Inbreeding in a dioecious plant has sex- and population origin-specific effects on its interactions with pollinators

We study the effects of inbreeding in a dioecious plant on its interaction with pollinating insects and test whether the magnitude of such effects is shaped by plant individual sex and the evolutionary histories of plant populations. We recorded spatial, scent, colour and rewarding flower traits as well as pollinator visitation rates in experimentally inbred and outbred, male and female Silene latifolia plants from European and North American populations differing in their evolutionary histories. We found that inbreeding specifically impairs spatial flower traits and floral scent. Our results support that sex-specific selection and gene expression may have partially magnified these inbreeding costs for females, and that divergent evolutionary histories altered the genetic architecture underlying inbreeding effects across population origins. Moreover, the results indicate that inbreeding effects on floral scent may have a huge potential to disrupt interactions among plants and nocturnal moth pollinators, which are mediated by elaborate chemical communication.

Detecting sex-linked genes using genotyped individuals sampled in natural populations

We propose a method, SDpop, able to infer sex-linkage caused by recombination suppression typical of sex chromosomes. The method is based on the modeling of the allele and genotype frequencies of individuals of known sex in natural populations. It is implemented in a hierarchical probabilistic framework, accounting for different sources of error. It allows statistical testing for the presence or absence of sex chromosomes, and detection of sex-linked genes based on the posterior probabilities in the model. Furthermore, for gametologous sequences, the haplotype and level of nucleotide polymorphism of each copy can be inferred, as well as the divergence between them. We test the method using simulated data, as well as data from both a relatively recent and an old sex chromosome system (the plant Silene latifolia and humans), and show that, for most cases, robust predictions are obtained with 5 to 10 individuals per sex.

Identification of developmentally important genes in Silene latifolia through chemical genetics and transcriptome profiling

Dioecious plants possess diverse sex determination systems and unique mechanisms of reproductive organ development; however, little is known about how sex-linked genes shape the expression of regulatory cascades that lead to developmental differences between sexes. In Silene latifolia, a dioecious plant with stable dimorphism in floral traits, early experiments suggested that female-regulator genes act on the factors that determine the boundaries of the flower whorls. To identify these regulators, we sequenced the transcriptome of male flowers with fully developed gynoecia induced by rapid demethylation in the parental generation. As the hermaphrodite flower trait is holandric (transmitted only from male to male, inherited on the Y chromosome), we screened for genes that are differentially expressed between male, female, and hermaphrodite flowers. Dozens of candidate genes that are upregulated in hermaphrodite flowers compared to male and female flowers were detected and found to have putative roles in floral organization, affecting the expression of floral MADS-box and other genes. Amongst these genes, eight candidates were found to promote gynoecium formation in female and hermaphrodite flowers, affecting organ size, whorl boundary, and the expression of mainly B class flower genes. To complement our transcriptome analysis, we closely examined the floral organs in their native state using a field emission environmental scanning electron microscope. Our results reveal the principal regulatory pathways involved in sex-specific flower development in the classical model of dioecy, S. latifolia.

Population history and the differential consequences of inbreeding and outcrossing in a plant metapoplation

ABSTRACTThe phenotypic consequences of inbreeding typically result in a fitness decline proportional to the increase in the inbreeding coefficient, F. This basic assumption of a predictable, inverse relationship between fitness and F has been questioned by a number of empirical studies. We explored the relationship between population history and inbreeding in a metapopulation of the plant Silene latifolia, for which long-term data are available for the historical size and spatial distribution of hundreds of local demes. We used a population genetic analysis to estimate gene flow and bi-parental inbreeding (FIS) in demes with different histories of spatial isolation. A controlled crossing experiment examined whether the effect of inbreeding and outcrossing on fitness-related traits varied with different histories of population size and isolation. Historically isolated demes experienced less gene flow and an increase in FIS, as well as significant inbreeding advantage and outbreeding depression for traits expressed early in life. The causes of variation in the F-fitness relationship among populations will include variance in the distribution of deleterious recessive alleles driven by aspects of population history, including population size, founder effects, gene flow, bi-parental inbreeding, and opportunities for the purging of genetic load. Our findings show that isolation and historical variation in population size likely contribute substantial variation in past inbreeding and the consequences of future inbreeding across the metapopulation.

Cyto-nuclear linkage disequilibrium resulting from admixture

ABSTRACTPrevious studies of North American populations of the invasive plant Silene latifolia showed significant cyto-nuclear linkage disequilibrium (CNLD) between SNP variants of a mitochondrial gene (atp1) and the most common allele at nuclear microsatellite loci. Fields et al. (2014) hypothesized that this CNLD arose partially as a consequence of admixture that occurred during the colonization of North American (NA) populations of S latifolia via seed dispersal from genetically differentiated European populations that represent a portion of the native range of this species. In order to evaluate the plausibility of the admixture hypothesis, as opposed to metapopulation processes alone, we estimated CNLD for these same loci using data collected from eastern (EEU) and western (WEU) European populations of S. latifolia known to be genetically differentiated and likely sources of the spread of the study species to North America. We show that the CNLD found previously in NA populations of S. latifolia can be attributed to admixture of the previously isolated European demes coupled with decay since that time. Our applied framework allows the separation of the forces generating and dissolving statistical associations between alleles in cytoplasmic organelles and the nuclear genome and may thus be of utility in the study of plant or animal microbiomes.

Pollination and fruit infestation under artificial light at night:light colour matters

Rapid human population growth and associated urbanization lead to increased artificial illumination of the environment. By changing the natural light–dark cycle, artificial lighting can affect the functioning of natural ecosystems. Many plants rely on insects in order to reproduce but these insects are known to be disturbed by artificial light. Therefore, plant–insect interactions may be affected when exposed to artificial illumination. These effects can potentially be reduced by using different light spectra than white light. We studied the effect of artificial lighting on plant–insect interactions in the Silene latifolia–Hadena bicruris system using a field set-up with four different light treatments: red, green, white and a dark control. We compared the proportion of fertilized flowers and fertilized ovules as well as the infestation of fruits by Hadena bicruris, a pollinating seed predator. We found no difference in the proportion of fertilized flowers among the treatments. The proportion of fruits infested by H. bicruris was however significantly higher under green and white light and a significantly lower proportion of fertilized ovules was found under green light. We show that artificial light with different colours impacts plant–insect interactions differently, with direct consequences for plant fitness.