Simone Fior

Evolution is expected to be crucial for the persistence of some populations exposed to changing climate, but demonstrations of rapid evolution in wild populations associated with ongoing climate change are scarce. Inferences about possible adaptive responses rest heavily on “space-for-time” approaches that are fraught with assumptions that are difficult to verify. In contrast, resurrection experiments offer a direct method to observe evolutionary changes over time but rarely span the periods of several decades over which climatic shifts have occurred. In this study, we integrated space-for-time, environmental manipulation, and resurrection experiments to investigate the evolution of the annual plant Lactuca serriola following 44 years of climate change in Israel and the Golan Heights. We found that contemporary plants flowered over 7 d earlier, a putative adaptation to increasingly warm and dry conditions, and also flowered earlier under experimental drought. However, in contrast to these patterns, plants originating from wetter populations flowered earlier than those from drier populations, indicating a mismatch between space-for-time predictions and observed temporal shifts in phenology. Our findings provide direct evidence for evolution in response to climate change in a wild species, while cautioning against applying predictions made from space-for-time studies to future climate change responses.

Arctic warming has coincided with dramatic changes in plant cover, but the impact that aboveground biomass shifts have on soil microbial communities and processes remains poorly understood. To address this, we investigated spatial patterns of soil microbes in relation to vegetation changes using a space-for-time approach in the high Arctic region of Longyearbyen, Svalbard. We collected and characterized 31 topsoil samples from three sites that differed in nutrient input, CO2 flux, soil chemistry, and plant cover. Pronounced vegetation differences were observed at fine spatial scales, including a highly localized graminoid-dominated hotspot within areas of mixed plant communities. This graminoid-rich hotspot coincided with locally elevated soil fertility and exhibited particularly high CO2 fluxes. In areas that transitioned from dwarf shrub- to graminoid-dominated vegetation, we observed an increase in estimated fungal abundance, a shift from heterogeneous to Ascomycota-dominated fungal communities, and a greater abundance of r-strategist prokaryotes. Multiple regression on biotic and abiotic distance matrices revealed that soil fungi may be especially sensitive to changes compared to prokaryotes and plants. These findings highlight the need for future experiments investigating fungi in high Arctic tundra to better understand feedback between biotic and abiotic factors under warming.

The Arctic has become warmer and greener in recent decades, mostly attributed to large-scale climatic influences, but greening trends are not ubiquitous. To gain insight into possible drivers of variation in Arctic greening, we investigated how plant functional traits and community composition vary along local gradients of soil disturbance and fertility on the High Arctic archipelago of Svalbard. Our goal was to investigate the possible contribution of shifts in community composition and plant traits to overall greening, to deepen our understanding of how rapidly vegetation change may occur under continued warming and associated changes in soil conditions. We found that local variation in soil conditions, particularly nutrient availability, interacts with regional climate to shape species composition, abundance, and trait expression. Nutrient-enriched environments, such as below bird cliffs and in human settlements, host many generalist tundra species that exhibit higher productivity and elevated trait values compared to communities growing in nutrient-poor tundra. These findings suggest that Arctic greening may occur rapidly, by favouring responsive species already present in tundra communities as edaphic and climatic conditions become more favourable.

Adaptive evolution is key for species to persist in a warming climate. However, how adaptive genetic variants arise and shape both past and future evolutionary trajectories remains largely unknown. In this work, we integrate genomics with functional and ecological assays to unravel the evolutionary history and adaptive potential of alleles governing adaptation to climate through flowering time in an Alpine carnation. We reveal that “warm” and “cold” alleles of the flowering inhibitor CENTRORADIALIS ( DsCEN/2 ) originated through recombination of highly divergent haplotypes during the carnation radiation, implicating ancestral variation in seeding climate-adaptive alleles. These alleles survived in glacial refugia before mediating the species’ range expansion in response to postglacial warming. We predict that, by recapitulating past evolution, warm alleles will continue to facilitate adaptation under future climate change.

Spatially divergent natural selection can drive adaptation to contrasting environments and thus the evolution of ecotypes. In perennial plants, selection shapes life history traits by acting on subsequent life stages, each contributing to fitness. While evidence of adaptation in perennial plants is common, the expression of life history traits is rarely characterized, limiting our understanding of their role in adaptive evolution. We conducted a multi‐year reciprocal transplant experiment with seedlings from low and high elevation populations of the alpine carnation Dianthus carthusianorum to test for adaptation linked to contrasting climates and inferred specific contributions of early life stages to fitness. We assessed genotype by environment interactions in single fitness components, applied matrix population models to achieve an integrated estimate of fitness through population growth rates, and performed trade‐off analyses to investigate the advantage of alternate life history traits across environments. We found evidence of genotype by environment interactions consistent with elevational adaptation at multiple stages of the early life cycle. Estimates of population growth rates corroborated a strong advantage of the local genotype. Early reproduction and survival are alternate major contributors to adaptation at low and high elevation, respectively, and are linked by trade‐offs that underlie the evolution of divergent life history traits across environments. While these traits have a strong genetic basis, foreign populations express co‐gradient plasticity, reflecting the adaptive strategy of the local populations. Our study reveals that selection associated to climate has driven the evolution of divergent life histories and the formation of elevational ecotypes. While the high energy environment and strong competition favor investment in early reproduction at low elevation, limiting resources favor a more conservative strategy relying on self‐maintenance at high elevation. The co‐gradient plasticity expressed by high‐elevation populations may facilitate their persistence under warming climatic conditions.

Summary: Local adaptation to contrasting environmental conditions along environmental gradients is a widespread phenomenon in plant populations, yet we lack a mechanistic understanding of how individual agents of selection contribute to this evolutionary process. Here, we developed a novel evolutionary functional–structural plant (E‐FSP) model that recreates local adaptation of virtual plants along an environmental gradient. First, we validate the model by testing if it can reproduce two elevational ecotypes of Dianthus carthusianorum occurring in the Swiss Alps. Second, we use the E‐FSP model to disentangle the relative contribution of abiotic (temperature) and biotic (competition and pollination) selection pressures to elevational adaptation in D. carthusianorum. Our results suggest that elevational adaptation in D. carthusianorum is predominantly driven by the abiotic environment. The model reproduced the qualitative differences between the elevational ecotypes in two phenological (germination and flowering time) and one morphological trait (stalk height), as well as qualitative differences in four performance variables that emerge from G × E interactions (flowering time, number of stalks, rosette area and seed production). Our approach shows how E‐FSP models incorporating physiological, ecological and evolutionary mechanisms can be used in combination with experiments to examine hypotheses about patterns of adaptation observed in the field.

Defining species boundaries within plant groups distributed along wide elevational and geographic gradients may lead to unstable taxonomic delimitations using morphological data only. Within the taxonomically challenging genus Dianthus, through an integrative approach we tested the taxonomic value of D. brachycalyx, a putative species endemic to mountain peaks of the central‐southern Apennines, with respect to the widespread central‐Mediterranean D. virgineus. We measured 30 morphological characters in 452 individuals from 25 populations and obtained 3202 single nucleotide polymorphisms using ddRAD‐seq techniques in 394 individuals from 36 populations. For climatic niche comparison, we built a dataset of 348 occurrence points. By comparing morphometric, genetic, and climatic niche data, we showed that D. brachycalyx cannot be considered a distinct species. Morphometric separation between the two species is detectable, but high‐elevation populations of D. virgineus are similar to D. brachycalyx. Genetic analyses revealed that the genetic structure of populations of D. brachycalyx and D. virgineus is mainly shaped by isolation‐by‐distance, irrespective of their taxonomic attribution. The climatic niches of the two species are overlapping, and the niche differences are just due to different availability of climatic conditions in their ranges. Accordingly, multiple lines of evidence do not support a separation of D. brachycalyx from D. virgineus, and the former should be considered a heterotypic synonym of the latter.

Evaluating the potential for species to adapt to changing climate relies on an appreciation of current patterns of adaptive variation and selection, which might vary in intensity across a species’ niche, affecting our inference of where adaptation might be most important in the future. Here we investigate the genetic basis of adaptation in Lactuca serriola , the wild relative of the common lettuce, growing along a steep precipitation gradient in Israel approaching the species’ arid niche limit, and used candidate loci to inform predictions of its past and future adaptive evolution. Environmental association analyses combined with generalized dissimilarity models revealed 98 candidate genes showing non-linear shifts in allele frequencies across the gradient, with a large proportion under strong directional selection near the dry niche edge. Selection acts on genes with separate suites of biological functions, specifically related to osmotic stress and phenological adjustments at the dry edge, and related to biotic interactions at the niche center. The adaptive genetic composition of populations, as inferred through polygenic risk scores, indicates that intensified selection may be the key determinant of the dry niche edge. However, inference of past and future evolutionary change suggests larger adaptive shifts in the mesic part of the range, which is most affected by climate change. Our study highlights that non-linear spatial variation in selection has implications for predicting past and future responses to climate change.

Populations expanding to new habitats may encounter novel selection regimes which can lead to ecotype formation. In the Alps, elevation corresponds to steep ecological gradients, along which ecotype formation has occurred in many species. The majority of alpine plant species are perennial and little is known about how selection acts across different stages of their life-cycles and how fitness trade-offs shape adaptive processes in perennials. We investigated how selection at opposite ends of elevational gradients has driven ecotype formation in Dianthus sylvestris , a perennial herb that expanded its ecological niche to low elevation habitats after the Last Glacial Maximum. Through a multi-year reciprocal transplant experiment including parental populations and recombinant crosses we assessed fitness under natural conditions and dissect how adaptation is mediated by different fitness components with inherent trade-offs, and pinpoint the contribution of growth and reproductive traits to this process. We show that the evolution of local adaptation proceeded by selection acting primarily through reproduction and survival at low and high elevation, respectively. At low elevation the primary contribution to adaptation was third year reproduction, concomitant with a left skewed age distribution. At high elevation the contribution to adaptation and the age distribution were more dispersed across the life cycle. We found that large, early flowering plants have a consistent fitness advantage. This was mediated by direct selection favoring large size through reproductive output at low elevation, and early flowering through the probability to produce seeds at high elevation. Our results indicate that the selection regime imposed by the warm low elevation habitat led to the evolution of an ecotype exhibiting a life-history strategy characterized by high investment in rapid growth and early reproduction. In contrast, the high elevation strategy favors high investment in self-maintenance. Our results suggest that weakening of a key fitness trade-off associated with resource allocation contributed to the evolution of distinct ecotypes in this perennial plant species.

Summary: Spatially divergent natural selection drives adaptation to contrasting environments and the evolution of ecotypes. Understanding this process in perennial plants is challenging because natural selection acts on multiple life history traits linked by fitness trade-offs. In a multi-year reciprocal transplant experiment of high and low elevation populations of the alpine carnation Dianthus carthusianorum in the Central Alps, we tested how different stages of the life cycle contribute to adaptation. Moreover, we used matrix population models to infer the specific contributions of individual life stages to fitness, coupled with trade-off analyses. We found genotype x environment interactions consistent with elevational adaptation both in single fitness components linked to reproduction and survival, and in integrative fitness estimates. Adaptation at low elevation is driven by early reproduction, in contrast to an opposite strategy at high elevation. Adaptive life-history differences between populations originating from low and high elevations are mediated by environmental effects on plant growth and trade-offs between reproduction and survival. Our work reveals elevational ecotypes of the perennial alpine plant D. carthusianorum that express alternative life history strategies in response to climatic differences shaping resource allocation.