The evolution of self-incompatibility when mates are limiting

Busch, Jeremiah W.; Schoen, Daniel J.

doi:10.1016/j.tplants.2008.01.002

Cited by 184 publications

(189 citation statements)

References 83 publications

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“…We detected low levels of inbreeding in H. oldfieldii , but these do not exclude the possibility of an SI system. Quantitative variation in the strength of SI responses is a recognized phenomenon (Busch and Schoen 2008), and some self‐fertilization or mating between relatives can occur. We suggest therefore that it may be the distribution of compatible mates throughout the population that results in a large proportion of successful pollen coming from more distant and unrelated sources.…”

Section: Discussionmentioning

confidence: 99%

Limiting inbreeding in disjunct and isolated populations of a woody shrub

Sampson

Byrne

Gibson

et al. 2016

Ecology and Evolution

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Pollen movements and mating patterns are key features that influence population genetic structure. When gene flow is low, small populations are prone to increased genetic drift and inbreeding, but naturally disjunct species may have features that reduce inbreeding and contribute to their persistence despite genetic isolation. Using microsatellite loci, we investigated outcrossing levels, family mating parameters, pollen dispersal, and spatial genetic structure in three populations of Hakea oldfieldii, a fire‐sensitive shrub with naturally disjunct, isolated populations prone to reduction in size and extinction following fires. We mapped and genotyped a sample of 102 plants from a large population, and all plants from two smaller populations (28 and 20 individuals), and genotyped 158–210 progeny from each population. We found high outcrossing despite the possibility of geitonogamous pollination, small amounts of biparental inbreeding, a limited number of successful pollen parents within populations, and significant correlated paternity. The number of pollen parents for each seed parent was moderate. There was low but significant spatial genetic structure up to 10 m around plants, but the majority of successful pollen came from outside this area including substantial proportions from distant plants within populations. Seed production varied among seven populations investigated but was not correlated with census population size. We suggest there may be a mechanism to prevent self‐pollination in H. oldfieldii and that high outcrossing and pollen dispersal within populations would promote genetic diversity among the relatively small amount of seed stored in the canopy. These features of the mating system would contribute to the persistence of genetically isolated populations prone to fluctuations in size.

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Section: Discussionmentioning

confidence: 99%

Limiting inbreeding in disjunct and isolated populations of a woody shrub

Sampson

Byrne

Gibson

et al. 2016

Ecology and Evolution

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“…The influence of the number of S-alleles on patterns of SGS at the S-locus has some consequences for conservation genetics issues. Indeed, a concern in managing very small plant populations with functional SI is that the number of S-alleles present in the population may be very small, such that any given individual may mostly receive pollen from individuals sharing the same alleles, hence reducing seed-set (Kirchner et al, 2006;Busch and Schoen, 2008). This effect (called the 'S-Allee effect' by Wagenius et al, 2007) was expected to be stronger under low pollen dispersal because of reproduction within local neighborhoods.…”

Section: Influence Of the Self-incompatibility Model On Sgs At The S-mentioning

confidence: 99%

Effect of balancing selection on spatial genetic structure within populations: theoretical investigations on the self-incompatibility locus and empirical studies in Arabidopsis halleri

et al. 2010

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The effect of selection on patterns of genetic structure within and between populations may be studied by contrasting observed patterns at the genes targeted by selection with those of unlinked neutral marker loci. Local directional selection on target genes will produce stronger population genetic structure than at neutral loci, whereas the reverse is expected for balancing selection. However, theoretical predictions on the intensity of this signal under precise models of balancing selection are still lacking. Using negative frequency-dependent selection acting on self-incompatibility systems in plants as a model of balancing selection, we investigated the effect of such selection on patterns of spatial genetic structure within a continuous population. Using numerical simulations, we tested the effect of the type of self-incompatibility system, the number of alleles at the selfincompatibility locus and the dominance interactions among them, the extent of gene dispersal, and the immigration rate on spatial genetic structure at the selected locus and at unlinked neutral loci. We confirm that frequency-dependent selection is expected to reduce the extent of spatial genetic structure as compared to neutral loci, particularly in situations with low number of alleles at the self-incompatibility locus, high frequency of codominant interactions among alleles, restricted gene dispersal and restricted immigration from outside populations. Hence the signature of selection on spatial genetic structure is expected to vary across species and populations, and we show that empirical data from the literature as well as data reported here on three natural populations of the herb Arabidopsis halleri confirm these theoretical results.

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“…In general, it seems that S-modifier loci are maintained as part of SI systems when they contribute to the regulation of outcrossing or compensate for conditions where the reproductive costs of full SI are high (Vallejo-Marín and Uyenoyama, 2004;Harder et al, 2007;Busch and Schoen, 2008).…”

Section: Introductionmentioning

confidence: 99%

“…However, the relationship is not a simple one because genetic load is also itself responsive to selection and coevolves with mating system (Latta, 1994;Glemín et al, 2001). Ecological factors such as pollination biology, dispersal and number of reproductive opportunities also affect reproductive assurance, and are extremely important for the maintenance and evolution of SI systems, because they influence the selective advantage of outcrossing versus selfing (Harder et al, 2007;Busch and Schoen, 2008;Johnston et al, 2009). Against this background of interacting factors that introduce shifting costs and benefits of outcrossing, it is perhaps no surprise that loci that influence SI expression and cause limited selfing (hereafter referred to as 'S modifiers') appear to be an extremely common feature of SI systems (Levin, 1996).…”

Section: Introductionmentioning

confidence: 99%

Sporophytic self-incompatibility in Senecio squalidus (Asteraceae): S allele dominance interactions and modifiers of cross-compatibility and selfing rates

2010

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Understanding genetic mechanisms of self-incompatibility (SI) and how they evolve is central to understanding the mating behaviour of most outbreeding angiosperms. Sporophytic SI (SSI) is controlled by a single multi-allelic locus, S, which is expressed in the diploid (sporophyte) plant to determine the SI phenotype of its haploid (gametophyte) pollen. This allows complex patterns of independent S allele dominance interactions in male (pollen) and female (pistil) reproductive tissues. Senecio squalidus is a useful model for studying the genetic regulation and evolution of SSI because of its population history as an alien invasive species in the UK. S. squalidus maintains a small number of S alleles (7-11) with a high frequency of dominance interactions. Some S. squalidus individuals also show partial selfing and/or greater levels of cross-compatibility than expected under SSI. We previously speculated that these might be adaptations to invasiveness. Here we describe a detailed characterization of the regulation of SSI in S. squalidus. Controlled crosses were used to determine the S allele dominance hierarchy of six S alleles and effects of modifiers on cross-compatibility and partial selfing. Complex dominance interactions among S alleles were found with at least three levels of dominance and tissue-specific codominance. Evidence for S gene modifiers that increase selfing and/or cross-compatibility was also found. These empirical findings are discussed in the context of theoretical predictions for maintenance of S allele dominance interactions, and the role of modifier loci in the evolution of SI.

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The evolution of self-incompatibility when mates are limiting

Cited by 184 publications

References 83 publications

Limiting inbreeding in disjunct and isolated populations of a woody shrub

Limiting inbreeding in disjunct and isolated populations of a woody shrub

Effect of balancing selection on spatial genetic structure within populations: theoretical investigations on the self-incompatibility locus and empirical studies in Arabidopsis halleri

Sporophytic self-incompatibility in Senecio squalidus (Asteraceae): S allele dominance interactions and modifiers of cross-compatibility and selfing rates

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