Maladaptation beyond a geographic range limit driven by antagonistic and mutualistic biotic interactions across an abiotic gradient

Abstract

Species’ geographic range limits often result from maladaptation to the novel environments beyond the range margin. However, we rarely know which aspects of the n‐dimensional environment are driving this maladaptation. Especially of interest is the influence of abiotic versus biotic factors in delimiting species’ distributions. We conducted a 2‐year reciprocal transplant experiment involving manipulations of the biotic environment to explore how spatiotemporal gradients in precipitation, fatal mammalian herbivory, and pollination affected lifetime fitness within and beyond the range of the California annual plant, Clarkia xantiana ssp. xantiana. In the first, drier year of the experiment, fitness outside the range edge was limited mainly by low precipitation, and there was some evidence for local adaptation within the range. In the second, wetter year, we did not observe abiotic limitations to plant fitness outside the range; instead biotic interactions, especially herbivory, limited fitness outside the range. Together, protection from herbivory and supplementation of pollen resulted in three‐ to sevenfold increases in lifetime fitness outside the range margin in the abiotically benign year. Overall, our work demonstrates the importance of biotic interactions, particularly as they interact with the abiotic environment, in determining fitness beyond geographic range boundaries.

Microbes, mutualism, and range margins: testing the fitness consequences of soil microbial communities across and beyond a native plant's range

“…Previous work has demonstrated that drought stress, herbivory, and pollen limitation all reduce mean fitness outside C. x. xantiana ’s range margin (Geber & Eckhart, 2005; Eckhart et al ., 2011; Moeller et al ., 2012; Benning et al ., 2019; Benning & Moeller, 2019). In this experiment we observed strong differentiation in soil microbial communities across the range boundary, and asked, does this microbial variation further contribute to C. x. xantiana ’s range limit?…”

“…Outside the range, we fully crossed all plant source populations with soil inocula from inside the range (but did not transplant soil inocula from outside the range into sites within the range). The experiment also included a caging treatment (where half of the grids within each treatment combination at each site were surrounded by wire caging) to test the effects of fatal mammal herbivory on lifetime fitness (reported in Benning & Moeller, 2019).…”

A systematic review of the direct and indirect effects of herbivory on plant reproduction mediated by pollination

“…Numerous mechanistic pathways can integrate the direct and indirect impacts of herbivores on plant reproduction through plant tissue, allocation strategies, and timing that impact plant pollination (Strauss, Conner & Rush, 1996;Mothershead & Marquis, 2000;Kelly et al, 2008;Botto-Mahan et al, 2011). In turn, negative impacts to pollinators can amplify the negative effects of herbivores on plant fitness by reducing both potential seed set (e.g., number of flowers available to set seed) (Strauss, Conner & Rush, 1996;Hambäck, 2001;Rusman et al, 2019) and actual seed set (i.e., flowers are not all pollinated due to decreased pollinator visitation) (Adler, Karban & Strauss, 2001;Benning & Moeller, 2019). The nature of how not only each type of herbivory, but also the joint impact of multiple types of herbivory impact pollination and plant reproduction are the basis of Fig.…”

Host-associated rhizobia fitness: Dependence on nitrogen, density, community complexity, and legume genotype

“…Biotic interactions have important consequences for population dynamics (Morris et al 2019), selection (Caruso et al 2017), and local adaptation (Runquist et al 2020) of interacting species. Of course, these biotic interactions do not occur in isolation and the benefits and costs of the interaction can be modified (Bronstein 1994) by population density, the presence of additional species (Wood et al 2018), genetics (Ford et al 2017) and abiotic factors such as resource availability (Schultz et al 2001;Lau et al 2014;Wurzburger & Ford Miniat 2014;Rivett et al 2016) or moisture levels (Wolinska & King 2009;Louthan et al 2018;Benning & Moeller 2019). These responses (i.e.…”