Contrasting environmental factors drive local adaptation at opposite ends of an environmental gradient in the yellow monkeyflower (Mimulus guttatus)

Abstract

Premise Identifying the environmental factors responsible for natural selection across different habitats is crucial for understanding the process of local adaptation in plants. Despite its importance, few studies have successfully isolated the environmental factors driving local adaptation in nature. In this study, we evaluated the agents of selection responsible for local adaptation of the monkeyflower Mimulus guttatus to California's coastal and inland habitats. Methods We implemented a manipulative reciprocal transplant experiment at coastal and inland sites, where we excluded aboveground stressors in an effort to elucidate their role in the evolution of local adaptation. Results Excluding aboveground stressors, most likely a combination of salt spray and herbivory, completely rescued inland annual plant fitness when transplanted to coastal habitat. The exclosures in inland habitat provided a benefit to the performance of coastal perennial plants. However, the exclosures are unlikely to provide much fitness benefit to the coastal plants at the inland site because of their general inability to flower in time to escape from the summer drought. Conclusions Our study demonstrates that a distinct set of selective agents (aboveground vs. belowground) are responsible for local adaptation at opposite ends of an environmental gradient.

The evolution of thermal performance in native and invasive populations of Mimulus guttatus

“…This conclusion is consistent with genomic data which reveal high rates of gene flow among coastal populations occupying similar latitudes in the native range relative to our study populations (Twyford & Friedman, 2015). Nonetheless, our findings are particularly surprising given the numerous studies documenting local adaptation to edaphic and hydrological conditions within the M. guttatus species complex (Hall & Willis, 2006; Wu et al, 2008; Lowry et al, 2009; Hall, Lowry, & Willis, 2010; Kooyers, Greenlee, Colicchio, Oh, & Blackman, 2015; Selby & Willis, 2018; Popovic & Lowry, 2020), and the evolution of parallel phenotypic clines in the introduced ranges of several species (van Boheemen et al, 2019; Hernández et al, 2019; McGoey, Hodgins, & Stinchcombe, 2020). Overall, our results suggest that while specializing in hydrological and edaphic aspects of niche space, native M. guttatus populations may be thermal generalists despite spanning a broad temperature gradient in western North America.…”

Divergence in bidirectional plant-soil feedbacks between montane annual and coastal perennial ecotypes of yellow monkeyflower (Mimulus guttatus)

“…Although plant-soil feedbacks affected most traits, plants in all-home (vs. all-away) soil+biota combinations did not exhibit the relatively high-performance characteristic of local adaptation. Thus, the coastal-montane adaptation evident in M. guttatus reciprocal transplants (Hall & Willis, 2006; Popovic & Lowry, 2020) may be mediated primarily by climate or other factors. Local adaptation appears common in home vs. away plant-soil-AMF combinations (Rúa et al , 2016), but non-AMF negative interactions in our whole soil treatments may outweigh any locally-adapted AMF associations (see below).…”

Plant–environment interactions from the lens of plant stress, reproduction, and mutualisms

“…Two contributions to this issue consider environmental factors as agents of selection by performing either reciprocal transplants or long-term analyses of selection in the wild. Popovic and Lowry (2020) used reciprocal transplants between inland and coastal lineages of Mimulus guttatas along with experimental exclosures that removed aboveground herbivores and salt spray. Strikingly, they found the fitness of inland lineages-which normally experience high rates of death in the coastal environment-to be completely rescued by exclosures at coastal sites, providing evidence that salt spray and/or herbivory were likely agents of selection.…”