Comparing the consequences of natural selection, adaptive phenotypic plasticity, and matching habitat choice for phenotype–environment matching, population genetic structure, and reproductive isolation in meta‐populations

Abstract

Organisms commonly experience significant spatiotemporal variation in their environments. In response to such heterogeneity, different mechanisms may act that enhance ecological performance locally. However, depending on the nature of the mechanism involved, the consequences for populations may differ greatly. Building on a previous model that investigated the conditions under which different adaptive mechanisms (co)evolve, this study compares the ecological and evolutionary population consequences of three very different responses to environmental heterogeneity: matching habitat choice (directed gene flow), adaptive plasticity (associated with random gene flow), and divergent natural selection. Using individual‐based simulations, we show that matching habitat choice can have a greater adaptive potential than plasticity or natural selection: it allows for local adaptation while protecting genetic polymorphism despite global mating or strong environmental changes. Our simulations further reveal that increasing environmental fluctuations and unpredictability generally favor the emergence of specialist genotypes but that matching habitat choice is better at preventing local maladaptation by individuals. This confirms that matching habitat choice can speed up the genetic divergence among populations, cause indirect assortative mating via spatial clustering, and hence even facilitate sympatric speciation. This study highlights the potential importance of directed dispersal in local adaptation and speciation, stresses the difficulty of deriving its operation from nonexperimental observational data alone, and helps define a set of ecological conditions which should favor its emergence and subsequent detection in nature.

Matching habitat choice and plasticity contribute to phenotype–environment covariation in a stream salamander

“…This study validates matching habitat choice as a mechanism of phenotype-environment matching, even under complex and dynamic natural conditions (Edelaar et al 2017, Nicolaus andEdelaar 2018). More broadly, our results show how crucial it is to account for movement in ecological and evolutionary research.…”

“…immediate and stronger when integrated over time. Additionally, the combined effects of matching habitat choice and phenotypic plasticity should increase phenotypic divergence among sites that differ in environmental stimuli (Jacob et al 2015, Nicolaus andEdelaar 2018) and influence any processes sensitive to the rate of phenotypic response (Harvell 1990, Padilla and Adolph 1996, DeWitt et al 1998.…”

Habitat choice stabilizes metapopulation dynamics by enabling ecological specialization

“…No control during any phase of dispersal likely applies to very few real systems such as wind‐dispersed plants. Many organisms are capable of more selective ways of moving than just random dispersal, illustrated by obvious examples of habitat preference based on colour matching (Gillis , Ahnesjö and Forsman ), the use of specific cues during movement (Prokopy ) and habitat choice (Jaenike and Holt , Edelaar et al , Jacob et al , ). Selective movement is even found in organisms for which it seems less obvious, such as zoochorous plants that disperse their seeds to suitable habitat via animals (Spiegel and Nathan ) or plankton that drift on currents but are able to select where to settle (Bonte et al , Burgess et al ).…”

“…However, if dispersal involves habitat choice, then dispersal and ecological specialization may be reconcilable (theory: Holt and Barfield , Armsworth , Ravigné et al , Bolnick and Otto , Scheiner ; empirical: Rice and Salt , Jacob et al , ). Habitat choice implies a non‐random subset of the local population dispersing and/or dispersers redistributing themselves in a non‐random way across a heterogeneous landscape (Holt , Rice and Salt , Edelaar et al , Edelaar and Bolnick ).…”

“…Habitat choice, affecting the evolution of dispersal and specialization in a heterogeneous landscape, is expected to affect ecological dynamics in the same, short time frame at both the local and metapopulation level (Hendry , Bonte et al ). First, local adaptation should increase population growth rate by increasing individual fitness.…”