Spatially and temporally varying selection influence species boundaries in two sympatric Mimulus

Abstract

Spatially and temporally varying selection can maintain genetic variation within and between populations, but it is less well known how these forces influence divergence between closely related species. We identify the interaction of temporal and spatial variation in selection and their role in either reinforcing or eroding divergence between two closely related Mimulus species. Using repeated reciprocal transplant experiments with advanced generation hybrids, we compare the strength of selection on quantitative traits involved in adaptation and reproductive isolation in Mimulus guttatus and Mimulus laciniatus between two years with dramatically different water availability . We found strong divergent habitat-mediated selection on traits in the direction of species differences during a drought in 2013, suggesting that spatially varying selection maintains species divergence. However, a relaxation in divergent selection on most traits in an unusually wet year (2019), including flowering time, which is involved in pre-zygotic isolation, suggests that temporal variation in selection may weaken species differences. Therefore, we find evidence that temporally and spatially varying selection may have opposing roles in mediating species boundaries. Given our changing climate, future growing seasons are expected to be more similar to the dry year, suggesting that in this system climate change may actually increase species divergence.

Short-term fluctuating and long-term divergent selection on sympatric Monkeyflowers: insights from decade-spanning reciprocal transplants

“…As in previous studies (Ferris & Willis, 2018;Tataru et al, 2023) herbivory pressure differed significantly between habitats in all years with greater herbivory in M. guttatus's meadows : 2021 (meadow 22%, granite 1.97%; χ²=552.3, d.f. = 1, p < 0.0001), 2022 (meadow 37.75%, granite 2.58%; χ²=921.78, d.f.…”

“…Here, we build on previous work investigating spatial and temporal variation in natural selection on interspecific divergence between Mimulus guttatus and M. laciniatus to provide five years of repeated reciprocal transplant experiments under dramatically varying abiotic conditions (Figure 1). Previously, hybrids and parents were transplanted into each species' habitat in Yosemite National Park, CA during years of historically low (Ferris & Willis, 2018) and high snowpack (Tataru et al 2023). Weaker divergent selection on a key isolating barrier, flowering time, was found during the high snowpack year which could erode species differentiation.…”

Local adaptation to an altitudinal gradient: the interplay between mean phenotypic trait variation and phenotypic plasticity inMimulus laciniatus

“…Our data supports the idea that highly lobed leaf shape is locally adaptive in high elevation and northern populations of M. laciniatus . In adaptation between Mimulus species we see evidence that ephemeral water availability in M. laciniatus’s dry rocky habitat may be driving the evolution of lobed leaf shape (Tataru et al 2023; Ferris and Willis 2018). However high elevation highly lobed populations of M. laciniatus tend to have higher water availability than low elevation populations with less lobing, implying that the selective force causing local adaptation in leaf shape within this species may be different than the force driving divergent evolution between species.…”

“…Given the likely genetic correlation this more universal plastic response in flowering and height across M. laciniatus populations may be due to genetic constraint (Auld, Agrawal, and Relyea 2010). Previous reciprocal transplant experiments have demonstrated that early flowering time is under strong selection in M. laciniatus ’ harsh rocky outcrop environments (Tataru et al 2023; Ferris and Willis 2018). Given the ephemeral nature of water availability in the shallow rocky soils of this species’ habitat and the significant variation in the amount and timing of snow melt from year to year it seems likely that an ability to respond plastically in the timing of flowering is adaptive across M. laciniatus’ range.…”

“…Reciprocal transplant experiments have found selection for early flowering time, more highly lobed leaves, and larger flowers in M. laciniatus’ s harsh granite outcrop habitat (Ferris and Willis 2018; Tataru, Wheeler, and Ferris 2023). However, it is not known whether these same traits are involved in local adaptation across M. laciniatus’ s range.…”