Influence of Plasticity and Learning on Evolution under Directional Selection

Abstract

Phenotypic plasticity and related processes (learning, developmental noise) have been proposed to both accelerate and slow down genetically based evolutionary change. While both views have been supported by various mathematical models and simulations, no general predictions have been offered as to when these alternative outcomes should occur. Here we propose a general framework to study the effects of plasticity on the rate of evolution under directional selection. It is formulated in terms of the fitness gain gradient, which measures the effect of a marginal change in the degree of plasticity on the slope of the relationship between the genotypic value of the focal trait and log fitness. If the gain gradient has the same sign as the direction of selection, an increase in plasticity will magnify the response to selection; if the two signs are opposite, greater plasticity will lead to slower response. We use this general result to derive conditions for the acceleration/deceleration under several simple forms of plasticity, including developmental noise. We also show that our approach explains the results of several specific models from the literature and thus provides a unifying framework.Keywords: Baldwin effect, genetic assimilation, learning, plasticity, developmental noise, fitness landscape.The relationship between the genotype and the phenotype is molded by broadly defined phenotypic plasticity. This includes phenomena such as random events during development (developmental noise) and direct effects of the * E-mail: ingo.paenke@aifb.uni-karlsruhe.de. † E-mail: bernhard.sendhoff@honda-ri.de. ‡ Corresponding author; e-mail: tadeusz.kawecki@unifr.ch. environment (such as poor nutrition resulting in small size). It also includes fortuitous interference of environmental factors, with development resulting in qualitatively new phenotypes (e.g., morphological phenocopies produced by heat shock in the classic experiments of Waddington [1952]). Another category consists of adaptive responses that evolved to maximize fitness in a heterogeneous environment, for example, induced defenses against predators or parasites. Finally, phenomena such as learning, intelligence, or the "memory" of vertebrate adaptive immune systems allow an individual to develop, within its lifetime, an adaptive response to a novel challenge, even one never encountered in the evolutionary past of the species. Much theoretical and empirical research in the past two decades has focused on the evolution of those various mechanisms of plasticity.Less attention has been paid to the consequences of those plastic processes for evolution. As plasticity changes the genotype-phenotype map, it will also usually change the relationship between genotype and fitness and thus affect the response to natural or artificial selection. In particular, adaptive plasticity or learning may allow genetically unfit individuals to compensate for the inadequacies of their genotypes and still attain high fitness. As a consequence, the genetic variation for fitness...

Causes and Consequences of Behavioral Interference between Species

“…However, learning can be costly, such as when it results in the copying of maladaptive behavior that leads to the rejection of conspecific or acceptance of heterospecific mates, or misidentification of competitors [82,94]. Fourth, learning influences the strength and direction of selection by shaping phenotypic variation and its relationship to genetic variation [81]. For example, learned recognition can permit selection causing character displacement of recognition traits [82].…”

“…Current theory also fails to fully address the consequences of asymmetries in behavioral interference [79,80], while empirical research suggests that asymmetries are common and closely linked to the ecological and evolutionary consequences of the interactions [25,27,42,45,47]. Learned mate and competitor recognition also pose interesting and largely unexplored challenges (Box 4; see Outstanding Questions) [81,82]. Further integration of theoretical and empirical research is needed.…”

The interplay between genetic and learned components of behavioral traits

“…Andersson 1995;Dopazo et al 2001). Recent models (Borenstein et al 2006;Paenke et al 2007) represent an attempt at unifying these predictions and do so by defining the theoretical conditions under which one or the other effect of learning prevails. In particular, Paenke et al (2007) argue that the curvature of the fitness landscape predicts when adaptive learning accelerates or decelerates evolution because it determines whether learning confers a larger fitness increase to those phenotypes (as well as underlying genotypes) that are relatively closer to the fitness peak (see also Egas et al (2004) for a similar argument).…”

“…The common approach in theoretical studies of the Baldwin effect (including Paenke et al 2007) is to assume that the learning ability does not evolve. However, the emerging empirical evidence shows a genetic basis for learning ability such that it is possible to select for higher or lower levels of learning (McGuire and Hirsch 1977;Mery and Kawecki 2002;Dukas 2004).…”

Effects of dispersal plasticity on population divergence and speciation

“…That is, how does phenotypic plasticity influence population establishment or persistence (for example, Chevin et al, 2010)? Once the population has established itself, how does plasticity influence rates and patterns of adaptation (reviewed in Paenke et al, 2007)? Finally, following local adaptation, does plasticity affect mate choice (for example, Price et al, 2003;Craig et al, 2005;Edelaar et al, 2008;Deere et al, 2012) thus promoting speciation (for example, Edelaar et al, 2008;Havens and Etges, 2013)?…”