Animal learning as a source of developmental bias

Abstract

As a form of adaptive plasticity that allows organisms to shift their phenotype toward the optimum, learning is inherently a source of developmental bias. Learning may be of particular significance to the evolutionary biology community because it allows animals to generate adaptively biased novel behavior tuned to the environment and, through social learning, to propagate behavioral traits to other individuals, also in an adaptively biased manner. We describe several types of developmental bias manifest in learning, including an adaptive bias, historical bias, origination bias, and transmission bias, stressing that these can influence evolutionary dynamics through generating nonrandom phenotypic variation and/or nonrandom environmental states. Theoretical models and empirical data have established that learning can impose direction on adaptive evolution, affect evolutionary rates (both speeding up and slowing down responses to selection under different conditions) and outcomes, influence the probability of populations reaching global optimum, and affect evolvability. Learning is characterized by highly specific, path-dependent interactions with the (social and physical) environment, often resulting in new phenotypic outcomes. Consequently, learning regularly introduces novelty into phenotype space. These considerations imply that learning may commonly generate plasticity first evolution. K E Y W O R D Sdevelopmental bias, evolvability, learning, plasticity, plasticity first

Historical and philosophical perspectives on the study of developmental bias

“…In a similar vein, the contributions to this special issue illustrate that the study of developmental bias spans different biological domains (and thus implicates different fields): gene regulation (e.g., Hu et al, 2019), parthenogenesis (Galis & van Alphen, 2019), phenotypic plasticity (Draghi, 2019;Levis & Pfennig, 2019;Parsons et al, 2019;Uller et al, 2019), the morphology of extant and fossil species (Jablonski, 2019;Jackson, 2019), brain development (Finlay & Huang, 2019), symbiosis and interactions involving microbial species (Gilbert, 2019), development of the vertebrate skeleton (Kavanagh, 2019), and behavior, learning, and niche construction (Hu et al, 2019;Laland et al, 2019), among others. Some of the studies are experimental, some include field work, and others make primarily use of theory and computational simulation (Draghi, 2019;Hordijk & Altenberg, 2019).…”

“…Salazar-Ciudad (2006) made the suggestion to replace the concept of developmental constraint with the concept of the variational properties of a developmental mechanism, which might also be a possible alternative to "developmental bias." Cases of niche construction and animal learning can lead to biases, in which case organism-environment mutual influences, organism-organism interactions, and animal behavior are part of the "developmental" account (Hu et al, 2019;Laland et al, 2019). As a result, my view is that for the purpose of setting a compelling explanatory agenda and of generating significant intellectual identity across different research projects, the label of "developmental bias" is preferable (similar to how the notion of novelty emphasizes the origin of quantitatively new structures).…”

“…Many will argue that an explanation of developmental bias requires more than the study of gene regulatory mechanisms. Indeed, several of the contributions to this special issue investigate cases where phenotypic plasticity (Draghi, 2019;Levis & Pfennig, 2019;Parsons, McWhinnie, Pilakouta, & Walker, 2019;Uller, Feiner, Radersma, Jackson, & Rago, 2019), niche construction (Hu et al, 2019;Laland, Toyokawa, & Oudman, 2019), and symbiosis (Gilbert, 2019) form the basis for biases in phenotypic variation. Generally, phenotypic variation is not only generated by means of mutations, but also by environmental changes, where such environmentally induced variation can matter for evolution (Sultan, 2017;West-Eberhard, 2003).…”

“…Biases result not only from the organization of gene regulatory networks, but in many cases also from the nature of phenotypic plasticity, so that the interaction between development and an organism's environment has to be part of the explanatory story (Draghi, ; Levis & Pfennig, ; Parsons et al, ; Uller et al, ). Cases of niche construction and animal learning can lead to biases, in which case organism–environment mutual influences, organism–organism interactions, and animal behavior are part of the “developmental” account (Hu et al, ; Laland et al, ). Examples of developmental biases due to symbiosis likewise broaden the scope of a general explanatory framework that can include metabolic and physiological interactions between organisms of different species (Gilbert, ).…”

Biases in the study of developmental bias

“…The significance of learning as a potential source of bias in the production of evolutionarily relevant phenotypic variation is the focus of a contribution by Laland, Toyokawa, and Oudman (). Learning does many things for organisms: It may help solve problems and increase adaptive fit, it may solve novel problems and hence introduce novel phenotypes into phenotype space, and if learning occurs via observing other individuals it may fuel the nongenetic inheritance of acquired traits.…”