Facilitated Adaptation as A Conservation Tool in the Present Climate Change Context: A Methodological Guide.

Climate change poses a novel threat to biodiversity that urgently requires the development of adequate conservation strategies. Living organisms respond to environmental change by migrating to locations where their ecological niche is preserved or by adapting to the new environment. While the first response has been used to develop, discuss and implement the strategy of assisted migration, facilitated adaptation is only beginning to be considered as a potential approach. Here, we present a review of the conceptual framework for facilitated adaptation, integrating advances and methodologies from different disciplines. Briefly, facilitated adaptation involves a population reinforcement that introduces beneficial alleles to enable the evolutionary adaptation of a focal population to pressing environmental conditions. To this purpose, we propose two methodological approaches. The first one (called pre-existing adaptation approach) is based on using pre-adapted genotypes existing in the focal population, in other populations, or even in closely related species. The second approach (called de novo adaptation approach) aims to generate new pre-adapted genotypes from the diversity present in the species through artificial selection. For each approach, we present a stage-by-stage procedure, with some techniques that can be used for its implementation. The associated risks and difficulties of each approach are also discussed.

Population origin determines the adaptive potential for the advancement of flowering onset in Lupinus angustifolius L. (Fabaceae).

In the present framework of global warming, it is unclear whether evolutionary adaptation can happen quick enough to preserve the persistence of many species. Specifically, we lack knowledge about the adaptive potential of the different populations in relation to the various constraints that may hamper particular adaptations. There is evidence indicating that early flowering often provides an adaptive advantage to plants in temperate zones in response to global warming. Thus, the objective of this study was to assess the adaptive potential for advancing flowering onset in Lupinus angustifolius L. (Fabaceae). Seeds from four populations from two contrasting latitudes in Spain were collected and sown in a common garden environment. Selecting the 25% of the individuals that flowered earlier in the first generation, over three generations, three different early flowering selection lines were established, involving both self-crosses and outcrosses. All artificial selection lines advanced their flowering significantly with respect to the control line in the northernmost populations, but not in the southern ones. Selection lines obtained from outcrossing had a greater advancement in flowering than those from self-crossing. No differences were found in the number or weight of the seeds produced between control and artificial selection lines, probably because plants in the common garden were drip irrigated. These results suggest that northern populations may have a greater adaptive potential and that southern populations may be more vulnerable in the context of climate warming. However, earlier flowering was also associated with changes in other traits (height, biomass, shoot growth, specific leaflet area, and leaflet dry matter content), and the effects of these changes varied greatly depending on the latitude of the population and selection line. Assessments of the ability of populations to cope with climate change through this and other approaches are essential to manage species and populations in a more efficient way.

Climate change conditions the selection of rust-resistant candidate wild lentil populations for in situ conservation.

Crop Wild Relatives (CWR) are a valuable source of genetic diversity that can be transferred to commercial crops, so their conservation will become a priority in the face of climate change. Bizarrely, in situ conserved CWR populations and the traits one might wish to preserve in them are themselves vulnerable to climate change. In this study, we used a quantitative machine learning predictive approach to project the resistance of CWR populations of lentils to a common disease, lentil rust, caused by fungus Uromyces viciae-fabae. Resistance is measured through a proxy quantitative value, DSr (Disease Severity relative), quite complex and expensive to get. Therefore, machine learning is a convenient tool to predict this magnitude using a well-curated georeferenced calibration set. Previous works have provided a binary outcome (resistant vs. non-resistant), but that approach is not fine enough to answer three practical questions: which variables are key to predict rust resistance, which CWR populations are resistant to rust under current environmental conditions, and which of them are likely to keep this trait under different climate change scenarios. We first predict rust resistance in present time for crop wild relatives that grow up inside protected areas. Then, we use the same models under future climate IPCC (Intergovernmental Panel on Climate Change) scenarios to predict future DSr values. Populations that are rust-resistant by now and under future conditions are optimal candidates for further evaluation and in situ conservation of this valuable trait. We have found that rust-resistance variation as a result of climate change is not uniform across the geographic scope of the study (the Mediterranean basin), and that candidate populations share some interesting common environmental conditions.

Effects of parental drought on offspring fitness vary among populations of a crop wild relative.

Transgenerational plasticity is a form of non-genetic inheritance that can reduce or enhance offspring fitness depending on parental stress. Yet, the adaptive value of such parental environmental effects and whether their expression varies among populations remain largely unknown. We used self-fertilized lines from climatically distinct populations of the crop wild relative Lupinus angustifolius. In the parental generation, full-siblings were grown in two contrasting watering environments. Then, to robustly separate the within-generation and transgenerational response to drought, we reciprocally assigned the offspring of parents to the same experimental treatments. We measured key functional traits and assessed lifetime reproductive fitness. Offspring of drought-stressed parents produced less reproductive biomass, but a similar number of lighter seeds, in dry soil compared to offspring of genetically identical, well-watered parents, an effect not mediated by differences in seed provisioning. Importantly, while the offspring of parents grown in the favourable environment responded to drought by slightly increasing individual seed mass, the pattern of plasticity of the offspring of drought-grown parents showed the opposite direction, and the negative effects of parental drought on seed mass were more pronounced in populations from cooler and moist habitats. Overall, our results show that parental effects may override immediate adaptive responses to drought and provide evidence of population-level variation in the expression of transgenerational plasticity.

Searching for Abiotic Tolerant and Biotic Stress Resistant Wild Lentils for Introgression Breeding Through Predictive Characterization.

Crop wild relatives are species related to cultivated plants, whose populations have evolved in natural conditions and confer them valuable adaptive genetic diversity, that can be used in introgression breeding programs. Targeting four wild lentil taxa in Europe, we applied the predictive characterization approach through the filtering method to identify populations potentially tolerant to drought, salinity, and waterlogging. In parallel, the calibration method was applied to select wild populations potentially resistant to lentil rust and broomrape, using, respectively, 351 and 204 accessions evaluated for these diseases. An ecogeographic land characterization map was used to incorporate potential genetic diversity of adaptive value. We identified 13, 1, 21, and 30 populations potentially tolerant to drought, soil salinity, waterlogging, or resistance to rust, respectively. The models targeting broomrape resistance did not adjust well and thus, we were not able to select any population regarding this trait. The systematic use of predictive characterization techniques may boost the efficiency of introgression breeding programs by increasing the chances of collecting the most appropriate populations for the desired traits. However, these populations must still be experimentally tested to confirm the predictions.

Habitat Fragmentation Differentially Affects Genetic Variation, Phenotypic Plasticity and Survival in Populations of a Gypsum Endemic.

Habitat fragmentation, i.e., fragment size and isolation, can differentially alter patterns of neutral and quantitative genetic variation, fitness and phenotypic plasticity of plant populations, but their effects have rarely been tested simultaneously. We assessed the combined effects of size and connectivity on these aspects of genetic and phenotypic variation in populations of Centaurea hyssopifolia, a narrow endemic gypsophile that previously showed performance differences associated with fragmentation. We grew 111 maternal families sampled from 10 populations that differed in their fragment size and connectivity in a common garden, and characterized quantitative genetic variation, phenotypic plasticity to drought for key functional traits, and plant survival, as a measure of population fitness. We also assessed neutral genetic variation within and among populations using eight microsatellite markers. Although C. hyssopifolia is a narrow endemic gypsophile, we found substantial neutral genetic variation and quantitative variation for key functional traits. The partition of genetic variance indicated that a higher proportion of variation was found within populations, which is also consistent with low population differentiation in molecular markers, functional traits and their plasticity. This, combined with the generally small effect of habitat fragmentation suggests that gene flow among populations is not restricted, despite large differences in fragment size and isolation. Importantly, population's similarities in genetic variation and plasticity did not reflect the lower survival observed in isolated populations. Overall, our results indicate that, although the species consists of genetically variable populations able to express functional plasticity, such aspects of adaptive potential may not always reflect populations' survival. Given the differential effects of habitat connectivity on functional traits, genetic variation and fitness, our study highlights the need to shift the focus of fragmentation studies to the mechanisms that regulate connectivity effects, and call for caution on the use of genetic variation and plasticity to forecast population performance.