1 Behavioral genetics The Cambridge Handbook of Evolutionary Perspectives on Sexual Psychology Severi Luoto, University of Auckland [email protected] Michael A. Woodley of Menie, Center Leo Apostel for Interdisciplinary Studies, Vrije Universiteit Brussel, Brussels, Belgium Cite this chapter as: Luoto, S. & Woodley of Menie, M. A. (in press). Behavioral genetics. In T. Shackelford (Ed.), The Cambridge Handbook of Evolutionary Perspectives on Sexual Psychology. Cambridge University Press. Word count: 12 019 (body text only), 15 352 (abstract, body text, references) Keywords: behavioral genetics, evolutionary psychology, evolution, natural selection, sexual selection 2 Abstract In this introductory chapter, we discuss the nexus between evolutionary theory and behavioral genetics, using it to elucidate the biological origins of human behavior and motivational predispositions. We introduce relevant behavioral genetics methods and evolutionary theoretical background to provide readers with the necessary conceptual tools to deepen their engagement with evolutionary behavioral genetics—as well as to help them take on the challenge of building a scientifically and evolutionarily more consilient account of human behavior. To demonstrate the utility of behavioral genetics in evolutionary behavioral science, our analytical examples range from personality, cognition, and sexual orientation to pair-bonding. We conclude by presenting a few recent landmark studies in behavioral genetics research with a particular focus on two aspects of sexual behavior: assortative mating and same-sex sexual behavior. This chapter considers behavioral genetics methods and their connection with evolutionary science more broadly while providing a succinct overview of recent advances in understanding the evolutionary genetic underpinnings of human sexual behavior, mate choice, and basic motivational processes. It is a sine qua non of scientifically principled evolutionary behavioral scientists to acknowledge the distal evolutionary and proximal genetic processes which, interlinked, underlie the psychobehavioral predispositions that form the variegated fabric of human societies and, more broadly, the diversity of life found in nature. These evolutionary processes operate from distal selection pressures acting on genetic material through hundreds of millions of years of natural selection—and from individual and population differences in genotypes to their manifestations in complex behavioral phenotypes and life outcomes in contemporary humans—which, in turn, enact concomitant selection pressures on the genetic material underlying and arising from them. 3 1. Introduction Evolutionary biology seeks to understand the ways in which various forms of selection make species better able to execute adaptations in order to maximise fitness (gene-copying success) in their varying environments. Evolutionary biology also studies non-adaptive evolutionary processes, which include genetic drift, mutation, and migration. When Charles Darwin proposed the rudiments of what would become the theory of evolution by natural selection, it was not properly integrated with an understanding of genetics or with Mendel’s laws of inheritance, neither of which were known when Darwin published On the Origin of Species by Means of Natural Selection in 1859. This integration occurred in the early 20th century with the “modern synthesis” which arose from the work of Huxley, Dobzhansky, Fisher, Haldane, Wright, and Mayr. Since then, advances in genetics have been integral to empirical and theoretical developments in evolutionary behavioral science. Evolutionary behavioral science and evolutionary psychology have, for instance, increasingly included insights on genetic variation in models for population and individual differences in life history strategies, male and female sexual orientation, and various forms of selection for attractiveness, intelligence, and creativity. Behavioral genetics is one of several fields with the potential to contribute to a sophisticated and mature science of evolutionary psychology. Behavioral genetics focusses on the elucidation of the genetic and environmental co-determinants of an organism’s behavior and, more generally, on such influences on individual differences in behavior. Both sociobiology (the major precursor to modern evolutionary psychology) and behavioral genetics matured as fields in the 1970s, aiming to integrate the study of human behavior with other branches of biology; however, behavioral genetics and (what went on to become) evolutionary psychology have mostly developed in isolation (cf. Segal & Macdonald, 1998; Zietsch, de Candia, & Keller, 2015). This distance between the fields arises from the way in which behavioral genetics focusses on proximate mechanisms—that is, how do genetic and environmental factors influence behavioral differences between individuals, and which specific genetic variants or environmental factors underlie individual differences in behavioral phenotypes. Evolutionary psychology, on the other hand, focusses (with some exceptions) on the ultimate level of explanation: what adaptive advantages, if any, do traits and behaviors provide for an organism, and what can this tell us about the relevant selection histories that shaped these adaptations in humans (Barkow, Cosmides, & Tooby, 1992; Zietsch et al., 2015; Zietsch, Sidari, Murphy, Sherlock, & Lee, 2020). Another point of divergence concerns the nature of the systems that each field specializes in studying. Behavioral genetics focusses on systems that vary between individuals (such as personality and intelligence), whereas the focus of evolutionary psychology has historically been on human universals: species-typical cognitive adaptations, or modules, that arose in response to specific, recurrent selection pressures in the course of human evolutionary history. Evolutionary psychologists have historically rejected 4 the idea that such systems exhibit heritability as modules are species-typical, and should not significantly vary genetically among (normal) individuals. Any variation that might arise in relation to the functioning of these modules is expected to be essentially random and non- heritable, stemming from developmental miscalibration (Tooby & Cosmides, 1990; see Woodley of Menie & Sarraf, 2021 for a detailed discussion of the history of evolutionary psychology). Contemporary evolutionary psychology does, however, acknowledge the heritability of individual differences as well as the many ways in which environmental inputs, particularly during sensitive periods in development, shape human cognition and behavior (Ellis et al., 2020; Figueredo, Vasquez, Brumbach, & Schneider, 2004; Luoto, Krams, & Rantala, 2019a; Syme & Hagen, 2020). Many research paradigms that are adjacent to evolutionary psychology, such as personality and individual differences, developmental and behavioral neuroscience, and behavioral genetics, need to be better integrated with an evolutionary perspective in order to acquire a broader understanding of human cognition and behavior. To that end, there have been several attempts to synthesize the proximate and ultimate levels of analyses of individual differences and their determinants into what can broadly be termed “evolutionary psychology” (Lewis, Conroy-Beam, Asao, & Buss, 2017; Luoto et al., 2019a; Rantala, Luoto, Borráz-León, & Krams, 2021). Woodley of Menie and Sarraf (2021) have termed this “Broad Church” evolutionary psychology, so as to distinguish it from the more narrowly focussed “High Church” or Santa Barbara School evolutionary psychology (this term was coined by Heyes, 2012). This integration between proximate mechanisms and ultimate functions is a major goal to which a scientifically well-rounded and robust evolutionary behavioral science should aspire (Lewis et al., 2017; Tinbergen, 1963; Zietsch et al., 2020). A major effort in this area has been to shift the focus of evolutionary psychology towards better understanding the ultimate functions and proximate mechanisms underlying individual differences. Personality, and more broadly life history variation (Woodley of Menie, Luoto, Peñaherrera-Aguirre, & Sarraf, 2021), for example, might produce enough behavioral polymorphism that it can hedge against fluctuations in the levels of environmental risk and in the availability of environmental micro-niches (Figueredo et al., 2005; Wilson, 1998; Woodley, 2011; Young, Frankenhuis, & Ellis, 2020). Individual differences might also arise from the sensitivity of cognitive and other systems to the (mostly deleterious) impacts of pleiotropic mutations (i.e., genetic variants that influence multiple systems) on their development. Thus, individual differences with respect to certain sources of both trait variation and covariation might arise from the action of various forms of selection on phenotypic condition, with this serving as a hard-to-fake signal of underlying system integrity (see e.g., Houle, 2000; Miller, 2000 on the possible existence of a "general fitness factor" among covarying sources of individual differences). Also significant are individual differences arising from the interaction between evolved psychological mechanisms and the environment (e.g., Del Giudice, 2020; Rantala, Luoto, Krama, & Krams, 2019; Varella, Luoto, Soares, & Valentova, 2021). Such individual differences might arise via a process of differential adaptive calibration in which the execution of biological and psychobehavioral adaptations is fine-tuned