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Gene-Culture Coinheritance of a Behavioral Trait vol. 192, no. 3 the american naturalist september 2018 Gene-Culture Coinheritance of a Behavioral Trait Elliot G. Aguilar* and Erol Akçay University of Pennsylvania, Philadelphia, Pennsylvania 19104 Submitted October 5, 2017; Accepted April 5, 2018; Electronically published July 16, 2018 Online enhancements: appendix. abstract: Many physical and behavioral traits in animals, including havior (Pérusse et al. 1994), handedness (Laland 2008), fer- humans, are inherited both genetically and culturally. The presence of tility (Kosova et al. 2010; Alvergne et al. 2011; Colleran and different inheritance systems affecting the same trait can result in com- Mace2015;Colleran2016),andAlzheimer’sdiseasebiomark- plex evolutionary dynamics. Here, we present a general model that elu- ers (Levy et al. 2016) in humans as well as song form in pas- cidates the distinct roles of cultural and genetic inheritance systems and serine birds (Freeberg 2000; Feher et al. 2009), mate choice their interaction in driving the evolution of complex phenotypes. In par- in Trinidadian guppies (Dugatkin 1992), and foraging be- ticular, we derive a Price equation that incorporates both cultural and havior in bottlenose dolphins (Krŭtzen et al. 2005). In each genetic inheritance of a phenotype where the effects of genes and cul- fi ture are additive. We then use this equation to investigate whether a of these cases, an important tness-related trait or behavior genetically maladaptive phenotype can evolve under dual transmission. is determined by not only genetic inheritance but also cul- We examine the special case of altruism using an illustrative model and tural transmission from individuals that may not have con- show that cultural selection can overcome genetic selection when the tributedanygeneticmaterial.Giventheimportanceofgenetic variance in culture is sufficiently high with respect to genes. We also and nongenetic inheritance in determining so many behav- show that the presence of cultural transmission can modify genetic se- ioral traits, it is imperative to develop a better theoretical un- lection itself, making genetic selection more favorable to a trait than derstanding of how such coinheritance affects the evolution under purely genetic inheritance. Last, we consider the effect of differ- ent timescales of genetic and cultural transmission. We discuss the im- of behavioral traits. plications of our results for understanding the evolution of important In recent years, evolutionary theorists have begun to in- coinherited behaviors, including how our framework can be used to vestigate the consequences of multiple inheritance systems generate quantitative estimates of selection pressures required for a ge- (Otto et al. 1995; Bonduriansky and Day 2009; Day and Bon- netically maladaptive trait to evolve. duriansky 2011). In a pair of articles, Day and Bondurianski Keywords: gene-culture coevolution, altruism, multiple inheritance, used the Price equation to construct a general framework for Price equation. modeling genetic and nongenetic traits that jointly deter- mined phenotype. However, their approach was limited to vertical transmission of the nongenetic trait and thus kept Introduction track of only the reproductive fitness consequences of both systems of inheritance. While this approach gives a mathe- Behavioral traits are among the most complex phenotypes matically valid description of evolutionary change in a trait, under study in evolutionary biology. At the heart of that com- it obscures the separate roles of genetic and nongenetic in- plexity is the interaction between genetic inheritance and the heritance and selection in causing that change. In another environment (Turkheimer 2000). In organisms with social recent article, El Mouden et al. (2014) developed a Price equa- learning, a significant component of the environment can tion for cultural evolution and addressed the question of how be conspecific individuals who serve as models for socially potential conflicts between cultural and genetic selection might learned behaviors, leading to cultural transmission. Differ- be resolved. However, their work considered cultural and ge- ential cultural transmission of behaviors or traits can lead netic transmission of (and selection on) a trait as mutually ex- to an evolutionary process that operates in tandem with ge- clusive alternatives and did not attempt to model the cotrans- netic evolution. Examples of behaviors that are influenced by mission of a single trait through both culture and genetics both genetic and cultural transmission span a wide range, (for more on this point, see “Discussion”). such as antisocial behavior (Maes et al. 2007), parental be- To account for the distinct causal roles of cultural and ge- netic selection, one needs to consider fitness measures in both * Corresponding author; email: [email protected]. ORCIDs: Akçay, http://orcid.org/0000-0001-8149-7124. systems of inheritance simultaneously. This is ultimately be- – q cause ancestors in one system may not be identical to the Am. Nat. 2018. Vol. 192, pp. 000 000. 2018 by The University of Chicago. fi 0003-0147/2018/19203-57995$15.00. All rights reserved. ancestors in another. A tness measure implies a mapping DOI: 10.1086/698872 from ancestral to descendant individuals: ancestors who map This content downloaded from 165.123.034.086 on August 14, 2018 21:07:50 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). 000 The American Naturalist (i.e., contribute hereditary material) to more descendants ple forms of inheritance are present. This point was high- have higher fitness. Multiple inheritance systems mean the lighted nearly 40 years ago by Richerson and Boyd (1978), possibilityofmultiplemappings.Forexample,imagineapop- who remarked that when both genes and culture determine ulation of asexual organisms (as in fig. 1) with a phenotype a single phenotype, the value of the phenotype that maximizes fi p determined by genetic and cultural inheritance. Let pa be genetic tness may differ from the value that maximizes cul- fi fl the phenotype of an ancestor and pd the phenotype of her ge- tural tness, leading to con icts between the two inheritance netic descendant. If both genes and culture are inherited from systems. Modeling phenotype as the outcome of a nonzero the same ancestor and we assume no flaws in transmission sum game between cultural and genetic inheritance, they p and identical environmental effects, then pa pd. However, showed the conditions under which the Nash equilibrium if one’s genetic parent and cultural role model are not the phenotype would be the cultural fitness optimum and not ( fi same individual, then it is possible that pa pd.Ifwecon- the optimum value for genetic tness. In the ensuing de- sider the mapping solely from genetic parents to offspring, cades, cultural evolution theory has largely focused on the this discrepancy will appear simply to be an unexplained de- case when the genetic trait encodes a learning rule that de- viation between parents and offspring. However, also keep- termines how a cultural trait is acquired (Cavalli-Sforza and ing track of the mapping between cultural role models and Feldman 1981; Boyd and Richerson 1988; Boyd et al. 2003; pupils, we might find that certain individuals map to more Guzmán et al. 2007; Lehmann et al. 2008). By contrast, the cultural descendants as a result of their phenotype because problem of conflict between inheritance systems that affect of selection in the cultural domain. Thus, what appears un- the same trait has received surprisingly little attention, with der one mapping to be an unexplained deviation between the notable exception of the model of Findlay (1992), which parent and offspring is revealed under another mapping to treated only vertical cultural transmission. This dearth of at- be a force of selection in its own right. tention is particularly surprising, given the anthropological The argument above underscores the importance of con- evidence for behavioral and social practices in humans that sidering fitness in each domain of inheritance when multi- reduce reproductive fitness (Glanville 1987; Logan and Qirko a A1 A2 A3 D1 D2 D3 b gcPhenotypes Reproductive fitness Cultural fitness 10 = 1 = 1 = 0 A1 pa1 w1 s1 10 = 1 = 2 = 0 A2 pa2 w2 s2 11 = 2 = 0 = 3 A3 pa3 w3 s3 11 = 2 D1 pd1 11 = 2 D2 pd2 11 = 2 D3 pd3 Figure 1: a, Diagram shows the hereditary relationships between ancestors (A1, A2, A3) and descendants (D1, D2, D3). Solid lines indicate reproductive relationships, while dashed lines show cultural learning. While A3 sired no offspring, he is the cultural learning model for all descendants. b, Genotype, culture type, phenotypic, and fitness values for each ancestor and descendant (excepting fitness values). Each p descendant has only one genetic and cultural ancestor; thus, each solid edge corresponds to vij 1, and each dashed edge corresponds to p gij 1. This content downloaded from 165.123.034.086 on August 14, 2018 21:07:50 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). Gene-Culture Coinheritance of a Trait 000 1996). Examples include clubbing pregnant women to in- ness, conscientiousness; Goldberg 1993), or a morphological duce birth in Colombia (Reichel-Dolmatoff and Reichel- one such as body size. We assume that the effects of genetic Dolmatoff 2013), unhygienic neonatal care practices in Ban- and cultural inheritance are additive; that is, we express an gladesh
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