Linking ecological niche models and common garden experiments to predict phenotypic differentiation in stressful environments: Assessing the adaptive value of marginal populations in an alpine plant

Abstract

Environmental variation within a species’ range can create contrasting selective pressures, leading to divergent selection and novel adaptations. The conservation value of populations inhabiting environmentally marginal areas remains in debate and is closely related to the adaptive potential in changing environments. Strong selection caused by stressful conditions may generate novel adaptations, conferring these populations distinct evolutionary potential and high conservation value under climate change. On the other hand, environmentally marginal populations may be genetically depauperate, with little potential for new adaptations to emerge. Here, we explored the use of ecological niche models (ENMs) linked with common garden experiments to predict and test for genetically determined phenotypic differentiation related to contrasting environmental conditions. To do so, we built an ENM for the alpine plant Silene ciliata in central Spain and conducted common garden experiments, assessing flowering phenology changes and differences in leaf cell resistance to extreme temperatures. The suitability patterns and response curves of the ENM led to the predictions that: (1) the environmentally marginal populations experiencing less snowpack and higher minimum temperatures would have delayed flowering to avoid risks of late‐spring frosts and (2) those with higher minimum temperatures and greater potential evapotranspiration would show enhanced cell resistance to high temperatures to deal with physiological stress related to desiccation and heat. The common garden experiments revealed the expected genetically based phenotypic differentiation in flowering phenology. In contrast, they did not show the expected differentiation for cell resistance, but these latter experiments had high variance and hence lower statistical power. The results highlight ENMs as useful tools to identify contrasting putative selective pressures across species ranges. Linking ENMs with common garden experiments provides a theoretically justified and practical way to study adaptive processes, including insights regarding the conservation value of populations inhabiting environmentally marginal areas under ongoing climate change.

Top ten hazards to avoid when modeling species distributions: a didactic guide of assumptions, problems, and recommendations

“…niche conservatism over space), which may closely approximate reality for many taxa and commonly used predictor variables (Peterson 2011). However, in an increasing number of studies, genetically determined differences have been documented for factors related to distributional limits among populations (Pelini et al 2009, Fournier‐Level et al 2011, Morente‐López et al 2022, Franklin 2023). Whereas the problem of violating this assumption of stationarity in SDMs has been addressed in studies of invasive species (van Boheemen et al 2019, Pili et al 2020), phylogeography (Costa et al 2002), and climate change (Fitzpatrick and Keller 2015, Moran and Ormond 2015, Martin et al 2020), resolving it fully involves multiple conceptual and practical challenges (Smith et al 2019).…”

“…Recommendations. Based on existing natural history or physiological information, researchers should strive to select environmental variables known or suspected to have a direct effect on suitability for the species, at relevant spatial and temporal resolutions (Hazard 1; Mod et al 2016, Petitpierre et al 2017, Reside et al 2019, Morente‐López et al 2022). Fortunately, advances continue regarding variables with various spatial resolutions and potentially tighter links with species physiologies (e.g.…”

Chronosequence of invasion reveals minimal losses of population genomic diversity, niche expansion, and trait divergence in the polyploid, leafy spurge

“…We developed an ecological niche model (ENM) using MaxEnt v.3.4.3 (Merow et al 2013;Phillips et al 2017) with the 'dismo' package in R (Hijmans et al 2022). Our goal was identify environmental gradients that could potentially drive phenotypic evolution during range expansion (Elith and Leathwick 2009;Araújo et al 2019;Morente-López et al 2022). We built ENMs with the same bioclimatic variables and in the same bounding box as the analyses of niche differentiation.…”

“…Alternatively, researchers have started to use ecological niche models (ENMs) to identify important environmental gradients that span from optimal to marginal habitat, such as from a range core to edge. Predictions are then made about traits that may promote adaptation to the novel environments found in marginal habitats (Searcy and Shaffer 2016;Dixon and Busch 2017;Capblancq et al 2020;Morente-López et al 2022). Finally, common garden experiments can determine whether the putative traits under selection have differentiated across the key environmental gradients identified by ENMs.…”

Marine environmental pollution and offshore aquaculture structure: Evidence from China

“…Specifically, if effects are nonlinear with respect to degree of pollution, then two individuals facing various degree of pollution will experience different marginal damages, even if they are identical in terms of all other factors that determine vulnerability; In cases where the terrigenous waste is still the main source of marine pollution, compared with modern marine cultured modes concealing itself at a safe distance from the coast, the fishery cultures (e.g., oyster beds), on the mudflats, suffer from more serious pollution. Therefore, Differences in marginal damages may also arise because environmental conditions and geographical location differ across populations (Morente-Loṕez et al, 2022). Alternatively-or in addition, even if two individuals are identical in terms of degree of pollution, heterogeneity also may stem from differences in individual adaptability that controls how pollution translates into damages, such as defensive investments (e.g., building a canal.)…”