Season-dependent effect of cleistogamy in Lamium amplexicaule: flower type origin versus inbreeding status.

PREMISE: Inbreeding depression is traditionally considered a major factor favoring outcrossing in hermaphrodites. Recent experiments have shown that environmental conditions can influence the magnitude of inbreeding depression, but their relevance in natural populations is unclear. To investigate this, we studied the cleistogamous species Lamium amplexicaule, an annual species with individuals experiencing either spring or autumn environmental conditions. In this species, the proportion of cleistogamous/chasmogamous flowers changes according to seasonal cues (e.g., temperature, photoperiod). Our hypothesis was that the plasticity of cleistogamy is an adaptation to seasonal fitness variation in different flower progenies. METHODS: To test this hypothesis, we produced the three possible types of progenies through controlled crosses: (1) selfed progeny from cleistogamous flowers; (2) chasmogamous selfed progeny; and (3) chasmogamous outcrossed progeny. Progeny fitness was then measured in a common garden in the two reproduction seasons (autumn and spring). RESULTS: The results showed that season had a major impact on fitness. The fitness of the different progeny types changed across seasons, indicating that the effect of cleistogamy on progeny performance is season-dependent, consistent with a previous study in a similar environment. Surprisingly, the flower from which the progeny issued (cleistogamous or chasmogamous) had more impact on fitness than the inbred status of the progeny (selfed versus outcrossed), suggesting a potential role of epigenetic processes. CONCLUSIONS: The observed patterns of variation were not consistent either with adaptation to environment-dependent inbreeding depression or to variation in resource availability, but were possibly consistent with adaptation to seasonal pollinator activity.

Patterns of Genome-Wide Nucleotide Diversity in the Gynodioecious Plant Thymus vulgaris Are Compatible with Recent Sweeps of Cytoplasmic Genes.

Gynodioecy is a sexual dimorphism where females coexist with hermaphrodite individuals. In most cases, this dimorphism involves the interaction of cytoplasmic male sterility (CMS) genes and nuclear restorer genes. Two scenarios can account for how these interactions maintain gynodioecy. Either CMS genes recurrently enter populations at low frequency via mutation or migration and go to fixation unimpeded (successive sweeps), or CMS genes maintain polymorphism over evolutionary time through interactions with a nuclear restorer allele (balanced polymorphism). To distinguish between these scenarios, we used transcriptome sequencing in gynodioecious Thymus vulgaris and surveyed genome-wide diversity in 18 naturally occurring individuals sampled from populations at a local geographic scale. We contrast the amount and patterns of nucleotide diversity in the nuclear and cytoplasmic genome, and find ample diversity at the nuclear level (π = 0.019 at synonymous sites) but reduced genetic diversity and an excess of rare polymorphisms in the cytoplasmic genome relative to the nuclear genome. Our finding is incompatible with the maintenance of gynodioecy via scenarios invoking long-term balancing selection, and instead suggests the recent fixation of CMS lineages in the populations studied.

Isolation and characterization of microsatellite markers for the cleistogamous species Lamium amplexicaule (Lamiaceae).

PREMISE OF THE STUDY: Lamium amplexicaule is a cleistogamous plant that produces both closed flowers (obligately self-pollinated) and open flowers (potentially outcrossed). The conditions for the maintenance of such a mating system depend on the outcrossing rate of the open flowers, which can be estimated using neutral microsatellite markers. • METHODS AND RESULTS: Forty primer pairs corresponding to microsatellite motifs obtained by coupling multiplex microsatellite enrichment and next-generation sequencing were tested. Thirteen primers amplified with satisfying results. The polymorphism of these markers was studied in four French populations. Allele number varied from one to eight per locus and per population. Heterozygosity levels were significantly lower than those expected under Hardy-Weinberg equilibrium. • CONCLUSIONS: Our results are consistent with a partial self-fertilization pattern. These markers will be used to estimate the outcrossing rate as well as population differentiation in L. amplexicaule.

Consequences of low mate availability in the rare self-incompatible species Brassica insularis.

Self-incompatibility systems prevent self-fertilization in angiosperms. Although numerous S alleles are usually maintained by negative frequency-dependent selection, the number of S alleles can be low in small populations, which limits mate availability and reduces fecundity in endangered populations of self-incompatible plants. Despite the increasing evidence of the negative effect of self-incompatibility in small populations, the direct link between the number and the distribution of S alleles and their reproductive consequences has been rarely reported. Brassica insularis is a rare self-incompatible species with medium to very small populations. Results of a previous study showed that the smallest population has very few S alleles. We investigated whether reduced mate availability affects reproduction in this species. We compared the pollination success and the fruit set in 4 populations differing in population size and number of S alleles. Our results suggest that reproduction may be negatively affected by the low S-allele diversity in the smallest population. Nevertheless, other populations also had reduced fruit set that could not be attributed to self-incompatibility alone.

Sex inheritance in gynodioecious species: a polygenic view.

Gynodioecy is defined as the coexistence of two different sexual morphs in a population: females and hermaphrodites. This breeding system is found among many different families of angiosperms and is usually under nucleo-cytoplasmic inheritance, with maternally inherited genes causing male sterility and nuclear factors restoring male fertility. Numerous theoretical models have investigated the conditions for the stable coexistence of females and hermaphrodites. To date, all models rest on the assumption that restoration of a given male sterile genotype is controlled by a single Mendelian factor. Here, we review data bearing on the genetic determinism of sex inheritance in three gynodiecious plant species. We suggest that restoration of male fertility is probably best viewed as a quantitative trait controlled by many loci. We develop a threshold model that accommodates an underlying polygenic trait, which is resolved at the phenotypic level in discrete sexual morphs. We use this model to reanalyse data in Thymus vulgaris, Silene vulgaris and Plantago coronopus. A simple Mendelian inheritance of sex determinism is unlikely in all three species. We discuss how our model can shed additional light on the genetics of restoration and point towards future efforts in the modelling of gynodioecy.