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When is it worth being a self-compatible hermaphrodite? Context-dependent effects of self-pollination on female advantage in gynodioecious Silene nutans.

ABSTRACT: In gynodioecious plant species with nuclear-cytoplasmic sex determination, females and hermaphrodites plants can coexist whenever female have higher seed fitness than hermaphrodites. Although the effect of self fertilization on seed fitness in hermaphrodites has been considered theoretically, this effect is far from intuitive, because it can either increase the relative seed fitness of the females (if it leads hermaphrodites to produce inbred, low quality offspring) or decrease it (if it provides reproductive assurance to hermaphrodites). Hence, empirical investigation is needed to document whether relative seed fitness varies with whether pollen is or is not limiting to seed production. In the current study, we measured fruit set and seed production in both females and hermaphrodites and the selfing rate in hermaphrodites in two experimental patches that differed in sex ratios in the gynodioecious plant Silene nutans. We found an impact of plant gender, patch, and their interaction, with females suffering from stronger pollen limitation when locally frequent. In the most pollen-limited situation, the selfing rate of hermaphrodites increased and provided hermaphrodites with a type of reproductive assurance that is not available to females. By integrating both the beneficial (reproductive assurance) and costly effects (through inbreeding depression) of self-pollination, we showed that whether females did or did not exhibit higher seed fitness depended on the degree of pollen limitation on seed production.

SUBMITTER: Lahiani E

PROVIDER: S-EPMC4485966 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundGynodioecious species exist in two sexes - male-sterile females and hermaphrodites. Male sterility in higher plants often results from mitonuclear interaction between the CMS (cytoplasmic male sterility) gene(s) encoded by mitochondrial genome and by nuclear-encoded restorer genes. Mitochondrial and nuclear-encoded transcriptomes in females and hermaphrodites are intensively studied, but little is known about sex-specific gene expression in plastids. We have compared plastid transcriptomes between females and hermaphrodites in two haplotypes of a gynodioecious species Silene vulgaris with known CMS candidate genes.ResultsWe generated complete plastid genome sequences from five haplotypes S. vulgaris including the haplotypes KRA and KOV, for which complete mitochondrial genome sequences were already published. We constructed a phylogenetic tree based on plastid sequences of S. vulgaris. Whereas lowland S. vulgaris haplotypes including KRA and KOV clustered together, the accessions from high European mountains diverged early in the phylogram. S. vulgaris belongs among Silene species with slowly evolving plastid genomes, but we still detected 212 substitutions and 112 indels between two accessions of this species. We estimated elevated Ka/Ks in the ndhF gene, which may reflect the adaptation of S. vulgaris to high altitudes, or relaxed selection. We compared depth of coverage and editing rates between female and hermaphrodite plastid transcriptomes and found no significant differences between the two sexes. We identified 51 unique C to U editing sites in the plastid genomes of S. vulgaris, 38 of them in protein coding regions, 2 in introns, and 11 in intergenic regions. The editing site in the psbZ gene was edited only in one of two plastid genomes under study.ConclusionsWe revealed no significant differences between the sexes in plastid transcriptomes of two haplotypes of S. vulgaris. It suggests that gene expression of plastid genes is not affected by CMS in flower buds of S. vulgaris, although both sexes may still differ in plastid gene expression in specific tissues. We revealed the difference between the plastid transcriptomes of two S. vulgaris haplotypes in editing rate and in the coverage of several antisense transcripts. Our results document the variation in plastid genomes and transcriptomes in S. vulgaris.

Project description:High reciprocal pollination specialization leading to pollinator isolation can prevent interspecific pollen transfer and competition for pollinators. Sharing pollinators may induce mating costs, but it may also increase pollination services and pollen dispersal and offer more resources to pollinators, which may be important in case of habitat fragmentation leading to pollination disruption. We estimated pollen dispersal and pollinator isolation or sharing between two reproductively isolated genetic lineages of Silene nutans (Caryophyllaceae), which are rare and occur in parapatry in southern Belgium, forming two edaphic ecotypes. As inter-ecotypic crosses may lead to pollen wastage and inviable progeny, pollinator isolation might have evolved between ecotypes. Silene nutans is mainly pollinated by nocturnal moths, including nursery pollinators, which pollinate and lay their eggs in flowers, and whose caterpillars feed on flowers and seeds. Pollinator assemblages of the two ecotypes are largely unknown and inter-ecotypic pollen flows have never been investigated. Fluorescent powdered dyes were used as pollen analogues to quantify intra- and inter-ecotypic pollen transfers and seeds were germinated to detect chlorotic seedlings resulting from inter-ecotypic pollination. Nocturnal pollinators were observed using infrared cameras on the field, and seed-eating caterpillars were collected and reared to identify nursery pollinator species. No pollinator isolation was found: we detected long-distance (up to 5 km) inter-ecotypic dye transfers and chlorotic seedlings, indicating inter-ecotypic fertilization events. The rare moth Hadena albimacula, a nursery pollinator specialized on S. nutans, was found on both ecotypes, as well as adults visiting flowers (cameras recordings) as seed-eating caterpillars. However, S. nutans populations harbor different abundance and diversity of seed predator communities, including other rare nursery pollinators, suggesting a need for distinct conservation strategies. Our findings demonstrate the efficiency of moths, especially of nursery pollinators, to disperse pollen over long distances in natural landscapes, so to ensure gene flow and population sustainability of the host plant. Seed-predator specificities between the two reproductively isolated genetic lineages of S. nutans, and pollinator sharing instead of pollinator isolation when plants occur in parapatry, suggest that conservation of the host plant is also essential for sustaining (rare) pollinator and seed predator communities.

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When is it worth being a self-compatible hermaphrodite? Context-dependent effects of self-pollination on female advantage in gynodioecious Silene nutans.

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