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.
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.
The EICA‐hypothesis predicts that invading plants adapt to their novel environment by evolving increased performance and reduced resistance in response to the release from natural enemies, and assumes a resource allocation tradeoff among both trait groups as mechanistic basis of this evolutionary change. Using the plant Silene latifolia as a study system, we tested these predictions by investigating whether 1) invasive populations evolved lower resistance and higher performance, 2) this evolutionary change is indeed adaptive, and 3) there is a negative genetic correlation between performance and resistance (i.e. a tradeoff) in native and introduced individuals. Moreover, we sampled eight native and eight invasive populations and determined their population co‐ancestry based on neutral SSR‐markers. We performed controlled crossings to produce five sib‐groups per population and exposed them to increased and reduced levels of enemy attack in a full‐factorial experiment to estimate performance and resistance. With these data, we performed trait‐by‐trait comparisons between ranges with ‘animal models’ that account for population co‐ancestry to quantify the amount of variance in traits explained by non‐adaptive versus adaptive evolution. Moreover, we tested for genetic correlations among performance and resistance traits within sib‐groups. We found significant reductions in resistance and increases in performance in invasive versus native populations, which could largely be attributed to adaptive evolution. While we detected a non‐significant trend towards negative genetic performance × resistance correlations in native populations, invasive populations exhibited both significant and non‐significant positive correlations. In summary, these results do not support a shift of performance and resistance trait values along a tradeoff line in response to enemy release, as predicted by EICA. They rather suggest that the independent evolution of both traits is not constrained by a tradeoff, and that various selective agents (including resource availability) interact in shaping both traits and in weakening negative genetic correlations in the invaded habitat.
Understanding the dynamics of pest insect populations in relation to the presence of non‐crop habitats and infestation levels of adjacent crops is essential to develop sustainable pest management strategies. The invasive pest species Drosophila suzukii (Diptera: Drosophilidae) is able to utilize a broad range of host plants. In viticulture, scientific risk assessment for D. suzukii has only recently started and studies assessing the effects of field margins containing wild host plants on D. suzukii population dynamics and on infestation risks in adjacent vineyards are lacking. Thus, in a one‐year field study, the role of different field margins on fly abundance and crop infestation in adjacent vineyards of Vitis vinifera, variety “Pinot Noir,” were investigated. Different monitoring methods were conducted to assess fly distribution, sex ratio and grape infestation in 14 vineyards adjacent to field margins containing either blackberry (BB) Rubus spp. or non‐host (NH) plants. Our results show that blackberries strongly enhanced D. suzukii abundance within field margin vegetation all year long, whereas fly abundance in vineyards adjacent to BB margins was just enhanced in some seasonal periods. Moreover, the influence of BB margins was limited by distance. However, high fly numbers in BB field margins did result in zero egg infestation of “Pinot Noir” berries. These results may have important implications for winegrowers to make efficient management decisions: regardless of high abundance of adult D. suzukii, only grape berry monitoring can assess the actual infestation risk and the potential need to take management action.
Inbreeding and herbivory can interactively reduce the performance of flowering plants. Here, we investigated whether the magnitude of plant inbreeding depression increases under herbivory as a result of diminished leaf metabolic responses to herbivory in inbreds, which entails increased herbivore growth and feeding damage. We additionally explored whether genetic differentiation among native and invasive plant populations impacts the magnitude and direction of these inbreeding × herbivory interactions. Inbred and outbred plants from eight European (native) and eight North American (invasive) populations of Silene latifolia were exposed to two consecutive control or herbivory treatments (infestation with larvae of Mamestra brassicae). After the first treatment, leaf metabolic responses to herbivory were assessed with untargeted metabolic fingerprinting using UHPLC‐ESI+‐QTOF‐MS/MS. After the second herbivory treatment, herbivore growth and plant feeding damage were assessed. Moreover, plant performance traits were recorded 4 weeks after the second herbivory treatment. Metabolic fingerprinting revealed that changes in the pool sizes of various metabolic features in response to herbivory were less intense in inbred than outbred plants from native and invasive populations. While herbivore growth and feeding damage were largely unaffected by plant breeding status in invasive populations, herbivores consumed more biomass from, but showed reduced growth on, inbred than outbred native plants. The magnitude of inbreeding depression in plant performance traits was not affected by herbivory. Synthesis. Our findings suggest that inbreeding compromises herbivory‐induced metabolic defences in S. latifolia, and simultaneously reduces the nutritional quality of plants. The magnitude and direction of these inbreeding effects were shaped by genetic differentiation among native and invasive plants. These range‐specific responses provide novel insights into the role of inbreeding x herbivory interactions in invasion success.
Habitat fragmentation and small population size can lead to genetic erosion in threatened plant populations. Classical theory implies that dioecy can counteract genetic erosion as it decreases the magnitude of inbreeding and genetic drift due to obligate outcrossing. However, in small populations, sex ratios may be strongly male- or female-biased, leading to substantial reductions in effective population size. This may theoretically result in a unimodal relationship between sex ratios and genetic diversity; yet, empirical studies on this relationship are scarce. Using AFLP markers, we studied genetic diversity, structure and differentiation in 14 highly fragmented Antennaria dioica populations from the Central European lowlands. Our analyses focused on the relationship between sex ratio, population size and genetic diversity. Although most populations were small (mean: 35.5 patches), genetic diversity was moderately high. We found evidence for isolation-by-distance, but overall differentiation of the populations was rather weak. Females dominated 11 populations, which overall resulted in a slightly female-biased sex ratio (61.5%). There was no significant relationship between population size and genetic diversity. The proportion of females was not unimodally but positively linearly related to genetic diversity. The high genetic diversity and low genetic differentiation suggest that A. dioica has been widely distributed in the Central European lowlands in the past, while fragmentation occurred only in the last decades. Sex ratio has more immediate consequences on genetic diversity than population size. An increasing proportion of females can increase genetic diversity in dioecious plants, probably due to a higher amount of sexual reproduction.
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.
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