Evolution in response to an abiotic stress shapes species coexistence

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Abstract

Adaptation to abiotic stresses is pervasive and generally relies on traits that are not independent from those affecting species interactions. Still, how such evolution affects species coexistence remains elusive. We addressed this using populations of two herbivorous spider mite species ( Tetranychus urticae and T. evansi ) evolving separately on tomato plants hyper-accumulating cadmium, a stressful environment for the mites, or on control plants with no-cadmium. Combinations of phenotypic analyses with structural stability theory predicted that adaptation of both species to cadmium allow them to coexist in that environment, whereas for cadmium-naïve mite populations the most likely outcome is competitive exclusion. The shift from exclusion to coexistence was due to an increase in structural niche differences caused by a simultaneous increase in intra and a decrease in interspecific competition. However, adaptation to cadmium did not affect species interactions and competitive outcomes in the cadmium-free environment, indicating that such evolutionary changes were environment-specific. Experimental outcomes of population dynamics with populations of the two species from each selection regime in each environment were fully compatible with model predictions. Therefore, evolution of single species in a new environment, even in absence of interspecific competitors, shapes species coexistence. Hence, population shifts to novel environments may have unforeseen evolutionary consequences for community composition and the maintenance of species diversity.

Significance Statement

The evolutionary consequences of strong selective pressures imposed by environmental changes on species interactions and their subsequent coexistence remain largely unknown. To fill this knowledge gap, we combined the power of experimental evolution and structural stability to analyze how evolution of two spider mite species on plants with or without cadmium affected their ability to coexist. We found that evolution in the high cadmium environment led to changes in growth rates, but also in the strength of intra-and interspecific competition, such that coexistence became possible, but only when the two species evolved in the new environment. Our study highlights that evolution under high pollutant concentrations, even in the absence of competitors, can shape long-term coexistence between species.

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