Mutualistic and antagonistic species interactions cause maladaptation beyond a geographic range limit that falls along a more apparent abiotic gradient

Background/Question/Methods

A species’ geographic range is a dynamic property that arises from the niche of the organism and historical contingencies that influence opportunities to disperse across landscapes. Understanding the determinants of species’ ranges is especially timely as it remains poorly understood how organisms will respond to the rapid pace of ongoing climate change. The causes of geographic range limits are ultimately evolutionary: the key question is why adaptation fails to occur at range margins? Therefore, experiments should ideally examine lifetime fitness to determine what factors cause maladaptation beyond range limits. Ecologists have increasingly used species distribution models to determine which abiotic variables are associated with geographic distributions and to generate hypotheses on range limiting factors to manipulate in experiments. However, these approaches have often overlooked the potential role of less apparent biotic interactions. We took an ecological genetic approach to test hypotheses on the limits to adaptation at the range margin of a California annual plant, Clarkia xantiana, which reaches its eastern range limit across an obvious abiotic gradient in precipitation. In particular, we used manipulative transplant experiments to examine the contribution of antagonistic and mutualistic interactions (herbivores, microbes, pollinators) to fitness and population persistence across and beyond the range limit.

Results/Conclusions

Biotic interactions made strong and unexpected contributions to maladaptation at and beyond the range margin. First, we found that the most effective pollinators (specialist bees) are entirely absent beyond the range, resulting in substantial pollen limitation of reproduction. Second, we found that unapparent fatal herbivory (by small mammals) increases exponentially at the range margin. Simulations and experiments further suggest that if fatal herbivory is eliminated, populations have the capacity to persist beyond the range. The strong non-linearity in both interactions at the range limit is consistent with predictions from theoretical models of what types of environmental gradients cause adaptation to fail. Last, we tested whether a lack of mutualistic soil microbes that mediate water and nutrient uptake limit lifetime fitness beyond the range. A combination of field and greenhouse experiments suggest that plant fitness beyond the range is reduced because of a lack of mutualist availability but elevated by escape from pathogens. In the case of both herbivore and microbe interactions, the strength of biotic interactions depends on the abiotic conditions in a given year. Taken together, our results indicate that biotic interactions play a central role in maladaptation despite the presence of an apparent and strong abiotic gradient.