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Population genetics of self-incompatibility in a clade of relict cliff-dwelling plant species.

ABSTRACT: The mating systems of species in small or fragmented populations impact upon their persistence. Small self-incompatible (SI) populations risk losing S allele diversity, responsible for the SI response, by drift thereby limiting mate availability and leading to population decline or SI system breakdown. But populations of relict and/or endemic species have resisted these demographic conditions over long periods suggesting their mating systems have adapted. To address a lack of empirical data on this topic, we studied the SI systems of three relict cliff-dwelling species of Sonchus section Pustulati (Asteraceae): S. masguindalii, S. fragilis and S. pustulatus in the western Mediterranean region. We performed controlled pollinations within and between individuals to measure index of SI (ISI) expression and identify S alleles in multiple population samples. Sonchus masguindalii and S. pustulatus showed strong SI (ISI?=?0.6-1.0) compared to S. fragilis (ISI?=?0.1-0.7). Just five S alleles were estimated for Spanish S. pustulatus and a moderate 11-15 S alleles for Moroccan S. pustulatus and S. fragilis, respectively. The fact that autonomous fruit set was generally improved by active self-pollination in self-compatible S. fragilis suggests that individuals with weak SI can show a wide range of outcrossing levels dependent on the degree of self or outcross pollen that pollinators bear. We conclude that frequent S allele dominance interactions that mask the incompatibility interactions of recessive S alleles leading to higher mate availability and partial breakdown of SI leading to mixed mating, both contribute to reproductive resilience in this group.

SUBMITTER: Silva JL

PROVIDER: S-EPMC4940477 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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Population genetics of self-incompatibility in a clade of relict cliff-dwelling plant species.

Silva Jose L JL Brennan Adrian C AC Mejías José A JA

AoB PLANTS 20160711

The mating systems of species in small or fragmented populations impact upon their persistence. Small self-incompatible (SI) populations risk losing S allele diversity, responsible for the SI response, by drift thereby limiting mate availability and leading to population decline or SI system breakdown. But populations of relict and/or endemic species have resisted these demographic conditions over long periods suggesting their mating systems have adapted. To address a lack of empirical data on t ...[more]

PMID: 27154621

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Project description:BACKGROUND:Papaver rhoeas possesses a gametophytic self-incompatibility (SI) system not homologous to any other SI mechanism characterized at the molecular level. Four previously published full length stigmatic S-alleles from the genus Papaver exhibited remarkable sequence divergence, but these studies failed to amplify additional S-alleles despite crossing evidence for more than 60 S-alleles in Papaver rhoeas alone. METHODOLOGY/PRINCIPAL FINDINGS:Using RT-PCR we identified 87 unique putative stigmatic S-allele sequences from the Papaveraceae Argemone munita, Papaver mcconnellii, P. nudicuale, Platystemon californicus and Romneya coulteri. Hand pollinations among two full-sib families of both A. munita and P. californicus indicate a strong correlation between the putative S-genotype and observed incompatibility phenotype. However, we also found more than two S-like sequences in some individuals of A. munita and P. californicus, with two products co-segregating in both full-sib families of P. californicus. Pairwise sequence divergence estimates within and among taxa show Papaver stigmatic S-alleles to be the most variable with lower divergence among putative S-alleles from other Papaveraceae. Genealogical analysis indicates little shared ancestral polymorphism among S-like sequences from different genera. Lack of shared ancestral polymorphism could be due to long divergence times among genera studied, reduced levels of balancing selection if some or all S-like sequences do not function in incompatibility, population bottlenecks, or different levels of recombination among taxa. Preliminary estimates of positive selection find many sites under selective constraint with a few undergoing positive selection, suggesting that self-recognition may depend on amino acid substitutions at only a few sites. CONCLUSIONS/SIGNIFICANCE:Because of the strong correlation between genotype and SI phenotype, sequences reported here represent either functional stylar S-alleles, tightly linked paralogs of the S-locus or a combination of both. The considerable complexity revealed in this study shows we have much to learn about the evolutionary dynamics of self-incompatibility systems.

Dataset Information

Population genetics of self-incompatibility in a clade of relict cliff-dwelling plant species.

Publications

Population genetics of self-incompatibility in a clade of relict cliff-dwelling plant species.

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