Evolutionary diversification of ecological specialists under informed resource choice

Raphaël Scherrer, Joris Damhuis, G. Sander van Doorn, Rampal S. Etienne

Behavior can be an important modulator of eco-evolutionary dynamics and genetic evolution that is not always taken into account in models of evolutionary diversification. On the one hand, classical models for the evolution of ecological specialization have been extended to account for flexible behavioral aspects such as diet choice or matching habitat choice, but only in a subset of all spatial settings relevant for adaptive speciation. On the other hand, models of adaptive speciation have been synthesized to encompass different types of spatial settings - either promoting diversification through within-habitat frequency-dependent forces arising from competition, or between-habitat local adaptation independent of competition - albeit with non-flexible behavior. Here, we study individual-based simulations of the emergence of multiple resource specialist strategies, when individuals are allowed to choose their resource based on profitability in a two-resource, two-habitat environment, inspired from previous models of adaptive diversification. We join other authors in finding that active resource choice favors resource conservatism and the maintenance of a single specialist when individuals are already somewhat specialized on one resource. When individuals start off as generalists, however, active resource choice maintains the convergence stability of the generalist branching point - meaning that selection leads to the diversification of two specialists - in the face of strong ecological trade-offs, where evolution towards a single specialist would have otherwise been favored without resource choice. Active resource choice also turns frequency-independent processes of diversification (relying on local adaptation) into frequency-dependent ones (relying on competition) when resources are spatially restricted. Consequently, the chances of ecological divergence in spatially heterogeneous scenarios are maximized at intermediate levels of resource choice accuracy, where frequency-dependent selection balances out selection for resource conservatism. Finally, we find that active resource choice promotes divergence when resources are compartmentalized within microhabitats, by avoiding the waste of energy that foraging in poor microhabitats represents.