Jacqui A. Shykoff

High genetic diversity in French invasive populations of common ragweed, Ambrosia artemisiifolia, as a result of multiple sources of introduction

Ambrosia artemisiifolia is an aggressive North American annual weed, found particularly in sunflower and corn fields. Besides its economic impact on crop yield, it represents a major health problem because of its strongly allergenic pollen. Ragweed was imported inadvertently to Europe in the 18th century and has become invasive in several countries, notably in the Rhône Valley of France. It has recently expanded in both the Provence‐Alpes‐Côte‐d’Azur and Bourgogne regions. As first steps towards understanding the causes and mechanisms of ragweed invasion, genetic variability of French and North American populations was analysed using microsatellites. Overall genetic variability was similar in North America and in the Rhône‐Alpes region, but within‐population levels of genetic variability were surprisingly lower in native than in invasive French populations. French populations also exhibited lower among‐population differentiation. A significant pattern of isolation by distance was detected among North American populations but not among French populations. Assignment tests and distribution of rare alleles did not point to a single origin for all French populations, nor for all individuals within populations and private alleles from different North American populations were found in the same French populations. Indeed, within all French populations, individual plants were roughly equally assigned to the different North American populations. Altogether, these results suggest that the French invasive populations include plants from a mixture of sources. Reduced diversity in populations distant from the original area of introduction indicated that ragweed range expansion probably occurred through sequential bottlenecks from the original populations, and not from subsequent new introductions.

LOCAL MALADAPTATION IN THE ANTHER-SMUT FUNGUS MICROBOTRYUM VIOLACEUM TO ITS HOST PLANT SILENE LATIFOLIA: EVIDENCE FROM A CROSS-INOCULATION EXPERIMENT

Conventional wisdom holds that parasites evolve more rapidly than their hosts and are therefore locally adapted, that is, better at exploiting sympatric than allopatric hosts. We studied local adaptation in the insect‐transmitted fungal pathogen Microbotryum violaceum and its host plant Silene latifolia. Infection success was tested in sympatric (local) and allopatric (foreign) combinations of pathogen and host from 14 natural populations from a metapopulation. Seedlings from up to 10 seed families from each population were exposed to sporidial suspensions from each of four fungal strains derived from the same population, from a near‐by population (< 10 km distance), and from two populations at an intermediate (< 30 km) and remote (< 170 km) distance, respectively. We obtained significant pathogen X plant interactions in infection success (proportion of diseased plants) at both fungal population and strain level. There was an overall pattern of local maladaptation of this pathogen: average fungal infection success was significantly lower on sympatric hosts (mean proportion of diseased plants = 0.32 ± 0.03 SE) than on allopatric hosts (0.40 ± 0.02). Five of the 14 fungal populations showed no strong reduction in infection success on sympatric hosts, and three even tended to perform better on sympatric hosts. This pattern is consistent with models of time‐lagged cycles predicting patterns of local adaptation in host‐parasite systems to emerge only on average. Several factors may restrict the evolutionary potential of this pathogen relative to that of its host. First, a predominantly selfing breeding system may limit its ability to generate new virulence types by sexual recombination, whereas the obligately outcrossing host 5. latifolia may profit from rearrangement of resistance alleles by random mating. Second, populations often harbor only a few infected individuals, so virulence variation may be further reduced by drift. Third, migration rates among host plant populations are much higher than among pathogen populations, possibly because pollinators prefer healthy over diseased plants. Migration among partly isolated populations may therefore introduce novel host plant resistance variants more often than novel parasite virulence variants. That migration contributes to the coevolutionary dynamics in this system is supported by the geographic pattern of infectivity. Infection success increased over the first 10–km range of host‐pathogen population distances, which is likely the natural range of gene exchange.

Effects of male sterility on reproductive traits in gynodioecious plants: a meta-analysis

Female fecundity advantage in gynodioecious plants is required for the spread and maintenance of this reproductive system. However, not all reproductive characters show female advantage in all species. We used a meta-analysis to summarise differences between females and hermaphrodites reported from the literature for several reproductive traits. Further we tested three hypotheses, (1) that female plants of species with many ovules produce more seeds per fruit while those with few ovules produce heavier seeds, (2) that females are more pollen limited than hermaphrodites, and (3) that floral sexual size dimorphism is more pronounced in species with few ovules, either because female reproductive success is less limited by pollen availability in such species or because flowers with few ovules require a smaller floral structure to protect the carpels. Overall, females compared to hermaphrodites produced more but smaller flowers, had higher fruit set, higher total seed production, and produced heavier seeds that germinated better. Species with many versus few ovules differed in female advantage for flower size dimorphism, flower number, fruit set and total seed production. However seed size, seed set per fruit and seed germination differences between females and hermaphrodites did not differ significantly between species with few and many ovules. We also found no evidence for differential pollen limitation between females and hermaphrodites. Degree of floral sexual size dimorphism differed significantly between species with few and many ovules. Though pistillate flowers were generally smaller than those of hermaphrodites, species with many ovules showed less difference in flower size between the sexes, suggesting either that the protective role of the perianth constrains the evolution of sexual size dimorphism in species with many ovules or that selection for adequate pollination in species with many ovules impedes the reduction in flower size of females.

Pollinator visitation patterns, floral rewards and the probability of transmission of Microbotryum violaceum, a venereal disease of plants

1 We investigated patterns of pollinator visitation to plants of the white campion, Silene alba, and related these to floral nectar rewards in healthy female and male plants and in plants diseased with the anther smut disease Microbotryum violaceum (= Ustilago violacea). 2 Pollinators preferred plants with large floral displays, and also preferred males to females and healthy to diseased plants. Male plants consistently produced nectar with higher sugar concentration, thereby offering higher quality floral rewards than either females or diseased plants. 3 Variation in nectar production was also found among individual plants and different plant families, suggesting that more attractive plants may be predisposed to infection since pollinating insects also serve as vectors for this fungal disease. 4 Such patterns of pollinator preference could affect the dynamics of disease transmission within populations by influencing the probability that insect visitors make transitions between diseased and healthy plants. This vector transmitted disease may therefore modify the course of selection on floral traits by imparting a cost to pollinator attraction.

Silene as a model system in ecology and evolution.

The genus Silene, studied by Darwin, Mendel and other early scientists, is re-emerging as a system for studying interrelated questions in ecology, evolution and developmental biology. These questions include sex chromosome evolution, epigenetic control of sex expression, genomic conflict and speciation. Its well-studied interactions with the pathogen Microbotryum has made Silene a model for the evolution and dynamics of disease in natural systems, and its interactions with herbivores have increased our understanding of multi-trophic ecological processes and the evolution of invasiveness. Molecular tools are now providing new approaches to many of these classical yet unresolved problems, and new progress is being made through combining phylogenetic, genomic and molecular evolutionary studies with ecological and phenotypic data.

Parasites and the advantage of genetic variability within social insect colonies

Genetic variability within colonies of eusocial insects is often higher than expected if kin selection alone explains sociality. Parasites and pathogens have been proposed as selective agents maintaining genetic variability in populations and promoting polyandry in social insects. Using the natural system, bumble bees, Bombus terrestris, and their trypanosome parasites, Crithidia bombi, we find that hosts vary in susceptibility or parasites in infectiousness, and that parasite transmission in social groups correlates with genetic relatedness among hosts. Therefore parasite-mediated negative frequency-dependent selection could play an important role in structuring the genetic composition of social groups by counteracting kin selection for high relatedness.

Cophylogeny of the anther smut fungi and their caryophyllaceous hosts: prevalence of host shifts and importance of delimiting parasite species for inferring cospeciation

BackgroundUsing phylogenetic approaches, the expectation that parallel cladogenesis should occur between parasites and hosts has been validated in some studies, but most others provided evidence for frequent host shifts. Here we examine the evolutionary history of the association between Microbotryum fungi that cause anther smut disease and their Caryophyllaceous hosts. We investigated the congruence between host and parasite phylogenies, inferred cospeciation events and host shifts, and assessed whether geography or plant ecology could have facilitated the putative host shifts identified.For cophylogeny analyses on microorganisms, parasite strains isolated from different host species are generally considered to represent independent evolutionary lineages, often without checking whether some strains actually belong to the same generalist species. Such an approach may mistake intraspecific nodes for speciation events and thus bias the results of cophylogeny analyses if generalist species are found on closely related hosts. A second aim of this study was therefore to evaluate the impact of species delimitation on the inferences of cospeciation.ResultsWe inferred a multiple gene phylogeny of anther smut strains from 21 host plants from several geographic origins, complementing a previous study on the delimitation of fungal species and their host specificities. We also inferred a multi-gene phylogeny of their host plants, and the two phylogenies were compared. A significant level of cospeciation was found when each host species was considered to harbour a specific parasite strain, i.e. when generalist parasite species were not recognized as such. This approach overestimated the frequency of cocladogenesis because individual parasite species capable of infecting multiple host species (i.e. generalists) were found on closely related hosts. When generalist parasite species were appropriately delimited and only a single representative of each species was retained, cospeciation events were not more frequent than expected under a random distribution, and many host shifts were inferred.Current geographic distributions of host species seemed to be of little relevance for understanding the putative historical host shifts, because most fungal species had overlapping geographic ranges. We did detect some ecological similarities, including shared pollinators and habitat types, between host species that were diseased by closely related anther smut species. Overall, genetic similarity underlying the host-parasite interactions appeared to have the most important influence on specialization and host-shifts: generalist multi-host parasite species were found on closely related plant species, and related species in the Microbotryum phylogeny were associated with members of the same host clade.ConclusionWe showed here that Microbotryum species have evolved through frequent host shifts to moderately distant hosts, and we show further that accurate delimitation of parasite species is essential for interpreting cophylogeny studies.

Morphological Developmental Stability in Plants: Patterns and Causes

Minor bilateral or radial asymmetry of leaves or flowers, the frequency of phenodeviants, intraindividual variation in repeated characters, and fractal dimensions of morphology are considered to represent measures of developmental instability since deviations from regularity of the phenotype constitute a measure of the inability to maintain developmental precision during ontogeny. First, we review patterns of fluctuating asymmetry in plants and show that levels of asymmetry are considerably greater than in animals. While petal asymmetry tends to decrease with petal size within species, leaf asymmetry tends to increase with leaf size. Intraspecific correlations of petal asymmetry and leaf asymmetry are weakly positive. Second, a meta‐analysis of the effects of environmental factors hypothesized to increase asymmetry in leaves and flowers, such as radiation, ultraviolet light, excess artificial fertilizer, pollutants, extreme saline conditions, herbivory, and competition, showed intermediate (i.e., explaining 10% of the variance) to large (i.e., explaining 25% of the variance) effects. Third, a meta‐analysis of the effects of genetic factors hypothesized to contribute to increased asymmetry in plants, such as homozygosity, hybridization, mutation, and quantitative genetic differences among individuals, showed variable but usually significant effects, although the number of studies generally was small. Controlled experimental studies of environmental and genetic effects on developmental instability of plants may increase our understanding of the mechanisms causing developmental instability.

Enemy release but no evolutionary loss of defence in a plant invasion: an inter-continental reciprocal transplant experiment

When invading new regions exotic species may escape from some of their natural enemies. Reduced top–down control (“enemy release”) following this escape is often invoked to explain demographic expansion of invasive species and also may alter the selective regime for invasive species: reduced damage can allow resources previously allocated to defence to be reallocated to other functions like growth and reproduction. This reallocation may provide invaders with an “evolution of increased competitive ability” over natives that defend themselves against specialist enemies. We tested for enemy release and the evolution of increased competitive ability in the North American native ragweed (Ambrosia artemisiifolia: Asteraceae), which currently is invading France. We found evidence of enemy release in natural field populations from the invaded and native ranges. Further we carried out a reciprocal transplant experiment, comparing several life history traits of plants from two North American (Ontario and South Carolina) and one French population in four common gardens on both continents. French and Canadian plants had similar flowering phenologies, flowering earlier than plants from further south in the native range. This may suggest that invasive French plants originated from similar latitudes to the Canadian population sampled. As with natural populations, experimental plants suffered far less herbivore damage in France than in Ontario. This difference in herbivory translated into increased growth but not into increased size or vigour. Moreover, we found that native genotypes were as damaged as invading ones in all experimental sites, suggesting no evolutionary loss of defence against herbivores.

Nuclear and Chloroplast Microsatellites Show Multiple Introductions in the Worldwide Invasion History of Common Ragweed, Ambrosia artemisiifolia

Background Ambrosia artemisiifolia is a North American native that has become one of the most problematic invasive plants in Europe and Asia. We studied its worldwide population genetic structure, using both nuclear and chloroplast microsatellite markers and an unprecedented large population sampling. Our goals were (i) to identify the sources of the invasive populations; (ii) to assess whether all invasive populations were founded by multiple introductions, as previously found in France; (iii) to examine how the introductions have affected the amount and structure of genetic variation in Europe; (iv) to document how the colonization of Europe proceeded; (v) to check whether populations exhibit significant heterozygote deficiencies, as previously observed. Principal Findings We found evidence for multiple introductions of A. artemisiifolia, within regions but also within populations in most parts of its invasive range, leading to high levels of diversity. In Europe, introductions probably stem from two different regions of the native area: populations established in Central Europe appear to have originated from eastern North America, and Eastern European populations from more western North America. This may result from differential commercial exchanges between these geographic regions. Our results indicate that the expansion in Europe mostly occurred through long-distance dispersal, explaining the absence of isolation by distance and the weak influence of geography on the genetic structure in this area in contrast to the native range. Last, we detected significant heterozygote deficiencies in most populations. This may be explained by partial selfing, biparental inbreeding and/or a Wahlund effect and further investigation is warranted. Conclusions This insight into the sources and pathways of common ragweed expansion may help to better understand its invasion success and provides baseline data for future studies on the evolutionary processes involved during range expansion in novel environments.