From common gardens to candidate genes: exploring local adaptation to climate in red spruce.

Local adaptation to climate is common in plant species and has been studied in a range of contexts, from improving crop yields to predicting population maladaptation to future conditions. The genomic era has brought new tools to study this process, which was historically explored through common garden experiments. In this study, we combine genomic methods and common gardens to investigate local adaptation in red spruce and identify environmental gradients and loci involved in climate adaptation. We first use climate transfer functions to estimate the impact of climate change on seedling performance in three common gardens. We then explore the use of multivariate gene-environment association methods to identify genes underlying climate adaptation, with particular attention to the implications of conducting genome scans with and without correction for neutral population structure. This integrative approach uncovered phenotypic evidence of local adaptation to climate and identified a set of putatively adaptive genes, some of which are involved in three main adaptive pathways found in other temperate and boreal coniferous species: drought tolerance, cold hardiness, and phenology. These putatively adaptive genes segregated into two 'modules' associated with different environmental gradients. This study nicely exemplifies the multivariate dimension of adaptation to climate in trees.

Pleistocene climatic oscillations rather than recent human disturbance influence genetic diversity in one of the world's highest treeline species.

PREMISE OF THE STUDY: Biological responses to climatic change usually leave imprints on the genetic diversity and structure of plants. Information on the current genetic diversity and structure of dominant tree species has facilitated our general understanding of phylogeographical patterns. METHODS: Using amplified fragment length polymorphism (AFLPs), we compared genetic diversity and structure of 384 adults of P. tarapacana with those of 384 seedlings across 32 forest sites spanning a latitudinal gradient of 600 km occurring between 4100 m and 5000 m a.s.l. in Polylepis tarapacana (Rosaceae), one of the world's highest treeline species endemic to the central Andes. KEY RESULTS: Moderate to high levels of genetic diversity and low genetic differentiation were detected in both adults and seedlings, with levels of genetic diversity and differentiation being almost identical. Four slightly genetically divergent clusters were identified that accorded to differing geographical regions. Genetic diversity decreased from south to north and with increasing precipitation for adults and seedlings, but there was no relationship to elevation. CONCLUSIONS: Our study shows that, unlike the case for other Andean treeline species, recent human activities have not affected the genetic structure of P. tarapacana, possibly because its inhospitable habitat is unsuitable for agriculture. The current genetic pattern of P. tarapacana points to a historically more widespread distribution at lower altitudes, which allowed considerable gene flow possibly during the glacial periods of the Pleistocene epoch, and also suggests that the northern Argentinean Andes may have served as a refugium for historical populations.

Genotypic variation and plasticity in climate-adaptive traits after range expansion and fragmentation of red spruce (Picea rubens Sarg.).

Shifting range limits are predicted for many species as the climate warms. However, the rapid pace of climate change will challenge the natural dispersal capacity of long-lived, sessile organisms such as forest trees. Adaptive responses of populations will, therefore, depend on levels of genetic variation and plasticity for climate-responsive traits, which likely vary across the range due to expansion history and current patterns of selection. Here, we study levels of genetic and plastic variation for phenology and growth traits in populations of red spruce (Picea rubens), from the range core to the highly fragmented trailing edge. We measured more than 5000 offspring sampled from three genetically distinct regions (core, margin and edge) grown in three common gardens replicated along a latitudinal gradient. Genetic variation in phenology and growth showed low to moderate heritability and differentiation among regions, suggesting some potential to respond to selection. Phenology traits were highly plastic, but this plasticity was generally neutral or maladaptive in the effect on growth, revealing a potential liability under warmer climates. These results suggest future climate adaptation will depend on the regional availability of genetic variation in red spruce and provide a resource for the design and management of assisted gene flow. This article is part of the theme issue 'Species' ranges in the face of changing environments (Part II)'.

Differentiation of reproductive and competitive ability in the invaded range of Senecio inaequidens: the role of genetic Allee effects, adaptive and nonadaptive evolution.

Genetic differentiation in the competitive and reproductive ability of invading populations can result from genetic Allee effects or r/K selection at the local or range-wide scale. However, the neutral relatedness of populations may either mask or falsely suggest adaptation and genetic Allee effects. In a common-garden experiment, we investigated the competitive and reproductive ability of invasive Senecio inaequidens populations that vary in neutral genetic diversity, population age and field vegetation cover. To account for population relatedness, we analysed the experimental results with 'animal models' adopted from quantitative genetics. Consistent with adaptive r/K differentiation at local scales, we found that genotypes from low-competition environments invest more in reproduction and are more sensitive to competition. By contrast, apparent effects of large-scale r/K differentiation and apparent genetic Allee effects can largely be explained by neutral population relatedness. Invading populations should not be treated as homogeneous groups, as they may adapt quickly to small-scale environmental variation in the invaded range. Furthermore, neutral population differentiation may strongly influence invasion dynamics and should be accounted for in analyses of common-garden experiments.

The making of a rapid plant invader: genetic diversity and differentiation in the native and invaded range of Senecio inaequidens.

To become invasive, exotic species have to succeed in the consecutive phases of introduction, naturalization, and invasion. Each of these phases leaves traces in genetic structure, which may affect the species' success in subsequent phases. We examined this interplay of genetic structure and invasion dynamics in the South African Ragwort (Senecio inaequidens), one of Europe's fastest plant invaders. We used AFLP and microsatellite markers to analyze 19 native African and 32 invasive European populations. In combination with historic data, we distinguished invasion routes and traced them back to the native source areas. This revealed that different introduction sites had markedly different success in the three invasion phases. Notably, an observed lag-phase in Northern Germany was evidently not terminated by factors increasing the invasiveness of the resident population but by invasive spread from another introduction centre. The lineage invading Central Europe was introduced to sites in which winters are more benign than in the native source region. Subsequently, this lineage spread into areas in which winter temperatures match the native climate more closely. Genetic diversity clearly increases with population age in Europe and less clearly decreases with spread rate up to population establishment. This indicates that gene flow along well-connected invasion routes counteracted losses of genetic diversity during rapid spread. In summary, this study suggests that multiple introductions, environmental preadaptation and high gene flow along invasion routes contributed to the success of this rapid invader. More generally, it demonstrates the benefit of combining genetic, historical, and climatic data for understanding biological invasions.

Associations between genomic ancestry, genome size and capitula morphology in the invasive meadow knapweed hybrid complex (Centaurea × moncktonii) in eastern North America.

Plant invasions are prime opportunities for studying hybridization and the nature of species boundaries, but hybrids also complicate the taxonomic treatment and management of introduced taxa. In this study, we use population genomics to estimate the extent of genomic admixture and test for its association with morphology and genome size in a hybrid complex of knapweeds invasive to North America: meadow knapweed (Centaurea × moncktonii) and its parental species (C. jacea and C. nigra). We sampled 20 populations from New York and Vermont, USA, and used genotyping by sequencing to identify single nucleotide polymorphisms in order to estimate genome-wide ancestry and classify individuals into hybrid genotype classes. We then tested for association between degree of genomic introgression and variation in a subset of traits diagnostic for the parental taxa, namely capitula morphology and monoploid genome size. Genomic clustering revealed two clearly defined lineages, as well as many admixed individuals forming a continuous gradation of introgression. Individual assignments to hybrid genotype classes revealed many advanced generation intercrosses and backcrosses, suggesting introgression has been extensive and unimpeded by strong reproductive barriers between taxa. Variation in capitula traits between the two unadmixed, presumed parental, lineages exhibited continuous, and in some cases transgressive, segregation among introgressed hybrids. Genome size was also divergent between lineages, although advanced generation hybrids had smaller genomes relative to additive expectations. Our study demonstrates deep introgression between the porous genomes of a hybrid invasive species complex. In addition to strong associations among genomic ancestry, genome size and morphology, hybrids expressed more extreme phenotypic values for capitula traits and genome size, indicating transgressive segregation, as well as a bias towards smaller genomes, possibly due to genomic downsizing. Future studies will apply these results to experimentally test how introgression, transgressive segregation and genome size reduction interact to confer invasiveness.

Release from natural enemies mitigates inbreeding depression in native and invasive Silene latifolia populations.

Inbreeding and enemy infestation are common in plants and can synergistically reduce their performance. This inbreeding ×environment (I × E) interaction may be of particular importance for the success of plant invasions if introduced populations experience a release from attack by natural enemies relative to their native conspecifics. Here, we investigate whether inbreeding affects plant infestation damage, whether inbreeding depression in growth and reproduction is mitigated by enemy release, and whether this effect is more pronounced in invasive than native plant populations. We used the invader Silene latifolia and its natural enemies as a study system. We performed two generations of experimental out- and inbreeding within eight native (European) and eight invasive (North American) populations under controlled conditions using field-collected seeds. Subsequently, we exposed the offspring to an enemy exclusion and inclusion treatment in a common garden in the species' native range to assess the interactive effects of population origin (range), breeding treatment, and enemy treatment on infestation damage, growth, and reproduction. Inbreeding increased flower and leaf infestation damage in plants from both ranges, but had opposing effects on fruit damage in native versus invasive plants. Inbreeding significantly reduced plant fitness; whereby, inbreeding depression in fruit number was higher in enemy inclusions than exclusions. This effect was equally pronounced in populations from both distribution ranges. Moreover, the magnitude of inbreeding depression in fruit number was lower in invasive than native populations. These results support that inbreeding has the potential to reduce plant defenses in S. latifolia, which magnifies inbreeding depression in the presence of enemies. However, future studies are necessary to further explore whether enemy release in the invaded habitat has actually decreased inbreeding depression and thus facilitated the persistence of inbred founder populations and invasion success.

The Genetic Paradox of Invasions revisited: the potential role of inbreeding × environment interactions in invasion success.

Invasive species that successfully establish, persist, and expand within an area of introduction, in spite of demographic bottlenecks that reduce their genetic diversity, represent a paradox. Bottlenecks should inhibit population growth and invasive expansion, as a decrease in genetic diversity should result in inbreeding depression, increased fixation of deleterious mutations by genetic drift (drift load), and reduced evolutionary potential to respond to novel selection pressures. Here, we focus on the problems of inbreeding depression and drift load in introduced populations as key components of the Genetic Paradox of Invasions (GPI). We briefly review published explanations for the GPI, which are based on various mechanisms (invasion history events, reproductive traits, genetic characteristics) that mediate the avoidance of inbreeding depression and drift load. We find that there is still a substantial lack of explanation and empirical evidence for explaining the GPI for strongly bottlenecked invasions, or for during critical invasion phases (e.g. initial colonization, leading edges of range expansion) where strong genetic depletion, inbreeding depression and drift load occurs. Accordingly, we suggest that discussion of the GPI should be revived to find additional mechanisms applicable to explaining invasion success for such species and invasion phases. Based on a synthesis of the literature on the population genetics of invaders and the ecology of invaded habitats, we propose that inbreeding × environment (I × E) interactions are one such mechanism that may have strong explanatory power to address the GPI. Specifically, we suggest that a temporary or permanent release from stress in invaded habitats may alleviate the negative effects of genetic depletion on fitness via I × E interactions, and present published empirical evidence supporting this hypothesis. We additionally discuss that I × E interactions can result in rapid evolutionary changes, and may even contribute to adaptation of invaders in the absence of high genetic variation. With a view to encouraging further empirical research, we propose an experimental approach to investigate the occurrence of I × E interactions in ongoing invasions. Revived research on the GPI should provide new fundamental insights into eco-evolutionary invasion biology, and more generally into the evolutionary consequences of the interactions between inbreeding and environment.

Knowledge and valuation of Andean agroforestry species: the role of sex, age, and migration among members of a rural community in Bolivia.

BACKGROUND: Agroforestry is a sustainable land use method with a long tradition in the Bolivian Andes. A better understanding of people's knowledge and valuation of woody species can help to adjust actor-oriented agroforestry systems. In this case study, carried out in a peasant community of the Bolivian Andes, we aimed at calculating the cultural importance of selected agroforestry species, and at analysing the intracultural variation in the cultural importance and knowledge of plants according to peasants' sex, age, and migration. METHODS: Data collection was based on semi-structured interviews and freelisting exercises. Two ethnobotanical indices (Composite Salience, Cultural Importance) were used for calculating the cultural importance of plants. Intracultural variation in the cultural importance and knowledge of plants was detected by using linear and generalised linear (mixed) models. RESULTS AND DISCUSSION: The culturally most important woody species were mainly trees and exotic species (e.g.Schinus molle, Prosopis laevigata, Eucalyptus globulus). We found that knowledge and valuation of plants increased with age but that they were lower for migrants; sex, by contrast, played a minor role. The age effects possibly result from decreasing ecological apparency of valuable native species, and their substitution by exotic marketable trees,loss of traditional plant uses or the use of other materials (e.g. plastic) instead of wood. Decreasing dedication to traditional farming may have led to successive abandonment of traditional tool uses, and the overall transformation of woody plant use is possibly related to diminishing medicinal knowledge. CONCLUSIONS: Age and migration affect how people value woody species and what they know about their uses.For this reason, we recommend paying particular attention to the potential of native species, which could open promising perspectives especially for the young migrating peasant generation and draw their interest in agroforestry. These native species should be ecologically sound and selected on their potential to provide subsistence and promising commercial uses. In addition to offering socio-economic and environmental services,agroforestry initiatives using native trees and shrubs can play a crucial role in recovering elements of the lost ancient landscape that still forms part of local people's collective identity.