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Male Homosexuality and Maternal Immune Responsivity to the Y-Linked Protein NLGN4Y

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Male Homosexuality and Maternal Immune Responsivity to the Y-Linked Protein NLGN4Y Male homosexuality and maternal immune responsivity to the Y-linked protein NLGN4Y Anthony F. Bogaerta,b,1, Malvina N. Skorskab,c, Chao Wangd, José Gabriea, Adam J. MacNeila, Mark R. Hoffarthb, Doug P. VanderLaanc,e, Kenneth J. Zuckerf, and Ray Blanchardf aDepartment of Health Sciences, Brock University, St. Catharines, ON L2S 3A1, Canada; bDepartment of Psychology, Brock University, St. Catharines, ON L2S 3A1, Canada; cDepartment of Psychology, University of Toronto Mississauga, Mississauga, ON L5L 1C6, Canada; dBrigham & Women’s Hospital, Harvard Medical School, Boston, MA 02115; eChild, Youth and Family Division, Underserved Populations Research Program, Centre for Addiction and Mental Health, Toronto, ON M6J 1H4, Canada; and fDepartment of Psychiatry, University of Toronto, Toronto, ON M5T 1R8, Canada Edited by S. Marc Breedlove, Michigan State University, East Lansing, MI, and accepted by Editorial Board Member Thomas D. Albright October 23, 2017 (received for review April 8, 2017) We conducted a direct test of an immunological explanation of the resulting in death of the affected cells or inducing miscarriage). finding that gay men have a greater number of older brothers Both PCDH11Y and NLGN4Y are part of families of cell ad- than do heterosexual men. This explanation posits that some hesion molecules thought to play an essential role in specific mothers develop antibodies against a Y-linked protein important cell–cell interactions in brain development (23). in male brain development, and that this effect becomes increas- In our study, blood samples and reproductive histories were ingly likely with each male gestation, altering brain structures un- collected from 54 mothers of gay sons (23 of whom had pre- derlying sexual orientation in their later-born sons. Immune assays viously given birth to a heterosexual son) and a control sample of targeting two Y-linked proteins important in brain development— 72 mothers of heterosexual sons, along with additional controls protocadherin 11 Y-linked (PCDH11Y) and neuroligin 4 Y-linked (16 women with no sons and 12 men). We developed in-house — (NLGN4Y; isoforms 1 and 2) were developed. Plasma from moth- ELISAs and used the plasma from participants to examine evi- ers of sons, about half of whom had a gay son, along with addi- dence of the existence of maternal antibodies to these proteins. tional controls (women with no sons, men) was analyzed for male protein-specific antibodies. Results indicated women had signifi- Results cantly higher anti-NLGN4Y levels than men. In addition, after sta- We examined antibody concentrations to each of these Y-linked tistically controlling for number of pregnancies, mothers of gay proteins (anti-PCDH11Y, anti-NLGN4Y isoform 1, anti-NLGN4Y sons, particularly those with older brothers, had significantly isoform 2) separately, but also used a z-scored combination of anti- higher anti-NLGN4Y levels than did the control samples of women, NLGN4Y isoforms 1 and 2 (combined anti-NLGN4Y). Such a including mothers of heterosexual sons. The results suggest an associ- composite could provide a more reliable estimate of response to ation between a maternal immune response to NLGN4Y and subse- common epitopes than either assay alone and thus might be a better quent sexual orientation in male offspring. index of humoral response to NLGN4Y. Due to the skewed nature of theassaydata(Fig. S1), our main analyses employed nonparametric sexual orientation | homosexuality | fraternal birth order | NLGN4Y | maternal immune hypothesis statistics, which use rank-orders of data (26). First, in a preliminary test, we expected women’simmunere- activity to exceed men’s on the assumption that, upon exposure, fraternal birth order (FBO) effect exists in the sexual ori- entation of men, but not of women, with older brothers (and A Significance no other sibling characteristic) increasing the odds of male ho- mosexuality (1–3). Although sexual orientation is likely determined by multiple (potentially independent) factors and FBO is associated Gay men have, on average, a greater number of older brothers with only a proportion of men’s sexual orientation (4–6), the effect than do heterosexual men, a well-known finding within sexual has been confirmed many times, including by independent inves- science. This finding has been termed the fraternal birth order tigators and in non-Western samples (2, 3, 7–10). FBO is in- effect. Strong scientific interest in sexual orientation exists dependent of potential confounds, such as maternal age (1, 11), and because it is a fundamental human characteristic, and because likely operates during prenatal life and not childhood (11). Evi- its origins are often the focal point of considerable social con- dence in favor of a maternal immune hypothesis underlying FBO troversy. Our study is a major advance in understanding the includes the finding that fetal material enters maternal circulation origins of sexual orientation in men by providing support for a at parturition (12), as exemplified by male microchimerism occur- theorized but previously unexamined biological mechanism—a ring in mothers of sons (13, 14) and by hemolytic disease of the maternal immune response to a protein important in male fetal newborn (15). There is also evidence that maternal immune brain development—and by beginning to explain one of the products, including antibodies, can enter the fetal compartment and most reliable correlates of male homosexuality: older brothers. pass the blood/brain barrier of the developing fetal brain (16–20). Finally, an incremental maternal immune response occurs to a Author contributions: A.F.B., M.N.S., C.W., and R.B. designed research; A.F.B., M.N.S., C.W., J.G., M.R.H., D.P.V., and K.J.Z. performed research; C.W., J.G., and A.J.M. contrib- Y-linked protein (SMCY/H-Y) in relation to prior male fetuses uted new reagents/analytic tools; A.F.B., M.N.S., M.R.H., and R.B. analyzed data; and (21), a phenomenon that, at times, may underlie widespread A.F.B., M.N.S., A.J.M., and R.B. wrote the paper. alteration of fetal development and induce miscarriage (22). The authors declare no conflict of interest. — Unlike SMCY, two Y-linked proteins protocadherin 11 Y- This article is a PNAS Direct Submission. S.M.B. is a guest editor invited by the Editorial linked (PCDH11Y) and neuroligin 4 Y-linked (NLGN4Y)— Board. have special relevance as candidates to underlie FBO and sexual This open access article is distributed under Creative Commons Attribution-NonCommercial- orientation (2, 3) because they are represented in the fetal brain NoDerivatives License 4.0 (CC BY-NC-ND). and feature primarily extracellular structures (23–25), which al- See Commentary on page 234. lows these proteins to be accessible to circulating antibodies. 1To whom correspondence should be addressed. Email: [email protected]. Thus, antibodies could bind to these proteins and alter their role This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. in typical sexual differentiation of the brain (without necessarily 1073/pnas.1705895114/-/DCSupplemental. 302–306 | PNAS | January 9, 2018 | vol. 115 | no. 2 www.pnas.org/cgi/doi/10.1073/pnas.1705895114 Downloaded by guest on September 27, 2021 these male-specific substances should be perceived by the women’s **** immune system as foreign to them. Using two-tailed Mann–Whitney *** SEE COMMENTARY U n = tests ( 154), this sex difference was supported for all three anti- ** NLGN4Y measures (isoform 1: P = 0.007; isoform 2: P = 0.007; 100 mrofosiY4NGLN * combined NLGN4Y: P = 0.003), but not for PCDH11Y (P = 0.855) (Fig. 1 and Table S1), a result that may partly reflect low antibody ycnangerprofgnillortnoc responses across all participants for PCDH11Y relative to NLGN4Y 80 (Fig. S1). Given that the expected sex difference was confirmed for NLGN4Y, we then examined anti-NLGN4Y levels among 60 women (n = 142) using an omnibus, two-tailed, Jonckheere– Terpstra test for ordered alternatives. In line with the maternal itnafoknarnae immune hypothesis, the predicted ordering for antibody con- 40 centrations to anti-NLGN4Y was as follows: women with no sons < mothers of heterosexual sons < mothers of gay sons with no older brothers < mothers of gay sons with older brothers. 20 Mothers of gay sons with older brothers were predicted to have the highest concentration of antibodies, but we also predicted mothers of gay sons with no older brothers to have higher con- M- 1 0 centrations than mothers of heterosexual sons and women with Women with Mothers of Mothers of Mothers of no sons, on the assumption that the former could be immunized no sons heterosexual gay sons gay sons on a first male pregnancy or, for example, include a subset of sons with no older with older mothers immunized by miscarried and possibly undetected male Group brothers brothers fetuses. In this analysis, we also controlled for total number of pregnancies (live births and miscarriages) because this re- Fig. 2. Mean rank of antibody concentrations (from lowest, 1, to highest, productive variable differed among the groups and was related to 142) for NLGN4Y isoform 1 by group controlling for pregnancy (n = 142). – = = anti-NLGN4Y levels (Materials and Methods and Tables S4 Omnibus standardized test statistic from the Jonckheere Terpstra test 3.90, P 0.000096, two-tailed, r = 0.33. Pairwise comparisons: ****P = 0.00035, r = 0.35; and S5). The expected ordering of groups was confirmed for anti- COGNITIVE SCIENCES = = = = = = PSYCHOLOGICAL AND P = ***P 0.008, r 0.39; **P 0.021, r 0.30; *P 0.024, r 0.19. All Ps for pair- NLGN4Y isoform 1 ( 0.000096) (Fig. 2), anti-NLGN4Y iso- wise comparisons are one-tailed. Error bars represent SEM. form 2 (P = 0.030), and combined anti-NLGN4Y (P = 0.0012). The largest of these effects, using statistical effect size estimates appropriate to the nonparametric statistics we employ here, would mothers of heterosexual sons, had higher antibody levels on all be designated as medium (e.g., rsapproximately= 0.30) (Fig.
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