Abstract
Organisms continuously modify their living conditions via extended genetic effects on their environment, microbiome, and in some species culture. These effects can impact the fitness of current but also future conspecifics due to non-genetic transmission via ecological or cultural inheritance. In this case, selection on a gene with extended effects depends on the degree to which current and future genetic relatives are exposed to modified conditions. Here, we detail the selection gradient on a quantitative trait with extended effects in a patch-structured population, when gene flow between patches is limited and ecological inheritance within patches can be biased towards offspring. Such a situation is relevant to understand evolutionary driven changes in individual condition that can be preferentially transmitted from parent to offspring, such as cellular state, micro-environments (e.g., nests), pathogens, microbiome, or culture. Our analysis quantifies how the interaction between limited gene flow and biased ecological inheritance influences the joint evolutionary dynamics of traits together with the conditions they modify, helping understand adaptation via non-genetic modifications. As an illustration, we apply our analysis to a gene-culture coevolution scenario in which genetically-determined learning strategies coevolve with adaptive knowledge. In particular, we show that when social learning is synergistic, selection can favour strategies that generate remarkable levels of knowledge under intermediate levels of both vertical cultural transmission and limited dispersal. More broadly, our theory yields insights into the interplay between genetic and non-genetic inheritance, with implications for how organisms evolve to transform their environments.
Highlights
Genes often exert effects that extend beyond the organism in which they are expressed, for instance by modifying the physical environment, by altering ecological interactions, or by creating cultural knowledge
While feedbacks between genes and the environment can impact evolutionary dynamics in various ways (Robertson, 1991), their relevance for adaptation depends on the associations between genes, their extended effects and fitness (Dawkins, 1982; Dawkins, 2004; Brodie, 2005; Govaert et al, 2019)
Consider for instance a genetic locus that influences the quality of individual nests. For selection at this locus to causally depend on feedback effects, genetic variation must be linked to nest variation such that over generations, genes associated with ‘‘good” nests replicate at the expense of competitor genes associated with ‘‘bad” nests
Summary
Genes often exert effects that extend beyond the organism in which they are expressed, for instance by modifying the physical environment (as with the building of nests or burrows), by altering ecological interactions (as when immunity genes influence an organism’s pathogens or microbiotic symbionts), or by creating cultural knowledge (as with the collection and dissemination of information about the environment; Dawkins, 1982; Lewontin, 1983; Odling-Smee et al, 2003; Bailey, 2012; Govaert et al, 2019). Evolutionary dynamics have been examined either under vertical transmission in panmictic populations (e.g., Kirkpatrick and Lande, 1989; Pál and Miklós, 1999; Bonduriansky and Day, 2009; Mullon and Lehmann, 2017), or under random transmission combined with limited gene flow (i.e., assuming that transmission within groups or spatial clusters that include parents and their offspring occurs randomly, Brown and Hastings, 2003; Hui et al, 2004; Silver and Di Paolo, 2006; Wakano, 2007; Lehmann, 2008; Han et al, 2009; Best et al, 2010; Débarre et al, 2012; Horns and Hood, 2012; Lion and Gandon, 2015; Mullon and Lehmann, 2018; Joshi et al, 2020; but see Ohtsuki et al, 2017, for a specific model of biased cultural inheritance under limited dispersal) To fill this gap, we compute the selection gradient acting on a genetic locus with extended effects (e.g., on nest quality, pathogen load or cultural information) in a patch-structured population, where dispersal among patches is limited and extended effects can be transmitted across generations in a biased manner within patches. We discuss how our framework can be useful to study other biological problems, such as host evolution to pathogens, symbiotic mutualism, and niche construction
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