Earlier spring reduces potential for gene flow via reduced flowering synchrony across an elevational gradient

Abstract

One of the best-documented ecological responses to climate warming involves temporal shifts of phenological events. However, we lack an understanding of how phenological responses to climate change vary among populations of the same species. Such variability has the potential to affect flowering synchrony among populations and hence the potential for gene flow. METHODS: To test whether an earlier start of the growing season affects the potential for gene flow among populations, we quantified the distributions of flowering times of two spring-flowering plants (Trillium erectum and Erythronium americanum) over 6 years along an elevational gradient. We developed a novel model-based metric of potential gene flow between pairs of populations to quantify the potential for pollen-mediated gene flow based on flowering phenology. RESULTS: Earlier onset of spring led to greater separation of peak flowering dates across the elevational gradient for both species investigated, but was only associated with a reduction in potential gene flow in T. erectum, not E. americanum. CONCLUSIONS: Our study suggests that climate change could decrease gene flow via phenological separation among populations along climatic gradients. We also provide a novel method for quantifying potential pollen-mediated gene flow using data on flowering phenology, based on a quantitative, more biologically interpretable model than other available metrics.

Long‐term changes in flowering synchrony reflect climatic changes across an elevational gradient

“…Changing conditions in temperature and precipitation across elevations are associated with large shifts in flowering synchrony both within species in different communities and among species in the same community over the last four decades. Because flowering synchrony affects gene flow (via pollen transfer among conspecifics), reproductive interference (via pollen transfer among heterospecifics) and competition as well as facilitation for pollination services, the reduced flowering phenology overlap observed will likely directly affect plant fitness (Ghazoul 2006, Morales and Traveset 2008, Ison et al 2014, Gleiser et al 2018, Hall et al 2018, Kehrberger and Holzschuh 2019, Rivest et al 2021). At the same time, reduced flower availability over time will likely affect pollinator fitness (Rundlöf et al 2014, Kaluza et al 2018, Schenk et al 2018), and ultimately the consequences are likely to be felt throughout ecosystems as processes such as nutrient cycling are altered (Forrest and Miller‐Rushing 2010, Delgado‐Baquerizo et al 2013, González de Andrés 2019).…”

Does Phenological Plasticity Help or Hinder Range Shifts Under Climate Change?

“…In the context of climate change, phenological plasticity may disrupt these patterns of historical gene flow. For example, advancing flowering phenology actually led to greater separation of peak flowering, and reduced potential for gene flow among populations along elevational gradients in Trillium erectum (Rivest et al, 2021). Alternatively, adaptive phenological plasticity could facilitate the spread of warm-adapted alleles by enabling trailing-edge genotypes to successfully migrate and interbreed with populations throughout the species' range, contributing to greater genetic variation and adaptive potential (Ensing and Eckert, 2019).…”

The ecological implications of intra‐ and inter‐species variation in phenological sensitivity

“…For example, the timing of leaf out, flowering, and fruiting have been found to be more sensitive to temperature in warmer regions across many plant species in temperate ecosystems (Zhang et al ., 2015; Park et al ., 2019). Thus, with climate change, intraspecific interactions and gene flow can be altered (Fox, 2003; Rivest et al ., 2021; Park et al ., 2022) and phenological synchrony between interacting species may shift heterogeneously across the landscape, differing among populations or morphotypes (Park et al ., 2022). Knowledge of both intra‐ and interspecific variation in phenological responses is therefore critical to assessing the ecological impacts of climate change.…”

“…For example, the timing of leaf out, flowering, and fruiting have been found to be more sensitive to temperature in warmer regions across many plant species in temperate ecosystems (Zhang et al, 2015;Park et al, 2019). Thus, with climate change, intraspecific interactions and gene flow can be altered (Fox, 2003;Rivest et al, 2021;Park et al, 2022) This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.…”