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A Mathematical Model of the Evolution of Individual Differences in Developmental Plasticity Arising Through Parental Bet-Hedging

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A Mathematical Model of the Evolution of Individual Differences in Developmental Plasticity Arising Through Parental Bet-Hedging UC Davis UC Davis Previously Published Works Title A mathematical model of the evolution of individual differences in developmental plasticity arising through parental bet-hedging. Permalink https://escholarship.org/uc/item/4bh108gv Journal Developmental science, 19(2) ISSN 1363-755X Authors Frankenhuis, Willem E Panchanathan, Karthik Belsky, Jay Publication Date 2016-03-01 DOI 10.1111/desc.12309 Peer reviewed eScholarship.org Powered by the California Digital Library University of California Developmental Science 19:2 (2016), pp 251–274 DOI: 10.1111/desc.12309 PAPER A mathematical model of the evolution of individual differences in developmental plasticity arising through parental bet-hedging Willem E. Frankenhuis,1 Karthik Panchanathan2 and Jay Belsky3 1. Behavioural Science Institute, Radboud University Nijmegen, The Netherlands 2. Department of Anthropology, University of Missouri, USA 3. Human Ecology, University of California, Davis, USA Abstract Children vary in the extent to which their development is shaped by particular experiences (e.g. maltreatment, social support). This variation raises a question: Is there no single level of plasticity that maximizes biological fitness? One influential hypothesis states that when different levels of plasticity are optimal in different environmental states and the environment fluctuates unpredictably, natural selection may favor parents producing offspring with varyinglevels of plasticity. The current article presents a mathematical model assessing the logic of this hypothesis – specifically, it examines what conditions are required for natural selection to favor parents to bet-hedge by varying their offspring’s plasticity. Consistent with existing theory from biology, results show that between- individual variation in plasticity cannot evolve when the environment only varies across space. If, however, the environment varies across time, selection can favor differential plasticity, provided fitness effects are large (i.e. variation in individuals’ plasticity is correlated with substantial variation in fitness). Our model also generates a novel restriction: Differential plasticity only evolves when the cost of being mismatched to the environment exceeds the benefits of being well matched. Based on mechanistic considerations, we argue that bet-hedging by varying offspring plasticity, if it were to evolve, would be more likely instantiated via epigenetic mechanisms (e.g. pre- or postnatal developmental programming) than genetic ones (e.g. mating with genetically diverse partners). Our model suggests novel avenues for testing the bet-hedging hypothesis of differential plasticity, including empirical predictions and relevant measures. We also discuss several ways in which future work might extend our model. Research highlights Introduction • We formalize Jay Belsky’s bet-hedging hypothesis of Developmental plasticity – the ability to adjust develop- differential plasticity. ment based on experience – is ubiquitous in nature • Results support the hypothesis’ logical coherence, but (Schlichting & Pigliucci, 1998), and evolves because it only under restrictive conditions. allows organisms to adaptively tailor their phenotypes to • Our model suggests novel avenues for empirically a range of environmental states (Dall, Giraldeau, Ollson, testing the bet-hedging hypothesis. McNamara & Stephens, 2005; West-Eberhard, 2003). • We suggest multiple theoretical extensions of our Empirical studies of humans show that the degree of model. plasticity itself may vary across individuals (‘differential plasticity’); that is, some individuals are shaped more ... it is advisable to divide goods which are exposed to than others by the same kinds of experiences (Belsky, some danger into several portions rather than to risk them 1997, 2005; Belsky & Pluess, 2009a, 2009b; Boyce & Ellis, all together. (Daniel Bernoulli, 1738 (trans. 1954), p. 30) 2005; Ellis, Boyce, Belsky, Bakermans-Kranenburg & van IJzendoorn, 2011; for studies of non-human ani- Put all your eggs in one basket and then watch that basket. mals, see Dingemanse & Wolf, 2013). In some cases, (Mark Twain, 1894, Pudd’nhead Wilson and Other Tales) highly plastic individuals are also more susceptible to Address for correspondence: Willem E. Frankenhuis, Behavioural Science Institute; Radboud University Nijmegen; Montessorilaan 3, PO Box 9104; 6500 HE, Nijmegen, The Netherlands; e-mail: [email protected] © 2015 John Wiley & Sons Ltd 252 Willem E. Frankenhuis et al. experience: that is, they are more adversely affected by offspring: one genetic by producing genetically diverse harmful environments as well as benefit more from offspring, the other experiential through pre- and post- supportive circumstances (‘differential susceptibility’; natal regulation of offspring plasticity. Belsky’s experi- Belsky, Jonassaint, Pluess, Stanton, Brummett et al., ential version of the bet-hedging hypothesis was inspired 2009; Boyce, Chesney, Alkon, Tschann, Adams et al., by the work of Boyce and Ellis (2005), who first 1995; Pluess & Belsky, 2011, 2013; Ellis et al., 2011). proposed that between-individual variation in biological Such for-better-and-for-worse susceptibility (Belsky, Bak- sensitivity to context – i.e. reactivity of neurobiological ermans-Kranenburg & van IJzendoorn, 2007) implies stress systems – can result from differences in experience that children may benefit or suffer differentially from (discussed below). In this paper, however, we are not such experiences as nurturance or abuse (Belsky & primarily concerned with the biological mechanisms that Pluess, 2009a, 2009b; Boyce et al., 1995), as well as from instantiate plasticity, or with the pathways through prevention and intervention efforts (Belsky & van which parents influence their offspring’s levels of plas- IJzendoorn, 2015; van IJzendoorn, Bakermans-Kranen- ticity. We provide references here (Belsky & Pluess, 2013; burg, Belsky, Beach, Brody et al., 2011). It is crucial to Ellis et al., 2011), and elsewhere in the paper, for readers recognize that for better and for worse, in this context, seeking more information about these mechanisms and refers to mental-health outcomes, not fitness payoffs. We processes. note this up front because we will later propose that, in fitness terms, plastic individuals achieve relatively fixed Motivating the model payoffs (rather than variable payoffs) across environ- mental conditions, because plasticity enables the devel- Our main goal is to present a mathematical model that opment of locally adaptive phenotypes (increasing evaluates the logical coherence of Belsky’s (1997, 2005; fitness), but also comes at a cost (reducing fitness). Belsky & Pluess, 2009a) bet-hedging hypothesis of A theoretical question is why between-individual var- differential plasticity. Specifically, we examine what are iation in plasticity exists. Explanations of differential the necessary conditions for natural selection to favor plasticity include differences in genes and epigenetic parents to hedge their bets by varying offspring plastic- regulation (Belsky et al., 2009; Belsky & Pluess, 2009a, ity. The idea that diversification of investments can be 2009b), as well as differences in prior experiences (Boyce & adaptive in an unpredictably fluctuating environment is Ellis, 2005; Ellis et al., 2011; Frankenhuis & Panchana- not novel: In both biology and economics, well-devel- than, 2011a, 2011b; Pluess & Belsky, 2011). This article oped literatures have addressed this issue, even if focuses on Belsky’s proposal (1997, 2005; Belsky & Pluess, psychologists – Belsky’s (1997, 2005; Belsky & Pluess, 2009a) that, when different levels of plasticity are optimal 2009a) intended audience – have not thought in such (in terms of biological fitness) in different environmental terms. Economists have focused on the conditions in states and the environment fluctuates unpredictably, which investors should diversify their portfolio so as to natural selection may favor parents producing offspring maximize their profit in a temporally fluctuating market with varying levels of plasticity. Before proceeding, a note (Bernoulli, 1738, trans. 1954; Markowitz, 1952; Stearns, on terminology: There is no implication that parents 2000). Biologists have focused on strategies that optimize deliberately weigh their options after estimating environ- organisms’ reproductive success in randomly varying mental variability and then decide on their offspring’s environments (reviewed in Childs, Metcalf & Rees, 2010; levels of plasticity. Rather, reproductive decisions result Donaldson-Matasci, Bergstrom & Lachmann, 2013; from mechanistic processes that are the products of Donaldson-Matasci, Lachmann & Bergstrom, 2008; natural selection; organisms need not be consciously Ellis, Figueredo, Brumbach & Schlomer, 2009; Meyers aware of these processes. Accordingly, when we refer to & Bull, 2002; Simons, 2009, 2011). As we will show parental ‘decisions’ or ‘choices’ – for instance, to produce below, Belsky’s (1997, 2005; Belsky & Pluess, 2009a) particular proportions of fixed and plastic offspring – we version of the bet-hedging argument is formally similar are referring to observable outcomes (epiphenomena) that to some classical bet-hedging models from biology (e.g. result from the entire array of causal mechanisms that Moran, 1992; Philippi & Seger, 1989; extended in determine behavior (from molecules to neural networks), Starrfelt & Kokko, 2012). including but not limited to cognitive processes. In biology, bet-hedging
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