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Not Your Grandma's Genetics : Some Theoretical Notes

Anne Fausto-Sterling Psychology of Women Quarterly published online 26 October 2012 DOI: 10.1177/0361684312462016 The online version of this article can be found at: http://pwq.sagepub.com/content/early/2012/10/26/0361684312462016

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Psychology of Women Quarterly 36(4) 411-418 The Author(s) 2012 Reprints and permission: sagepub.com/journalsPermissions.nav DOI: 10.1177/0361684312462016 http://pwq.sagepub.com

Not Your Grandmas Genetics: Some Theoretical Notes

Anne Fausto-Sterling1

Everybody breathe a sigh of relief: We do not have to fight biology anymore. But, take a deep breath: If we invite biology back into our theoretical lives, we have to do it right; and to do it right, we need to insist that certain theoretical approaches are better than others. Luckily, we have a strong and diverse history of genetic and developmental theory on which we can draw. My goal in this comment is not only to build on the Salk and Hyde (2012) exhortation but also to shape it toward certain kinds of developmental/genetic theory and away from others. I have several priorities: (a) to emphasize best practices in empirically defensible, nonreductive biology, (b) to provide feminist (and other) biologists with ways of understanding organisms and behavior in a social and environmental context, and thus (c) to guide both biological and psychological researchers toward planning more informative empirical studies. Feminist psychologists Rachel Salk and Janet Hyde call on gender researchers to think about genetic contributions to behavior. They acknowledge the bad blood fostered by a version of genetics that rigidly presents how genes might constrict human potential. But, they suggest, new knowledge about gene function, as well as about geneenvironment interaction, has rendered the old genetics moot. They want gender researchers to consider, in teaching and in research, a new view of genes as active collaborators with the environment in the production of behavior. To this end, they provide a kind of primer to contemporary genetics, which has, indeed, changed a great deal since a series of feminist critiques with the rubric Genes and Gender appeared starting in the late 1970s (Hubbard, 1990; Hubbard & Lowe, 1979; Tobach & Rosoff, 1994). Salk and Hyde are on the right track, but there is a peril: The old genetics is not dead and it can still be put to intellectually and politically questionable use (Charney & English, 2012). To keep an underlying current of genetic determinism at bay, we need a better understanding of the parallel histories of nondeterministic and highly deterministic versions of genetics, and we need to further elaborate new approaches to development. Knowledge of individual developmental history becomes essential for understanding behavioral development and potential.

Biometry Versus Development

Two intellectual traditionsthe biometric and the developmentalshare the field of genetics. As they emerged in the first quarter of the 20th century, their cohabitation has been far from peaceful, differentiated as they were, and still are, by their research problems (variation in a population vs. individual development), their approach to causation (causes of variation vs. causal mechanisms), their causal questions (How much? vs. How?), and their methodologies (statistical vs. interventionist; Tabery, 2009). It is safe to say that the founders of these approaches (R. A. Fisher vs. Sewall Wright, Lancelot Hogben, and C. H. Waddington) were also divided by their approaches to the origins of societal conflict and the best ways to achieve social change (Mackenzie, 1981; Tabery, 2008; Werskey, 1978). One of the challenges for psychologistsfeminist or otherwiseis to be clear about their own placement within these knowledge traditions and to look carefully at the point of view of the geneticists with whom they wish to engage. Salk and Hyde are not alone in using the work of Caspi and Moffitt as the poster child for the benefits of studying genes in environmental contextthe good new genetics, not the bad old guys (Caspi & Moffitt, 2006; Caspi et al., 2003). And with good reason. Caspi and Moffitts (2003) article is admirable in several respects. It is a prospective longitudinal study that assessed the mental health status of its participants every 2 years, starting at the age of 3. The authors also assessed life stress events while dividing the study group into two genetic groups: one with a short, and the other with a long, allele form of a serotonin transporter gene. Their report that childhood maltreatment predicted adult depression only in participants with one or two copies of the short allele, but not in those with

Department of Molecular Biology, Cell Biology and Biochemistry, Brown University, Providence, RI, USA Corresponding Author: Anne Fausto-Sterling, Department of Molecular Biology, Cell Biology and Biochemistry, Brown University, Providence, RI 02912, USA Email: anne_fausto-sterling@brown.edu

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a Neuroscience evidence base Neuroscience

b Epidemiological geneenvironment interaction research Geneenvionment interaction

c Experimental neuroscience Neuroscience

Building blocks

Hypothesis

Finding

New studies

1 Disorder links to neural substrate N 2 Environment affects neural substrate N 3 Genotype affects neural substrate N GED

D Genetic variation in neurosystem responses to environments E

Figure 1. Figure 1 is a proposal from Caspi and Moffitt for a research plan in which scientists use knowledge of neuroscience to hunt for candidate genes that might interact with the environment to affect behavior. Note the linear nature of the diagrams and the unidirectional nature of all the arrows. Genotype and environment are represented as the base of a pyramid, the apex of which is a behavioral disorder. There is no developmental information and environment is completely unspecified. From Gene-environment interactions in psychiatry: Joining forces with neuroscience, by A. Caspi & T. E. Moffitt, 2006. Nature Reviews Neuroscience, 7, p. 584. Copyright 2006. Reprinted with permission.

two copies of the long allele, is now often used to show that gene effects can only be claimed in specific social contexts. As important as Caspi and Moffitts (2003) work is however, it does not tell the whole story. Nor do they claim otherwise. Their study is biometric, but their hope is that by identifying known candidate alleles as contributors to variation, they will hone a path that can unite biometrics to developmental mechanism. I share Taberys (2009) and Taylors (2009) skepticism that their approach can succeed without serious attention to developmental aspects of the problem. A central issue for me (as mentioned by Salk & Hyde, 2012) is the failure to specify environment in much detail. I want as well to focus on Caspi and Moffitts overreliance on linear modeling. Compare Figure 1 (Caspi & Moffitt, 2006), which focuses on genetic variation and the brain, to a diagram of the genesis of depression visually conceptualized by Peter Taylor (2009; Figure 2). This latter diagram emphasizes longitudinal life events and suggests the multiple possible routes leading to clinical depression. Furthermore, a more diverse set of environmental contributors to the possibility of major depression are brought into view. Taylors approach is individual and developmental rather than statistical and biometric. Yet, it could certainly be augmented

by more precise knowledge of geneenvironment interactions of the sort discussed in Salk and Hyde.

Dynamic Systems
I have argued elsewhere that adopting a dynamic developmental approach to understanding gender differentiation would help us better understand individual gender variability and move us away from a statistical approach to difference gender and otherwise (Fausto-Sterling, Coll, & Lamarre, 2012a, 2012b). If we are to encourage individuals to develop their full potentials and continue to work toward a more equitable society, then moving beyond an analysis of variance is essential. We can build on several new versions of a much older genetic tradition, one I like to date back to the work of Sewall Wrightthe original developer of path analysisbased on his work from the 1920s forward. In his chapter on gene and character, Wright (1968) explicates the concepts of physiological genetics to explain how genes and environment co-construct specific characters (phenotypes). It was formerly common, he wrote, . . . to attribute the development of characters partly to physiological processes

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Figure 2. This diagram based on the work of Brown and Harris, Bowlby and Taylor, represents a behavioral disorder, depression, as part of a multilayered network of events. The dashed lines indicate that each strand tends to build on what has happened earlier in different strands. The dynamic systems features include a building on prior events, a dispersed notion of causation, and the possibility that stability based on a dynamic equilibrium can be disrupted by a severe life event. From Infrastructure and scaffolding: Interpretation and change of research involving human genetic information, by P. J. Taylor, 2009. Science as Culture, 18, p.446. Copyright 2009. Reprinted with permission.

and partly to heredity, as if heredity could operate by some sort of sympathetic magic, independently of physiological processes . . . (Wright, 1968). Figure 3 reproduces Wrights conceptualization of character development as an historical process jointly produced by genes and environment. The relationships are netlike (p. 59) rather than linear. Nor is it a new discovery (since Wright emphasized it from the beginning) that phenotypic variation is affected by a large number of loci and that, conversely, gene alterations affect many different characters (the principle of universal pleiotropy). Wrights contemporary, C. H. Waddington (1957) echoed these themes while focusing more directly on problems of embryological development. Waddingtons visualization of development as an epigenetic landscape through time has profoundly influenced modern developmental systems theorists, including those who focus on human development (Gottlieb, 1991, 1997; Huang, 2012; Newell, Liu, & MayerKress, 2003; Thelen, 1995 [see Figure 2 on p. 84]; Thelen, 2005; Waddington, 1957 [see figure 4 on p. 29]). Esther Thelen (2005), in particular, built a bridge from the hills and valleys of Waddingtons epigenetic landscapes, to the attractors and repellors of modern dynamic systems theory.

Adding in Gender
During their first year of life, infants gradually learn to differentiate males from females. During their second year, they acquire knowledge of socially expected gender roles, and by Year 3, they apply this knowledge to themselves and others (Fausto-Sterling et al., 2012a, 2012b). In a period that starts before language acquisition and ends (if ever!)

after they learn to speak, children develop gender identities that are profoundly embodied (Fausto-Sterling, 2012). Thelen (2005) argues that second-by-second activities create changes over a longer time span as an infants body responds motorically and emotionally to, and is changed by, sensory and emotional input from its caregiver and others. For example, a toddlers attachment to a particular color (say pink) is not merely a cognitive appreciation of that hue. Rather it is an embodied attraction to, desire for, and pleasure received from pink objects. If one embraces Thelens theoretical approach (also see Lewis, Lamey, & Douglas, 1999), then some critical questions for gender theorists might be: Which second-by-second inputs are salient for gender development? How do they translate from short time spans into changes over a longer period of time? What are the neural and physiological mechanisms which ground gender embodiment? And, within this context, what gene activities are critical for the operation of these mechanisms? This approach profoundly shifts what questions we ask about genes and how we ask them. It is a fair distance from Caspi and Moffitt (2003) to Thelen. Let us dig a little deeper in genes, gender, and developmentstarting with the work of David Crews, a biologist well known for his study of sexual development in organisms ranging from snakes and turtles to mammals (Crews, Lou, Fleming, & Ogawa, 2006; Crews, Rushworth, Gonzalez-Lima, & Ogawa, 2009). Crews and colleagues have developed methods for studying the relationships among gene networks, metabolic changes in social behavior networks in the brain, and environment, and Crews echoes dynamic systems themes: Complex behaviors and their underlying bases are cumulative processes

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Figure 3. Wrights drawing of the relationship between genes and environment gives environment a central role in development, even in the embryo. The jackknifed dotted lines represent individual gene activities, while the solid lines show developmental time and direction. Note that past events shape future processes. From Evolution and the genetics of populations: Genetics and biometric foundations (Vol. 1, p. 59) by S. Wright, 1968, Chicago, IL: University of Chicago Press. Copyright 1968. Reprinted with permission.

to be understood in terms of prior individual history, and current states provide the basis on which future development builds. With regard to genes, in particular, prior experience shapes how genes respond to subsequence experiences, whereas later experiences may modify earlier effects (Crews et al., 2006). In the past decade, Crews has built on the idea that most social behaviors are supported by an interconnected network of interconnected brain nuclei (Crews et al., 2009). Crews developed a new form of landscape graphics which allows him to represent the shifting alliances of metabolic activity in a network of brain nuclei that mediate social behavior. The example shown in Figure 4 demonstrates how the sex ratio in a litter of mice affects brain metabolism in specific regions of the limbic system (a brain region that supports emotion, behavior, motivation, and more) and how those changes correlate with changes in anxiety-like and social behaviors. Crews also shows (in data not reported here) that both the genotype of litter mates and the adult experience have profound brain metabolic and

behavioral effects. Although the types of controlled experiments used in mice cannot be done in humans, it is possible to develop analogous approaches. Instead of using an enzyme level to measure brain activity, it ought to be possible to use functional magnetic resonance imaging or some other scanning technique (Kuhl, 2010; Kuhl & Rivera-Gaxiola, 2008; Neville et al., 1998; Swain, Lorberbaum, Kose, & Strathearn, 2007). In terms of the early part of my essay, my most important point is that while Crews studies how genes and environment relate to the brain and behavior, his approach uses dynamic systems and development rather that biometrics and the analysis of variance. As he writes, Genetics proposes, epigenetics disposes (Crews et al., 2006, p. 120).

On Becoming Boys and Girls

Let me close by considering how we might use dynamic systems to think about gender in human development. Salk

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415 and Hyde (2012) refer to gender researchers, but they do not elaborate on the types of gender research for which genetics might be appropriate. By implication, it seems they refer primarily to work on gender disparities in mental and physical health. Indeed, Hyde (2005) argues elsewhere that fundamental differences in cognition and personality types are either small in magnitude, spurious, or heavily context dependent. Although I generally agree with Hydes Gender Similarities Hypothesis, there are some fundamental aspects of gender and early development that are understudied, are wildly undertheorized, and could well relate to adult emergence of health-related gender differences. Furthermore, several early sex-related differences are often deployed in specious arguments concerning social inequalities such as employment channeling and pay differentials. Therefore, we still need theories of gender in early development that have sufficient intellectual force to displace the nature/genetics/ nurture/environment paradigm that continues to shape most discussions of difference. In the final pages of my essay, therefore, I offer some broad brush strokes for how a dynamic systems approach might be used to shape the study of gender identity formation and some of its behavioral consequences. The formation of gender identity (knowledge of self as male or female) and gender expression (embodied range of masculine and feminine expression) probably begins at or before birth but slowly emerges starting around an infants first birthday. Thereafter, components of self-identity strengthen, becoming more detailed and specific (FaustoSterling, 2012). I hypothesize that individual variability in identity and embodied expression starts with infantcaregiver interactions. Individual differences in physiology at birth (temperament, activity levels, irritability, sleep cycles, etc.) are part of a developmental network that includes caregiver responses (Fogel et al., 1997; Lavelli & Fogel, 2002, 2005). The latter depend on parental experience, personality, and current life circumstances. I have represented this basic idea in the landscape diagram shown in Figure 5, which represents infant variants as balls rolling down a corrugated landscape (parenting variability). We do not know what the most salient aspects of neonatal physiological variability might be, but we could start by looking at some known average sex differences at birth. For example, in a large data set shared with me by my colleague Stephen Buka (Gilman, Gardener, & Buka, 2008), we found small but significant differences in head circumference, birth weight, and 20-min Apgar scores (Table 1). Often such variables are used individually to correlate with some later-developing trait (Vasiliadis, Buka, Martin, & Gilman, 2010; Wen et al., 2010). But how do the traits in Table 1 correlate with one another? Because newborns are systems of traits, how might a child with a low birth weight but larger head circumference and higher Apgar score compare behaviorally to another with a high birth weight but smaller head circumference and lower Apgar score? Are there

Figure 4. The top two graphs show the metabolic activity of different regions of the brain in mice raised in all female (F), wild type (W) litters (FW/FW) versus half male and half female litters (FW/MW). Each peak refers to metabolic activity in one of the following brain regions: Brain nuclei abbreviations: CMPO, central medial preoptic area; RMPO, rostral medial preoptic area; CoAMY, corticomedial amygdala; CeAMY, central amygdala; BNST, bed nucleus of the stria terminalis; BNSTma, main bed nucleus of the stria terminalis; PVN, paraventricular nucleus. Asterisks indicate significant differences in specific nuclei. The bottom graph isolates the differential effects of having male littermates to make the sibling effect more visible. From From gene networks underlying sex determination and gonadal differentiation to the development of neural networks regulating sociosexual behavior, by D. Crews, W. Lou, A. Fleming, and S. Ogawa, 2006. Brain Research, 1126, p. 119. Copyright 2006. Reprinted with permission.

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Figure 5. An epigenetic landscape showing the production of possible gender variants (GV-1, GV-2, etc.). The ball (infant at birth) might be in the center of the gentle valley or slightly on one of the sloping sides. Location might skew where it starts to roll. At the same time, the valleys and hills (which represent environmental inputs and constraints) become more pronounced. The arrow extending from GV-2 suggests the possibility that the ball could move out of its valley and into another one, but it has to roll uphill which requires some sort of unusual input or set of events. Table 1. Average Sex Differences at Birth Trait Head circumference (cm) Weight (kg) 20-min Apgar Male, M (SD) 33.93 (1.70) 3.16 (0.67) 7.93 (2.60) Female, M (SD) 33.34 (1.60) 3.05 (0.62) 8.21 (2.45)

differing sex-related patterns when several physiological traits are looked at together? We have begun a project to visualize some of these early traits with slight sex-related differences as three dimensional meshes (see Figure 6). Using data from 526 infants (half boys and half girls), we have created mesh plots derived from the location of each infant in a space that represents their head circumference, birth weight, and Apgar score at 5 min and 20 min after birth. Representing data in this fashion opens up some doors. We can see at a glance that 5 min after birth there is a group of girls (but no boys) occupying a space with low-to-medium Apgar scores and medium-to-high birth weight and head size, as well as a group of girls high on all three parameters. By the time the 20-min Apgar score has been taken, enough of the boys Apgars have improved that the only obvious area of nonoverlap is for the 3-D space of high Apgar, high birth weight, and large head circumference. Furthermore, the overall dimensions of both male and female meshes have contracted, indicating a stabilization and a lowering of variability. To what, if anything, might these differences at birth relate? Do infants whose starting characteristics fall in different parts of the mesh differ in terms of traits such as irritability and alertness? How might such differences affect

Figure 6. A. Neonatal distributions of males and females birth weight, head circumference and 5 minute Apgar score. B. Neonatal distributions of males and females birth weight, head circumference and 20 minute Apgar score. C. Distribution of the total number of times during biweekly 5-minute observations made from ages 4 months to 12 months that mothers of sons or mothers of daughters vocalized, touched affectionately and assisted infant movement in the same time frame.

parental caresay by disrupting sleep or making parent infant-parent bonding more or less difficult? How might parental personality, past experience, and life experience become part of a network of emotional and sensory input that shapes early development? Are bodily manifestations of infant sex (as opposed to parental behaviors related to knowledge of the sex of their infant) the most salient measure, or is neonatal physiology, morphology, and developmental maturityin combination with the parenting

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417 to understand child behavior are ways of looking at how they appear. Again I turn to a dynamic systems framework. I think of a strong preference, such as toy or color preference, as a valley or attractor basin in a developmental landscape. I suggest that toy preference, gender knowledge (of self and in the world), and skills develop in the same time frame. In Figure 7, I represent 4 times (from younger to older) as lines that are actually cross-sections of a 3-D landscape such as the one shown in Figure 4. The top line represents birth to 10 months, during which there are no demonstrable sex differences in toy preference, whereas the bottom line, which represents 3-year-olds, shows that toy preference and gender have merged to form a single, deep attractor basin. How has this come about? I hypothesize that, on the one hand, boys and girls are exposed more often to one type of toy than another and that, rather than contempt, familiarity breeds pleasure and preference. Simultaneously, on the other hand, infants learn to recognize sex and gender in the world and gradually learn to apply this knowledge to themselves. At some point, familiarity links with self-knowledge, and gender-related toy preference becomes a trait that is stable for 3-year-olds. (Note that stable traits are not necessarily permanent traits. So I am not making a general argument about permanent differences in toy preference, only one about how it might develop in 3-year-olds). Of course, the actual networks of behaviors and preferences are more varied and intricate than this depiction, but it captures the theoretical structure that I want to emphasize in this essay.

Figure 7. T-1 to T-4 represent 4 times (from younger to older). The lines are cross-sections of a 3-D landscape such as the one shown in Figure 5. At T-3 separate toy preference and gender attractors have formed and by T-4 they have merged into a single fairly strong gender/toy preference attractor. T-1 and T-2 are times before 10 months of age. T-4 represents 3 years of age. T-3 is a transition time period.

style and abilities of the primary caregiverthe critical set of features contributing to the development of masculine and feminine identities and self-expression as infants become toddlers and then older children? Finally, Figure 6C shows the possibilities of examining several behaviors at once. In this case we have graphed the confluence of 2 maternal behaviors, vocalization, and affectionate touch in the mothers of boys or girls and one infant behavior, assisted locomotion, over a several month period. What is striking in this graph is a wing of instances in which there are large numbers of all three behaviors directed at sons but not daughters. Might such differences relate to differences in gross motor activity that emerge as infants start to crawl and walk? I have elaborated a bit more of this developmental theory elsewhere (Fausto-Sterling, 2012), but I would like to close by considering how dynamic developmental systems might help us reconceptualize the emergence of one wellestablished sex difference in toddlersthat of toy preference. Sex differences in toy preference emerge gradually during the second and third years of life. Many researchers reach back into the womb to cite prenatal hormone differences as an explanatory factor, but the type of argument used to support such claims is fraught with methodological difficulties (FaustoSterling et al., 2012a; Jordan-Young, 2010, 2012). The biggest among these connects back to Taberys (2009) distinction between the goals of biometricians and developmentalists: The studies correlating hormones and play behavior can at best offer information on how much. Instead, I argue that what we need

Conclusion
My reflection is an extended plea to devise new paradigms for understanding gender differences as dynamic systems that develop over time, stabilize, destabilize, and reform. Specific genes that relate to neural physiology and that may be differently activated or suppressed in different environments (from hormonal to social) obviously contribute to behavioral systems. But it is critical to move beyond a biometric approach for identifying such genes to a study of their role in developmental systems. Genes are a strand in the net, not the base of a pyramid. For me, the goal is to understand how differences and similarities develop, what systems maintain them, and how they do or do not change. References
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