Life history trait divergence among populations of a non-palatable species reveals strong non-trophic indirect effects of an abundant herbivore

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Abstract

When large herbivores exert selection on their prey plant species, co-occurring, non-prey species may experience selection through non-trophic indirect effects. Such selection is likely common where herbivores are overabundant. Yet, empirical studies of non-trophic indirect effects as drivers of non-prey trait evolution are lacking. Here we test for adaptive shifts in life history traits in an unpalatable species, Arisaema triphyllum, a common forest perennial that is unique because it exhibits size-dependent sex switching. We collected A. triphyllum from six sites that experience a gradient in abiotic stress caused by deer browse pressure on prey plant species that generate indirect effects. We grew A. triphyllum from these sites in a common garden for five years to evaluate life history predictions linking strong indirect effects and abiotic stress to changes in life history traits: flowering onset size threshold, female flowering size threshold, relative growth rate (RGR), biomass allocation, and asexual reproduction. Despite observed differences among phenotypes in the field, expression of flowering onset size threshold, biomass allocation, and asexual reproduction did not differ among the six populations in the garden, indicating common plastic responses. In contrast, A. triphyllum collected from sites experiencing the two highest deer impacts exhibited smaller female flowering size thresholds and the highest RGR. Responses in these traits support the predictions of adaptive divergence in response to indirect effects. Our results reinforce the idea that non-trophic indirect effects of large herbivores can elicit evolutionary responses in some traits of non-prey species. In general, life history traits of unpalatable species may be cryptically adapting to stressful indirect effects where large herbivores are overabundant.

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