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Fine-scale spatial genetic structure and gene dispersal in Silene latifolia.

ABSTRACT: Plants are sessile organisms, often characterized by limited dispersal. Seeds and pollen are the critical stages for gene flow. Here we investigate spatial genetic structure, gene dispersal and the relative contribution of pollen vs seed in the movement of genes in a stable metapopulation of the white campion Silene latifolia within its native range. This short-lived perennial plant is dioecious, has gravity-dispersed seeds and moth-mediated pollination. Direct measures of pollen dispersal suggested that large populations receive more pollen than small isolated populations and that most gene flow occurs within tens of meters. However, these studies were performed in the newly colonized range (North America) where the specialist pollinator is absent. In the native range (Europe), gene dispersal could fall on a different spatial scale. We genotyped 258 individuals from large and small (15) subpopulations along a 60?km, elongated metapopulation in Europe using six highly variable microsatellite markers, two X-linked and four autosomal. We found substantial genetic differentiation among subpopulations (global F(ST)=0.11) and a general pattern of isolation by distance over the whole sampled area. Spatial autocorrelation revealed high relatedness among neighboring individuals over hundreds of meters. Estimates of gene dispersal revealed gene flow at the scale of tens of meters (5-30?m), similar to the newly colonized range. Contrary to expectations, estimates of dispersal based on X and autosomal markers showed very similar ranges, suggesting similar levels of pollen and seed dispersal. This may be explained by stochastic events of extensive seed dispersal in this area and limited pollen dispersal.

SUBMITTER: Barluenga M

PROVIDER: S-EPMC3183859 | biostudies-other | 2011 Jan

REPOSITORIES: biostudies-other

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Fine-scale spatial genetic structure and gene dispersal in Silene latifolia.

Barluenga M M Austerlitz F F Elzinga J A JA Teixeira S S Goudet J J Bernasconi G G

Heredity 20100414 1

Plants are sessile organisms, often characterized by limited dispersal. Seeds and pollen are the critical stages for gene flow. Here we investigate spatial genetic structure, gene dispersal and the relative contribution of pollen vs seed in the movement of genes in a stable metapopulation of the white campion Silene latifolia within its native range. This short-lived perennial plant is dioecious, has gravity-dispersed seeds and moth-mediated pollination. Direct measures of pollen dispersal sugge ...[more]

PMID: 20389310

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Project description:Climate warming is predicted to increase the frequency of invasions by pathogens and to cause the large-scale redistribution of native host species, with dramatic consequences on the health of domesticated and wild populations of plants and animals. The study of historic range shifts in response to climate change, such as during interglacial cycles, can help in the prediction of the routes and dynamics of infectious diseases during the impending ecosystem changes. Here we studied the population structure in Europe of two Microbotryum species causing anther smut disease on the plants Silene latifolia and Silene dioica. Clustering analyses revealed the existence of genetically distinct groups for the pathogen on S. latifolia, providing a clear-cut example of European phylogeography reflecting recolonization from southern refugia after glaciation. The pathogen genetic structure was congruent with the genetic structure of its host species S. latifolia, suggesting dependence of the migration pathway of the anther smut fungus on its host. The fungus, however, appeared to have persisted in more numerous and smaller refugia than its host and to have experienced fewer events of large-scale dispersal. The anther smut pathogen on S. dioica also showed a strong phylogeographic structure that might be related to more northern glacial refugia. Differences in host ecology probably played a role in these differences in the pathogen population structure. Very high selfing rates were inferred in both fungal species, explaining the low levels of admixture between the genetic clusters. The systems studied here indicate that migration patterns caused by climate change can be expected to include pathogen invasions that follow the redistribution of their host species at continental scales, but also that the recolonization by pathogens is not simply a mirror of their hosts, even for obligate biotrophs, and that the ecology of hosts and pathogen mating systems likely affects recolonization patterns.

Project description:BackgroundThe evolution of sex chromosomes is often accompanied by gene or chromosome rearrangements. Recently, the gene AP3 was characterized in the dioecious plant species Silene latifolia. It was suggested that this gene had been transferred from an autosome to the Y chromosome.ResultsIn the present study we provide evidence for the existence of an X linked copy of the AP3 gene. We further show that the Y copy is probably located in a chromosomal region where recombination restriction occurred during the first steps of sex chromosome evolution. A comparison of X and Y copies did not reveal any clear signs of degenerative processes in exon regions. Instead, both X and Y copies show evidence for relaxed selection compared to the autosomal orthologues in S. vulgaris and S. conica. We further found that promoter sequences differ significantly. Comparison of the genic region of AP3 between the X and Y alleles and the corresponding autosomal copies in the gynodioecious species S. vulgaris revealed a massive accumulation of retrotransposons within one intron of the Y copy of AP3. Analysis of the genomic distribution of these repetitive elements does not indicate that these elements played an important role in the size increase characteristic of the Y chromosome. However, in silico expression analysis shows biased expression of individual domains of the identified retroelements in male plants.ConclusionsWe characterized the structure and evolution of AP3, a sex linked gene with copies on the X and Y chromosomes in the dioecious plant S. latifolia. These copies showed complementary expression patterns and relaxed evolution at protein level compared to autosomal orthologues, which suggests subfunctionalization. One intron of the Y-linked allele was invaded by retrotransposons that display sex-specific expression patterns that are similar to the expression pattern of the corresponding allele, which suggests that these transposable elements may have influenced evolution of expression patterns of the Y copy. These data could help researchers decipher the role of transposable elements in degenerative processes during sex chromosome evolution.

Project description:BACKGROUND:Molecular studies in social mammals rarely compare the inferences gained from genetic analyses with field information, especially in the context of dispersal. In this study, we used genetic data to elucidate sex-specific dispersal dynamics in the Virunga Massif mountain gorilla population (Gorilla beringei beringei), a primate species characterized by routine male and female dispersal from stable mixed-sex social groups. Specifically, we conducted spatial genetic structure analyses for each sex and linked our genetically-based observations with some key demographic and behavioural data from this population. RESULTS:To investigate the spatial genetic structure of mountain gorillas, we analysed the genotypes of 193 mature individuals at 11 microsatellite loci by means of isolation-by-distance and spatial autocorrelation analyses. Although not all males and females disperse, female gorillas displayed an isolation-by-distance pattern among groups and a signal of dispersal at short distances from their natal group based on spatial autocorrelation analyses. In contrast, male genotypes were not correlated with spatial distance, thus suggesting a larger mean dispersal distance for males as compared to females. Both within sex and mixed-sex pairs were on average genetically more related within groups than among groups. CONCLUSIONS:Our study provides evidence for an intersexual difference in dispersal distance in the mountain gorilla. Overall, it stresses the importance of investigating spatial genetic structure patterns on a sex-specific basis to better understand the dispersal dynamics of the species under investigation. It is currently poorly understood why some male and female gorillas disperse while others remain in the natal group. Our results on average relatedness within and across groups confirm that groups often contain close relatives. While inbreeding avoidance may play a role in driving female dispersal, we note that more detailed dyadic genetic analyses are needed to shed light on the role of inbreeding avoidance as an ultimate cause of female dispersal in mountain gorillas.

Dataset Information

Fine-scale spatial genetic structure and gene dispersal in Silene latifolia.

Publications

Fine-scale spatial genetic structure and gene dispersal in Silene latifolia.

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