviour may lead to indirect sperm transfer to females through a male intermediary. Although the male’s homosexual partner contributed only 0.5% to each female’s total progeny (Levan et al. 2009), the transfer of a small quantity of non-self sperm might decrease a males’ reproductive success. Alternatively, albeit speculatively, a male might be induced to perform a same-sex encounter by female mimicry of a rival to make the mounting male temporary unable to inseminate a female, which has been described in salamanders (Arnold 1976). In this case the indirect sperm translocation would represent a male counter-adaption. However, this line of thought has not been taken into account and the homosexual copulation was explained by Levan et al. 2009 as a way to discard older sperm, indicating that more work is required to understand this in full.