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.
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.
Summary• 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.
Summary As a consequence of founder effects, inbreeding can hamper colonization success: First, in species with self‐incompatibility controlled by an S‐locus, inbreeding may decrease cross‐compatibility, mainly due to the sharing of identical S‐alleles between closely related mating partners. Secondly, inbreeding can reduce fitness of inbred relative to outbred offspring (i.e. inbreeding depression). Polyploids often show reduced inbreeding depression compared to diploids, which may contribute to the overrepresentation of polyploids among invasive species. This is the first study that tests how the effects of inbreeding differ between geocytotypes (i.e. ploidy levels within a given range). Our model organism, Centaurea stoebe, is strictly self‐incompatible and comprises three geocytotypes: diploids are more frequent than tetraploids in the native range, while only tetraploids occur in the invasive range. We conducted a breeding experiment (sib‐mating vs. outcrossing) with 14 native diploid, 13 native tetraploid and 15 invasive tetraploid populations. We recorded cross‐compatibility and estimated a cumulative index for offspring fitness. Since frequent inbreeding can result in purging of genetic load responsible for inbreeding depression, our analyses included a metric for within‐population relatedness, based on eight microsatellite markers, to assess the effect of purging. Inbreeding was found to reduce cross‐compatibility, which was similarly pronounced in diploids and tetraploids. It also caused inbreeding depression in cumulative fitness, which was significant in diploids but not in tetraploids. No evidence of purging was observed as inbred fitness was not affected by within‐population relatedness. Synthesis. Our results provide new insights into the contrasting invasion success of the cytotypes of C. stoebe. As the effects of cross‐compatibility and purging were comparable between cytotypes, both processes can be ruled out to affect the colonization success of diploids versus tetraploids. Our findings are consistent with the hypothesis that polyploidy increases the masking of recessive mutations, which maintains high fitness in inbred tetraploids and may thus facilitate colonization of new ranges. We highlight that reduced inbreeding depression may add to previously acknowledged advantages of polyploids in range expansions, a mechanism that may hitherto have been underestimated due to a lack of data on variation in inbreeding depression across geocytotypes.
Comparing genetic diversity, genetic differentiation, and performance between native and nonnative populations has advanced our knowledge of contemporary evolution and its ecological consequences. However, such between‐range comparisons can be complicated by high among‐population variation within native and nonnative ranges. For example, native vs. nonnative comparisons between small and non‐representative subsets of populations for species with very large distributions have the potential to mislead because they may not sufficiently account for within‐range adaptation to climatic conditions, and demographic history that may lead to non‐adaptive evolution. We used the cosmopolitan weed Conyza canadensis to study the interplay of adaptive and demographic processes across, to our knowledge, the broadest climatic gradient yet investigated in this context. To examine the distribution of genetic diversity, we genotyped 26 native and 26 nonnative populations at 12 microsatellite loci. Furthermore, we recorded performance traits for 12 native and 13 nonnative populations in the field and in the common garden. To analyze how performance was related to range and/or climate, we fit pedigree mixed‐effects models. These models weighed the population random effect for co‐ancestry to account for the influence of demographic history on phenotypic among‐population differentiation. Genetic diversity was very low, selfing rates were very high, and both were comparable between native and nonnative ranges. Nonnative populations out‐performed native populations in the field. However, our most salient result was that both neutral genetic differentiation and common garden performance were far more correlated with the climatic conditions from which populations originated than native vs. nonnative range affiliation. Including co‐ancestry of our populations in our models greatly increased explained variance and our ability to detect significant main effects for among‐population variation in performance. High propagule pressure and high selfing rates, in concert with the ability to adapt rapidly to climatic gradients, may have facilitated the global success of this weed. Neither native nor nonnative populations were homogeneous groups but responded comparably to similar environments in each range. We suggest that studies of contemporary evolution should consider widely distributed and genotyped populations to disentangle native vs. nonnative range effects from varying adaptive processes within ranges and from potentially confounding effects of demographic history.
Summary 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.
BackgroundAgroforestry 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.MethodsData 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 discussionThe 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.ConclusionsAge 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.
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