A generalised approach to the study and understanding of adaptive evolution

Abstract

Evolutionary theory has made large impacts on our understanding and management of the world, in part because it has been able to incorporate new data and new insights successfully. Nonetheless, there is currently a tension between certain biological phenomena and mainstream evolutionary theory. For example, how does the inheritance of molecular epigenetic changes fit into mainstream evolutionary theory? Is niche construction an evolutionary process? Is local adaptation via habitat choice also adaptive evolution? These examples suggest there is scope (and perhaps even a need) to broaden our views on evolution. We identify three aspects whose incorporation into a single framework would enable a more generalised approach to the understanding and study of adaptive evolution: (i) a broadened view of extended phenotypes; (ii) that traits can respond to each other; and (iii) that inheritance can be non‐genetic. We use causal modelling to integrate these three aspects with established views on the variables and mechanisms that drive and allow for adaptive evolution. Our causal model identifies natural selection and non‐genetic inheritance of adaptive parental responses as two complementary yet distinct and independent drivers of adaptive evolution. Both drivers are compatible with the Price equation; specifically, non‐genetic inheritance of parental responses is captured by an often‐neglected component of the Price equation. Our causal model is general and simplified, but can be adjusted flexibly in terms of variables and causal connections, depending on the research question and/or biological system. By revisiting the three examples given above, we show how to use it as a heuristic tool to clarify conceptual issues and to help design empirical research. In contrast to a gene‐centric view defining evolution only in terms of genetic change, our generalised approach allows us to see evolution as a change in the whole causal structure, consisting not just of genetic but also of phenotypic and environmental variables.

Experimental rapid and small-scale ecological population divergence in the absence of current natural selection

“…Our experimental results are largely consistent with predictions from theoretical (Bolnick & Otto, 2013;Edelaar et al, 2008Edelaar et al, , 2017Edelaar et al, , 2023Edelaar & Bolnick, 2012;Mortier et al, 2019;Ravigné et al, 2009;Scheiner et al, 2022) and empirical studies (Benkman, 2017;Camacho & Hendry, 2020;Holtmann et al, 2017;Porter & Benkman, 2022;Regan et al, 2022). Even more, MHC was able to operate in a novel environment and be based on a novel ecological trait.…”

Comparative transcriptome and methylome of polar bears, giant and red pandas reveal diet‐driven adaptive evolution

“…Adaptive evolution is a dynamic process by which species or populations become better suited to their environment through natural selection mechanisms (Edelaar et al., 2023 ). Organisms respond to environmental pressures like food or climate change by constantly adjusting their phenotype, making their phenotypic traits more favourable for survival in complex environments.…”

Quantifying heritability of the environment using animal models: a case study

“…However, recent studies have synthesized and highlighted how organisms can affect their local environment by either adjusting or selecting it to match their 'phenotypic templates' (Edelaar et al, 2019(Edelaar et al, , 2023K. Laland et al, 2016).…”

“…Under such circumstances, natural selection should favor mechanisms that facilitate individuals to select environments that best match their phenotypes (Davis & Stamps, 2004), or to modify them (Callahan et al, 2014). Thus, the causal relationship between organisms and their environment in adaptation terms can be bidirectional, the organism and the environment can each be changed to match the other (Edelaar et al, 2023; K. N. Laland & Sterelny, 2006).…”

“…Following the nest example, when a bird selects a nest site (such as a nest cavity), and its characteristics affect reproductive success, the outcome is similar to that of nest building, and nest site selection is expected to evolve. In this paper we focus on the selected habitat as an extended phenotype which can be inherited and therefore have its own evolutionary dynamics (Edelaar et al, 2023).…”