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A Life History Approach to the Female Sexual Orientation Spectrum: Evolution, Development, Causal Mechanisms, and Health

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A Life History Approach to the Female Sexual Orientation Spectrum: Evolution, Development, Causal Mechanisms, and Health Archives of Sexual Behavior (2019) 48:1273–1308 https://doi.org/10.1007/s10508-018-1261-0 TARGET ARTICLE A Life History Approach to the Female Sexual Orientation Spectrum: Evolution, Development, Causal Mechanisms, and Health Severi Luoto1,2 · Indrikis Krams3,4 · Markus J. Rantala5 Received: 15 October 2017 / Revised: 29 May 2018 / Accepted: 14 June 2018 / Published online: 18 September 2018 © Springer Science+Business Media, LLC, part of Springer Nature 2018 Abstract Women’s capacity for sexual fuidity is at least as interesting a phenomenon from the point of view of evolutionary biology and behavioral endocrinology as exclusively homosexual orientation. Evolutionary hypotheses for female nonheterosexuality have failed to fully account for the existence of these diferent categories of nonheterosexual women, while also overlooking broader data on the causal mechanisms, physiology, ontogeny, and phylogeny of female nonheterosexuality. We review the evolutionary-developmental origins of various phenotypes in the female sexual orientation spectrum using the synergistic approach of Tinbergen’s four questions. We also present femme-specifc and butch-specifc hypotheses at proximate and ultimate levels of analysis. This review article indi- cates that various nonheterosexual female phenotypes emerge from and contribute to hormonally mediated fast life history strategies. Life history theory provides a biobehavioral explanatory framework for nonheterosexual women’s masculinized body morphology, psychological dispositions, and their elevated likelihood of experiencing violence, substance use, obesity, teenage pregnancy, and lower general health. This pattern of life outcomes can create a feedback loop of environmental unpredictability and harshness which destabilizes intrauterine hormonal conditions in mothers, leading to a greater likelihood of fast life history strategies, global health problems, and nonheterosexual preferences in female ofspring. We further explore the potential of female nonheterosexuality to function as an alloparental bufer that enables masculinizing alleles to execute their characteristic fast life history strategies as they appear in the female and the male phenotype. Synthesizing life history theory with the female sexual orientation spectrum enriches existing scientifc knowledge on the evolutionary-developmental mechanisms of human sex diferences. Keywords Female sexual orientation · Homosexuality · Neurodevelopment · Evolutionary-developmental psychology · Behavioral endocrinology · Life history evolution · Women’s health Introduction [E]ven the most fexible models have artifcial assump- tions. […] Therefore, we attempt to treat the same prob- lem with several alternative models each with diferent * Severi Luoto simplifcations but with a common biological assump- [email protected] tion. Then, if these models, despite their diferent assump- 1 English, Drama and Writing Studies, University tions, lead to similar results we have what we can call a of Auckland, Arts 1, Building 206, Room 616, 14A Symonds robust theorem which is relatively free of the details of the St., Auckland 1010, New Zealand model. Hence our truth is the intersection of independent 2 School of Psychology, University of Auckland, Auckland, lies. (Levins, 1966, p. 423) New Zealand There has been a considerable disequilibrium in past evo- 3 Department of Zoology and Animal Ecology, University lutionary research focusing on male rather than female sexual of Latvia, Riga, Latvia orientation. Theoretical discussion on the evolution of female 4 Institute of Ecology and Earth Sciences, University of Tartu, nonheterosexuality has, however, substantially increased in Tartu, Estonia recent years (Apostolou, 2016a, b; Apostolou, Shialos, Khalil, 5 Department of Biology & Turku Brain and Mind Center, & Paschali, 2017; Burri, Spector, & Rahman, 2015; Camperio University of Turku, Turku, Finland Vol.:(0123456789)1 3 1274 Archives of Sexual Behavior (2019) 48:1273–1308 Ciani, Battaglia, Cesare, Camperio Ciani, & Capiluppi, 2018; 2017a, b; Fisher, Ristori, Morelli, & Maggi, 2018; Motta- Kanazawa, 2017; Kuhle & Radtke, 2013). Advances in the Mena & Puts, 2017) and the calibration of life history evolution study of female sexual orientation have been partially deceler- (Adkins-Regan, 2005; Bribiescas, Ellison, & Gray, 2012; Elli- ated by a lack of attempts to integrate research from broader son, 2017; Gettler et al., 2017; Hau & Wingfeld, 2011; Jasien- areas of inquiry. By neglecting research on the causal mecha- ska, Bribiescas, Furberg, Helle, & Núñezde la Mora, 2017; nisms, physiology, ontogeny, and phylogeny of various mani- Minkov & Bond, 2015; Muehlenbein & Flinn, 2011; Roney, festations of female sexual orientation, recent evolutionary 2016). Despite this important mechanistic connection between theorizing has provided an inadequate account of its evolu- LH evolution and sexual orientation—occurring both in humans tionary trajectories (see Fleischman, Fessler, & Cholakians, and in nonhuman animals—prior research has failed to inte- 2015 for an exception), valuable though the hypothesizing and grate LH theory into research on female sexual orientation. subsequent research has been. This has been a crucial omission. Because LH theory makes Complete biological explanations of behaviors or traits need sense of covariation among diferent traits, psychological dis- to address four diferent levels of analysis—phylogeny, ontog- positions, behaviors, and their biological substrates (Immonen, eny, proximate mechanisms, and ultimate function(s) (Bateson Hämäläinen, Schuett, & Tarka, 2018), it makes important & Laland, 2013; Lewis, Al-Shawaf, Conroy-Beam, Asao, & contributions to individual diferences psychology (Csathó & Buss, 2017). These can be reformulated into four questions con- Birkás, 2018; Del Giudice & Belsky, 2011; Ellis, Skorska, & cerning any feature of an organism: How did it evolve over the Bogaert, 2017b; Richardson et al., 2016; Sng, Neuberg, Var- history of a species and what is its relationship to corresponding num, & Kenrick, 2017), to motivational psychology (Kenrick, features in other species (phylogeny)? How does it develop dur- Griskevicius, Neuberg, & Schaller, 2010; Neel, Kenrick, White, ing the lifetime of an individual (ontogeny)? How does it work & Neuberg, 2016), to biomedical science (Maner, Dittmann, (proximate mechanisms)? And what is it for (ultimate func- Meltzer, & McNulty, 2017; Wells, Nesse, Sear, Johnstone, & tion)? Answers to these “Tinbergen’s four questions” are ideally Stearns, 2017), to human development (Kuzawa & Bragg, 2012; synthesized into a common explanatory network elucidating Muehlenbein & Flinn, 2011; Said-Mohamed, Pettifor, & Norris, the origins and ftness benefts of behaviors or traits (Bateson & 2018; Stearns, Allal, & Mace, 2008; Worthman & Trang, 2018), Gluckman, 2011; Bateson & Laland, 2013; Tinbergen, 2005). and as we argue here, to female sexual orientation. Recent evolutionary hypotheses about female nonhetero- A mid-level theory derived from general evolutionary theory, sexuality have focused specifcally on ultimate ftness value LH theory is a powerful tool for describing organismal alloca- without adequately considering the other three questions. tion of bioenergetic resources between somatic efort (the growth The existence of the various phenotypes in the female sexual and survival of an organism) and reproductive efort (produc- orientation spectrum has also mostly been overlooked. By tion and support of ofspring) (Ebneter, Pick, & Tschirren, 2016; addressing and synthesizing not only one, but all four of Tin- Figueredo, Cabeza de Baca, & Woodley, 2013; Stearns, 1992; bergen’s questions, we are better able to review the validity of Worthman & Trang, 2018). LH theory analyzes how the entire recent hypotheses on the evolution of female nonheterosexu- life cycle of an organism is designed by natural selection to opti- ality and suggest novel hypotheses when the existing ones mize reproductive success in the face of environmental challenges are inadequate to explain patterns of experimental fndings. (Stearns et al., 2008; Wells et al., 2017). This design—set within a The present article reviews comparative, developmental, framework of constraints and trade-ofs shaped by past evolution- neurophysiological, psychological, and biobehavioral research ary pressures and current environmental contingencies—works on the various manifestations of female nonheterosexuality in on the materials out of which organisms are built, as well as the humans. Our fnal aim is to explore the evolutionary origins of developmental, physiological, and psychological mechanisms variation in female sexual orientation. These diferent levels of that they have inherited from their ancestors (Figueredo et al., analysis are essential for clarifying what is often a misunder- 2004, 2005, 2006; Flatt & Heyland, 2011; Hämäläinen et al., stood or a mischaracterized relationship between sociocultural 2018; Immonen et al., 2018; Krams et al., 2016, 2017a, b, c; and evolutionary hypotheses (Lewis et al., 2017). Stearns et al., 2008). LH theory has traditionally been applied to differences Life History Theory between species (characterized as r-selected or K-selected ones depending on species-typical LH traits), but the theory One of the primary suggestions given in this review is that has since then been fruitfully utilized in analyzing individu- research on female sexual orientation would beneft from inte- als within species (Ellis,
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