The Social Brain Meets the Reactive Genome: Neuroscience, Epigenetics and the New Social Biology

HYPOTHESIS AND THEORY ARTICLE published: 21 May 2014 HUMAN NEUROSCIENCE doi: 10.3389/fnhum.2014.00309 The social brain meets the reactive genome: neuroscience, epigenetics and the new social biology Maurizio Meloni* School of Sociology and Social Policy, Institute for Science and Society, University of Nottingham, Nottingham, UK Edited by: The rise of molecular epigenetics over the last few years promises to bring the discourse Jan Slaby, Freie Universität Berlin, about the sociality and susceptibility to environmental influences of the brain to an Germany entirely new level. Epigenetics deals with molecular mechanisms such as gene expression, Reviewed by: Hannah Landecker, University of which may embed in the organism “memories” of social experiences and environmental California Los Angeles, USA exposures. These changes in gene expression may be transmitted across generations Karola Stotz, Macquarie University, without changes in the DNA sequence. Epigenetics is the most advanced example of Australia the new postgenomic and context-dependent view of the gene that is making its way into *Correspondence: contemporary biology. In my article I will use the current emergence of epigenetics and its Maurizio Meloni, School of Sociology and Social link with neuroscience research as an example of the new, and in a way unprecedented, Policy, Institute for Science and sociality of contemporary biology. After a review of the most important developments Society, University of Nottingham, of epigenetic research, and some of its links with neuroscience, in the second part Law and Social Science Building, I reflect on the novel challenges that epigenetics presents for the social sciences for a University Park, Nottingham NG7 2RD, UK re-conceptualization of the link between the biological and the social in a postgenomic age. e-mail: Although epigenetics remains a contested, hyped, and often uncritical terrain, I claim that [email protected] especially when conceptualized in broader non-genecentric frameworks, it has a genuine potential to reformulate the ossified biology/society debate. Keywords: epigenetics, Meaney, methylation, neuroepigenetics, postgenomics, plasticity, social neuroscience AFTER GENE-CENTRISM: THE NEW SOCIAL BIOLOGY Paradoxically, it was exactly the completion of the Human Profound conceptual novelties have interested the life-sciences Genome Project that showed that the view of the gene as a discrete in the last three decades. In several disciplines, from neuro- and autonomous agent powerfully leading traits and developmen- science to genetics, we have witnessed a growing (and parallel) tal processes is more of a fantasy than actually being founded on crisis of models that tended to sever biological factors from scientific evidence, as highlighted by the “missing heritability” social/environmental ones. This possibility of disentangling neatly case (Maher, 2008). The image of a distinct, particulate gene what seemed to belong to the “biological” from the “environ- marked by “clearly defined boundaries” and performing just one mental” and to attribute a sort of causal primacy to biological job, i.e., coding for proteins, has been overturned in recent years factors (equated with genetic) in opposition to social or cultural (Griffiths and Stotz, 2013: 68; see also Barnes and Dupré, 2008; ones (thought of as being more superficial, or appearing later Keller, 2011). Although discussions are far from being settled, the in the ontology of development) was part and parcel of very work of the ENCODE consortium for instance has been crucial vocal research-programs in the 1990s. These programs were all in showing the important regulatory functions of what, in a more or less heirs of the gene-centrism of sociobiology: from narrow “gene-centric view”,was supposed to be mere “junk DNA” evolutionary psychology, to a powerful nativism that was very (Encode, 2007, 2012; Pennisi, 2012). Not only does a very small influential in psychology and cognitive neuroscience with its percentage of the genome (less than 2%) act according to the obsessive emphasis on hardwiring culture or morality into the classical definition of the gene as a protein-coding sequence, but brain. most of the non-protein coding DNA in fact plays an important These programs have always received a barrage of criti- regulatory function. The genome is therefore today best described cisms from several intellectual traditions (Griffiths, 2009; Meloni, as a “vast reactive system” (Keller, 2011) embedded in a complex 2013a), particularly those with roots in ethology (Lehrman, 1953, regulatory network with distributed specificity (Griffiths and 1970; Bateson, 1991; Bateson and Martin, 1999), and devel- Stotz, 2013). An important part of this regulatory network is opmental biology (West and King, 1987; Griffiths and Gray, involved in responding to environmental signals, which can cover 1994; Gottlieb, 1997; Oyama, 2000a[1985],b; Oyama et al., 2001; a very broad range of phenomena, from the cellular environment Griffiths, 2002; Moore, 2003). However, never as in this last around the DNA, to the entire organism and, in the case of human decade, we have had scientific evidence that the dichotomous beings, their social and cultural dynamics. view of biology vs. society and biology vs. culture is biologically To sum up a decade of empirical and conceptual novelties fallacious (Meaney, 2001a). the conceptualization of the gene has become dynamic and Frontiers in Human Neuroscience www.frontiersin.org May 2014 | Volume 8 | Article 309 | 1 Meloni The social brain meets the reactive genome “perspectival” (Moss, 2003), in what can be called the new of a series of important conceptual shifts (Jablonka and Lamb, “postgenomic view1”; it addresses genes as part of a broader regu- 2002; Haig, 2012; Griffiths and Stotz, 2013). The notion was lative context, “embedded inside cells and their complex chemical firstly coined by embryologist and developmental biologist C. environments” that are, in turn, embedded in organs, systems and H. Waddington (1905–1975) in the 1940s as a neologism from societies (Lewkowicz, 2010). Genes are now seen as “catalysts” epigenesis to define, in a broader non-molecular sense, the “whole more than “codes” in development (Elman et al., 1996), “fol- complex of developmental processes” that connects genotype and lowers” rather than “leaders” in evolution (West-Eberhard, 2003; phenotype (reprinted in Waddington, 2012). For Waddington Robert, 2004). The more genetic research has gone forward, the epigenetics was “the branch of biology which studies the causal more genomes are seen to “respond in a flexible manner to signals interactions between genes and their products which bring the from a massive regulatory architecture that is, increasingly, the phenotype into being” (Waddington, 1968 see Jablonka and real focus of research in ‘genetics’” (Griffiths and Stotz, 2013: 2; Lamb, 2002). see also Barnes and Dupré, 2008; Dupré, 2012). A parallel origin of the concept is having probably a stronger As Michael Meaney(2001a: 52, 58) wrote more than a decade influence on the present understanding of epigenetics. This latter ago: “There are no genetic factors that can be studied indepen- tradition originates with Nanney’s(1958) paper in Epigenetic dently of the environment, and there are no environmental factors Control Systems, and refers more specifically to the existence of a that function independently of the genome::: . At no point in second non-genetic system, at the cellular level, that regulates gene life is the operation of the genome independent of the context in expression (Nanney, 1958; see, Haig, 2004; Griffiths and Stotz, which it functions.” Moreover, “environmental events occurring 2013). at a later stage of development ::: can alter a developmental It is this second narrower molecular meaning that is becoming trajectory” making meaningless any linear regression studies of increasingly influential in the contemporary literature (Griffiths nature and nurture. Genes are always “genes in context”,“context- and Stotz, 2013). This is why it is probably more correct to dependent catalysts of cellular changes, rather “controllers” of call contemporary epigenetics “molecular epigenetics” to dif- developmental progress and direction” (Nijhout, 1990: 444), ferentiate it from the broader Waddingtonian sense and the susceptible to be reversed in their expression by individual’s developmentalist-embryological tradition in which the term was experiences during development (Champagne and Mashoodh, firstly conceived, although it is true that the two meanings are 2009). not in principle irreconcilable as they both emphasize the context (molecular or at the level of the organism) where genetic func- EPIGENETICS tioning takes place (Hallgrímsson and Hall, 2011). The recent surge of interest in molecular epigenetics is probably In the present mainstream molecular sense, a rather standard the most visible example of these conceptual changes in con- and very often quoted definition of “epigenetics” is “the study of temporary biology. After a delay of almost fifty years from its mitotically and/or meiotically heritable changes in gene function coining, epigenetics has become a “buzzword” in XXI century that cannot be explained by changes in DNA sequence” (my italics, biology (Jablonka and Raz, 2009: 131): the vertical growth of Russo et al., 1996, quoted in Bird, 2007: 396; see also Feng and publications in the field in the last decade certifies this epidemic of Fan, 2009). This definition in

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