DOES FREQUENCY‐DEPENDENT SELECTION WITH COMPLEX DOMINANCE INTERACTIONS ACCURATELY PREDICT ALLELIC FREQUENCIES AT THE SELF‐INCOMPATIBILITY LOCUS IN ARABIDOPSIS HALLERI?

Frequency-dependent selection is a major force determining the evolutionary dynamics of alleles at the self-incompatibility locus (S-locus) in flowering plants. We introduce a general method using numerical simulations to test several alternative models of frequency-dependent selection on S-locus data from sporophytic systems, taking into account both genetic drift and observed patterns of dominance interactions among S-locus haplotypes (S-haplotypes). Using a molecular typing method, we estimated S-haplotype frequencies in a sample of 322 adult plants and of 245 offspring obtained from seeds sampled on 22 maternal plants, collected in a single population of Arabidopsis halleri (Brassicaceae). We found eight different S-haplotypes and characterized their dominance interactions by controlled pollinations. We then compared the likelihood of different models of frequency-dependent selection: we found that the observed haplotype frequencies and observed frequency changes in one generation best fitted a model with (1) the observed dominance interactions and (2) no pollen limitation. Overall, our population genetic models of frequency-dependent selection, including patterns of dominance interactions among S-haplotypes and genetic drift, can reliably predict polymorphism at the S-locus. We discuss how these approaches allow detecting additional processes influencing the evolutionary dynamics of the S-locus, such as purifying selection on linked loci.     

Uneven segregation of sporophytic self-incompatibility alleles in Arabidopsis lyrata

Self-incompatibility in Arabidopsis lyrata is sporophytically controlled by the multi-allelic S-locus. Self-incompatibility alleles (S-alleles) are under strong negative frequency dependent selection because pollen carrying common S-alleles have fewer mating opportunities. Population genetics theory predicts that deleterious alleles can accumulate if linked to the S-locus. This was tested by studying segregation of S-alleles in 11 large full sib families in A. lyrata. Significant segregation distortion leading to an up to fourfold difference in transmission rates was found in six families. Differences in transmission rates were not significantly different in reciprocal crosses and the distortions observed were compatible with selection acting at the gametic stage alone. The S-allele with the largest segregation advantage is also the most recessive, and is very common in natural populations concordant with its apparent segregation advantage. These results imply that frequencies of S-alleles in populations of A. lyrata cannot be predicted based on simple models of frequency-dependent selection alone.     

Disentangling the effects of breakdown of self-incompatibility and transition to selfing in North American Arabidopsis lyrata

A breakdown of self‐incompatibility (SI) followed by a shift to selfing is commonly observed in the evolution of flowering plants. Both are expected to reduce the levels of heterozygosity and genetic diversity. However, breakdown of SI should most strongly affect the region of the SI locus (S‐locus) because of the relaxation of balancing selection that operates on a functional S‐locus, and a potential selective sweep. In contrast, a transition to selfing should affect the whole genome. We set out to disentangle the effects of breakdown of SI and transition to selfing on the level and distribution of genetic diversity in North American populations of Arabidopsis lyrata. Specifically, we compared sequence diversity of loci linked and unlinked to the S‐locus for populations ranging from complete selfing to fully outcrossing. Regardless of linkage to the S‐locus, heterozygosity and genetic diversity increased with population outcrossing rate. High heterozygosity of self‐compatible individuals in outcrossing populations suggests that SI is not the only factor preventing the evolution of self‐fertilization in those populations. There was a strong loss of diversity in selfing populations, which was more pronounced at the S‐locus. In addition, selfing populations showed an accumulation of derived mutations at the S‐locus. Our results provide evidence that beyond the genome‐wide consequences of the population bottleneck associated with the shift to selfing, the S‐locus of A. lyrata shows a specific signal either reflecting the relaxation of balancing selection or positive selection.     

Evolutionary dynamics of mating system shifts in Arabidopsis lyrata

Outcrossing is the prevalent mode of reproduction in plants and animals despite its substantial costs, while selfing and mixed mating occur at much lower frequency. Comparative research on plants has demonstrated the lability of self‐incompatibility, but there is little information about the transition on a within‐species level from self‐incompatibility to predominant selfing. We studied variation in mating system among 18 populations of Arabidopsis lyrata within a phylogenetic context to shed light on the evolution of selfing. Realized and potential mating systems were assessed by genetic analysis with microsatellite markers and hand‐self‐pollinations on 30 plants from each population. The fraction of self‐incompatible plants in a population was highly correlated with the outcrossing rate, showing that the spread of self‐compatibility is accompanied by or soon followed by an increase in the rate of selfing. The four predominantly selfing populations (outcrossing rates < 0.25) fell into more than one phylogenetic cluster, suggesting that the transition to selfing occurred more than once independently. Hence, A. lyrata offers an opportunity for the comparative analysis of outcrossing as a predominant mode of reproduction in plants and of the causes of the shift to selfing.     

UNDERSTANDING PROMISCUITY: WHEN IS SEEKING ADDITIONAL MATES BETTER THAN GUARDING AN ALREADY FOUND ONE?

Paternity protection and the acquisition of multiple mates select for different traits. The consensus from theoretical work is that mate‐guarding intensifies with an increasing male bias in the adult sex ratio (ASR). A male bias can thus lead to male monogamy if guarding takes up the entire male time budget. Given that either female‐ or male‐biased ASRs are possible, why is promiscuity clearly much more common than male monogamy? We address this question with two models, differing in whether males can assess temporal cues of female fertility. Our results confirm the importance of the ASR: guarding durations increase with decreasing female availability and increasing number of male competitors. However, several factors prevent the mating system from switching to male monogamy as soon as the ASR becomes male biased. Inefficient guarding, incomplete last male sperm precedence, any mechanism that allows sperm to fertilize eggs after the male's departure, and (in some cases) the unfeasibility of precopulatory guarding all help explain cases where promiscuity exists on its own or alongside temporally limited mate‐guarding. Shortening the window of fertilization shifts guarding time budgets from the postcopulatory to the precopulatory stage.     

The best of both worlds? A review of delayed selfing in flowering plants

Premise of Study

In a seminal body of theory, Lloyd showed that the fitness consequences of selfing will depend on its timing in anthesis. Selfing that occurs after opportunities for outcrossing or pollen dispersal can provide reproductive assurance when pollinators are limited and is expected to incur little cost, even when inbreeding depression is high. As a result, delayed selfing is often interpreted as a “best‐of‐both‐worlds” mating system that combines the advantages of selfing and outcrossing.

Methods

We surveyed 65 empirical studies of delayed selfing, recording floral mechanisms and examining information on inbreeding depression, autofertility, and other parameters to test the support for delayed selfing as a best‐of‐both‐worlds strategy.

Key Results

Phylogenetic distribution of the diverse floral mechanisms suggests that some basic floral structures may predispose plant taxa to evolve delayed selfing. Delayed selfing appears to serve as a best‐of‐both‐worlds strategy in some but not all species. While the capacity for autonomous selfing is often high, it is lower, in some cases, than in related species with earlier modes of selfing. In other delayed‐selfers, low inbreeding depression and reduced investment in corollas and pollen suggest limited benefits from outcrossing.

Conclusions

Despite a growing literature on the subject, experimental evidence for delayed selfing is limited and major gaps in knowledge remain, particularly with respect to the stability of delayed selfing and the conditions that may favor transitions between delayed and earlier selfing. Finally, we suggest a potential role of delayed selfing in facilitating transitions from self‐incompatibility to selfing.     

Flexible mating: cross-pollination affects sex-expression in a marine clonal plant

Many functionally hermaphroditic plants have evolved mechanisms to reduce interference between the sex functions and to optimize reproductive output. In addition to physical mechanisms such as the spatial (herkogamy) and temporal (dichogamy) separation of male and female functions, plasticity in sex expression by means of mate-recognition (flexible mating) could be important in plants with variable access to cross-pollen. This applies particularly to clonal plants because of their modular growth form. We experimentally tested for the effects of pollen source and vegetative neighbourhood on instantaneous sex ratio and seed production in the self-compatible clonal marine angiosperm Zostera marina L. To this end, we exposed the (monoecious) flowering shoots to self and cross-pollen and to neighbourhoods of their own and a mix of foreign vegetative shoots. Flowering shoots that had been exposed to cross-pollen showed (1) a significantly lower female/male ratio at peak flowering, evidence for mate-recognition, and (2) a significantly higher seed set by the end of the season. Both effects were independent of the genetic composition of their vegetative neighbourhood. The results suggest that Z. marina maintains a cryptic self-incompatibility system not previously described for angiosperms with sub-aqueous pollination. In Z. marina, and possibly other self-compatible clonal plant species, mate-recognition could be a means of increasing the out-crossing probability for flowering shoots with central positions within their clone.