Primate Sex and Its Role in Pleasure, Dominance and Communication

Round 1

Reviewer 1 Report

I think this commentary approaches a very interesting and novel subject, regarding sex in primates and highlights several aspects that may change future perspectives regarding animal (specific primate) sexuality and its role in animal populations. I think the authors properly present arguments that sustain several relevant questions to be answered by future research.

However, there are some concerns that I have regarding it:

1) References and citations are not at the format expressed in "Instructions for authors" section. They should numbered and not with author-date format (https://www.mdpi.com/journal/animals/instructions#references)

2) There are some references that I didn't find the correspondent citation in the text such as: "Vaglio, S., Rodriguez Villanueva, M., Ducroix, L., Consiglio, R., Kim, J. A., Neilands, P., 466 Stucky, K. & Lameira, A. (2020) Female copulation calls vary with male ejaculation in 467 captive olive baboons. Behaviour 157(8-9): 807-822.". Only (Vaglio, 2021) appears, which is another reference from the reference list, not (Vaglio, 2020). Please re-check your references and citation for other similar issues.

3) In the middle of the introduction, I became a little bit confused about the purpose of the article. As far as I understand you are focusing sexual interactions and their role in primates (rather than only reproduction and species preservation) as in communication, dominance, social structure...... But in the first two paragraphs of the introduction, you talk about the strict division of sexes, how this can be debatable and introduce other topis and facts as hermaphrodites. I think that would be another discussion not so related with the one you are having here, so I do not think this should introduce your commentary.

4) This is more like a suggestion for your commentary. There are several primates with matriarchal (bonobos, lemurs...) rather than patriarchal social structures. Do sexual behaviours and the role of sex suffer significant changes depending on this? It would be important to comment on the subject as well, even if it was a small address of the topic.

Author Response

Please see the attachment.

Author Response File: Author Response.pdf

Reviewer 2 Report

This paper aims to review the functions of non-conceptive of sex in primates, as well as the mechanisms and evolutionary significance of sexual behaviors that have no chance of producing offspring. Among them, the authors particularly focused on sex for pleasure, dominance, protection from infanticide, reconciliation, and communication.

This is a well-written and informative review that has the potential to contribute to an understudied component of sexual behavior in non-human primates.

My main comment pertains to the fact that the authors did not include some relatively recent publications that focus on the sexual (rather than socio-sexual) nature of numerous non-conceptive sexual behaviors in macaques, with an emphasis on sexual gratification in the form of pleasurable feedback.

If the authors are willing to consider my suggestions below, then I am happy to recommend this manuscript for publication.

 

SUGGESTIONS FOR ADDITIONAL REFERENCES

 

Line 130-132: I believe this statement could benefit from citing additional studies that emphasized the sexual (rather than socio-sexual) nature of numerous non-conceptive sexual behaviors in nonhuman primates, including masturbation, female-female mounting, female-male mounting, and heterosexual mounting in macaques. Suggestions for additional relevant references include (but are not limited to):

 

Cenni C, Christie JBA, Van der Pant Y, Gunst N, Vasey PL, Wandia IN, Leca JB. (2022). Do monkeys use sex toys? Evidence of stone tool-assisted masturbation in free-ranging long-tailed macaques. Ethology, 128(9), 632-646.

 

Gunst N, Leca JB, Vasey PL. (2022). Sexual adaptation: Is female-male mounting a supernormal courtship display in Japanese macaques? Behaviour, 159(11): 999-1027.

 

Leca JB, Gunst N, Ottenheimer Carrier L, Vasey PL. (2014). Inter-group variation in non-conceptive sexual activity in female Japanese macaques: Could it be cultural? Animal Behavior and Cognition, 1(3), 387-409.

 

LL 135 and the entire Section #3: When addressing sex for pleasure, it’s almost impossible to skip Paul Vasey’s foundational research on female-female homosexual behavior and its hedonic component, including the following references:

 

Vasey, P. L. (2006). The pursuit of pleasure: Homosexual behaviour, sexual reward and evolutionary history in Japanese macaques. In V. Sommer & P. L. Vasey (Eds.), Homosexual behaviour in animals: An evolutionary perspective (pp. 191–219). Cambridge: Cambridge University Press.

 

Vasey, P. L., & Duckworth, N. (2006). Sexual reward via vulvar, perineal and anal stimulation: A proximate mechanism for female

homosexual mounting in Japanese macaques. Archives of Sexual Behavior, 35, 52–532.

 

Vasey, P. L., Foroud, A., Duckworth, N., & Kovacovsky, S. D. (2006). Male-female and female–female mounting in Japanese macaques: A comparative analysis of posture and movement. Archives of Sexual Behavior, 35, 116–128.

 

Vasey, P. L., & VanderLaan, D.P. (2012). Is female homosexual behaviour in Japanese macaques truly sexual? In J.-B. Leca, M.A. Huffman, & P. L. Vasey (Eds.), The monkeys of stormy mountain: 60 years of primatological research on the Japanese macaques of Arashiyama (pp. 153–172). Cambridge: Cambridge University Press.

 

LL223 and the entire Section #5: When addressing sex as a means of communication with a focus on reconciliation, it’s almost impossible to miss the highly conspicuous socio-sexual behaviors performed by stumptailed macaques during post-conflict reunions. One example of such studies is:

 

Call J, Aureli F, de Waal FBM. (2002). Postconflict third-affiliation affiliation in stumptailed macaques. Animal Behaviour, 63(2), 209-216.

 

Minor comments:

Line 1: Please remove the final stop at the end of the title.

 

Line 17: “in pedagogical contexts” – What do you mean exactly? In the classroom, including sex-related teaching activities? Please explain the relevance of this specific note. What about research contexts? 

Author Response

Please see the attachment.

Author Response File: Author Response.pdf

Reviewer 3 Report

This paper covers an important topic. Why do primate species engage in sexual behavior that is outside the female’s fertility period? The authors summarize the argument under 4 categories:

Non-conceptive sex; sex for pleasure; sex for dominance and infanticide protection; and sex as communication (for relationship building and restoration).

However, these important topics are covered in just 4.5 pages of text and thus the coverage is broad and superficial rather than deep. I think the paper will be much more useful in several ways:

First is there any relationship between the type of social or mating system and the form of sex outside of fertility? It seems that relationship strength might be more important to biparental and cooperatively breeding species than other systems. In contrast, sex for paternity confusion and infanticide protection may be more common in species without long term close relationships among males and females.

Second, the authors mention inly briefly the hormonal mechanisms that could be involved and there is an abundant literature on potential reward mechanisms of sex. Several German studies have reported pulses of prolactin and oxytocin at orgasm in both men and women. Correlational studies have shown that pairs of tamarins with greater sexual activity have higher levels of both prolactin and oxytocin. Oxytocin is often written about as a “feel-good” hormone and prolactin inhibits dopamine. Since dopamine is present in the “wanting” stage of motivated behavior, prolactin (and perhaps oxytocin) can be seen as the “Liking” stage. Experimental studies have injected or infused oxytocin into primates.

Third, another source of evidence for the reward function of sex are studies on sexual conditioning. For example, marmosets can be conditioned to expect sex when exposed to a novel odor (Lemon) and in test trials show erections in response to lemon odors alone with no partner present. The ability to condition a sexual response based on sexual reward is a clear indication of pleasure.

Fourth, the authors call attention to some of the problems of using noninvasive measures and these are real, but surmountable. The great majority of primate species are classified as vulnerable to critically endangered, so minimally invasive measures are critical. Furthermore, many hormones are released as pulses into the bloodstream so serum measures may be less accurate than urinary measures with the bladder serving to integrate hormonal release over time.

Fifth, sex outside of fertility can be used to restore or repair relationships. Biparental and cooperatively breeding show signs of increased sexual activity following presentation of an intruder or the odors of a novel ovulating female, or short separations, suggesting that sex is one way to repair a relationship under stress.

Sixth, I did not see any mention of the concealed ovulation hypothesis which has been very popular. Ovulation may be concealed to the scientist but obvious to the males being tested, but nonetheless, this has been a useful hypothesis for considering the advantage of non-conceptive sex, not in confusing paternity, but cementing the male’s commitment.

In summary, this is a very interesting topic that needs to be publicized, but the current version is underdeveloped and would be of much greater importance, if it were expanded along the lines given above.

Author Response

Please see the attachment.

Author Response File: Author Response.pdf

Round 2

Reviewer 1 Report

The authors addressed all the topics I mentioned in my review report and properly correct them in this second version of the manuscript. Therefore, I have nothing to add.

Author Response

Yes, we can confirm that we have addressed all the reviewer comments. We thank the reviewer very much for their comments and useful suggestions which have helped us prepare a, we believe, much improved report.

Reviewer 3 Report

If imitation is the sincerest form of flattery, the authors have clearly flattered me. Not only have the incorporated my suggestions, the have copied them verbatim into the text without quotation marks or any paraphrasing or text changes. This comes close to plagiarism. Moreover, my comments are not always in the proper place-ll. 139-152 are really about sex as reward yet are in the section on nonconceptive sex. The material about the utility of hormonal assays appears in ll. 168-172 but the results of hormonal studies appeared much earlier. This does not make for a clear flow.

Ll. 190-194 talk of paternity confusion, yet this is a different conceptual topic from sex for pleasure and so is out of place.

ll. 203-209 talk about a need for studies to document pleasure, yet the material cited earlier on conditioning and oxytocin would seem more useful here.

The material beginning on l. 226 about infanticide deserves a separate paragraph since it introduces a new topic. There is a need for another paragraph break later in this long paragraph.

ll. 262-265 are another verbatim quote from my review.

l. 318 can the authors be more specific about the research that is still needed?

Homosexuality is discussed under several topics but in a paper dealing with potential parallels to human sexuality, a separate section on homosexuality might be appropriate.

In summary, the authors need to avoid verbatim quoting from the reviewers, can make the logical flow of the paper better and should perhaps give more attention to homosexuality as a separate form of nonconceptive sex.

Author Response

Please see the attachment.

Author Response File: Author Response.pdf