Transgenerational plasticity to drought: contrasting patterns of non-genetic inheritance in two semi-arid Mediterranean shrubs.

BACKGROUND AND AIMS: Intra- and transgenerational plasticity may provide substantial phenotypic variation to cope with environmental change. Since assessing the unique contribution of the maternal environment to the offspring phenotype is challenging in perennial, outcrossing plants, little is known about the evolutionary and ecological implications of transgenerational plasticity and its persistence over the life cycle in these species. We evaluated how intra- and transgenerational plasticity interplay to shape the adaptive responses to drought in two perennial Mediterranean shrubs. METHODS: We used a novel common garden approach that reduced within-family genetic variation in both the maternal and offspring generations by growing the same maternal individual in two contrasting watering environments, well-watered and drought, in consecutive years. We then assessed phenotypic differences at the reproductive stage between offspring reciprocally grown in the same environments. KEY RESULTS: Maternal drought had an effect on offspring performance only in Helianthemum squamatum. Offspring of drought-stressed plants showed more inflorescences, less sclerophyllous leaves and higher growth rates in both watering conditions, and heavier seeds under drought, than offspring of well-watered maternal plants. Maternal drought also induced similar plasticity patterns across maternal families, showing a general increase in seed mass in response to offspring drought, a pattern not observed in the offspring of well-watered plants. In contrast, both species expressed immediate adaptive plasticity, and the magnitude of intragenerational plasticity was larger than the transgenerational plastic responses. CONCLUSIONS: Our results highlight that adaptive effects associated with maternal drought can persist beyond the seedling stage and provide evidence of species-level variation in the expression of transgenerational plasticity. Such differences between co-occurring Mediterranean species in the prevalence of this form of non-genetic inheritance may result in differential vulnerability to climate change.

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.

Phenotypic integration does not constrain phenotypic plasticity: differential plasticity of traits is associated to their integration across environments.

Understanding constraints to phenotypic plasticity is key given its role on the response of organisms to environmental change. It has been suggested that phenotypic integration, the structure of trait covariation, could limit trait plasticity. However, the relationship between plasticity and integration is far from resolved. Using a database of functional plasticity to drought of a Mediterranean shrub that included 20 ecophysiological traits, we assessed environmentally-induced changes in phenotypic integration and whether integration constrained the expression of plasticity, accounting for the within-environment phenotypic variation of traits. Furthermore, we provide the first test of the association between differential trait plasticity and trait integration across an optimum and a stressful environment. Phenotypic plasticity was positively associated with phenotypic integration in both environments, but this relationship was lost when phenotypic variation was considered. The similarity in the plastic response of two traits predicted their integration across environments, with integrated traits having more similar plasticity. Such variation in the plasticity of traits partly explained the lower phenotypic integration found in the stressful environment. We found no evidence that integration may constitute an internal constraint to plasticity. Rather, we present the first empirical demonstration that differences in plastic responses may involve a major reorganization of the relationships among traits, and challenge the notion that stress generally induces a tighter phenotype.

Phylogeography of a gypsum endemic plant across its entire distribution range in the western Mediterranean.

PREMISE: Gypsum soils in the Mediterranean Basin house large numbers of edaphic specialists that are adapted to stressful environments. The evolutionary history and standing genetic variation of these taxa have been influenced by the geological and paleoclimatic complexity of this area and the long-standing effect of human activities. However, little is known about the origin of Mediterranean gypsophiles and the factors affecting their genetic diversity and population structure. METHODS: Using phylogenetic and phylogeographic approaches based on microsatellites and sequence data from nuclear and chloroplast regions, we evaluated the divergence time, genetic diversity, and population structure of 27 different populations of the widespread Iberian gypsophile Lepidium subulatum throughout its entire geographic range. RESULTS: Lepidium subulatum diverged from its nearest relatives ~3 million years ago, and ITS and psbA/matK trees supported the monophyly of the species. These results suggest that both geological and climatic changes in the region around the Plio-Pleistocene promoted its origin, compared to other evolutionary processes. We found high genetic diversity in both nuclear and chloroplast markers, but a greater population structure in the chloroplast data. These results suggest that while seed dispersal is limited, pollen flow may be favored by the presence of numerous habitat patches that enhance the movement of pollinators. CONCLUSIONS: Despite being an edaphic endemic, L. subulatum possesses high genetic diversity probably related to its relatively old age and high population sizes across its range. Our study highlights the value of using different markers to fully understand the phylogeographic history of plant species.

High differentiation in functional traits but similar phenotypic plasticity in populations of a soil specialist along a climatic gradient.

BACKGROUND AND AIMS: Plants experiencing contrasting environmental conditions may accommodate such heterogeneity by expressing phenotypic plasticity, evolving local adaptation or a combination of both. We investigated patterns of genetic differentiation and plasticity in response to drought in populations of the gypsum specialist Lepidium subulatum. METHODS: We created an outdoor common garden with rain exclusion structures using 60 maternal progenies from four distinct populations that substantially differ in climatic conditions. We characterized fitness, life history and functional plasticity in response to two contrasting treatments that realistically reflect soil moisture variation in gypsum habitats. We also assessed neutral genetic variation and population structure using microsatellite markers. KEY RESULTS: In response to water stress, plants from all populations flowered earlier, increased allocation to root tissues and advanced leaf senescence, consistent with a drought escape strategy. Remarkably, these probably adaptive responses were common to all populations, as shown by the lack of population × environment interaction for almost all functional traits. This generally common pattern of response was consistent with substantial neutral genetic variation and large differences in population trait means. However, such population-level trait variation was not related to climatic conditions at the sites of origin. CONCLUSIONS: Our results show that, rather than ecotypes specialized to local climatic conditions, these populations are composed of highly plastic, general-purpose genotypes in relation to climatic heterogeneity. The strikingly similar patterns of plasticity among populations, despite substantial site of origin differences in climate, suggest past selection on a common norm of reaction due to similarly high levels of variation within sites. It is thus likely that plasticity will have a prevalent role in the response of this soil specialist to further environmental change.