Disentangling the effects of mating systems and mutation rates on cytoplamic diversity in gynodioecious Silene nutans and dioecious Silene otites

Abstract

Many flowering plant species exhibit a variety of distinct sexual morphs, the two most common cases being the co-occurrence of females and males (dioecy) or the co-occurrence of hermaphrodites and females (gynodioecy). In this study, we compared DNA sequence variability of the three genomes (nuclear, mitochondrial and chloroplastic) of a gynodioecious species, Silene nutans, with that of a closely related dioecious species, Silene otites. In the light of theoretical models, we expect cytoplasmic diversity to differ between the two species due to the selective dynamics that acts on cytoplasmic genomes in gynodioecious species: under an epidemic scenario, the gynodioecious species is expected to exhibit lower cytoplasmic diversity than the dioecious species, while the opposite is expected in the case of balancing selection maintaining sterility cytoplasms in the gynodioecious species. We found no difference between the species for nuclear gene diversity, but, for the cytoplasmic loci, the gynodioecious S. nutans had more haplotypes, and higher nucleotide diversity, than the dioecious relative, S. otites, even though the latter has a relatively high rate of mitochondrial synonymous substitutions, and therefore presumably a higher mutation rate. Therefore, as the mitochondrial mutation rate cannot account for the higher cytoplasmic diversity found in S. nutans, our findings support the hypothesis that gynodioecy in S. nutans has been maintained by balancing selection rather than by epidemic-like dynamics.

Lineages ofSilene nutansdeveloped rapid, strong, asymmetric postzygotic reproductive isolation in allopatry

“…This breeding system gives rise to genomic conflict between cytoplasmic male sterility factors and nuclear restorers of fertility (Saumitou-Laprade et al 1994;Garraud et al 2011). Previous studies on S. nutans have suggested that gynodioecy is under balancing selection, thus enabling the maintenance of cytoplasmic genomes for a long period of time that could ultimately accumulate mutations genetically linked to the sterilizing gene (Touzet and Delph 2009;Lahiani et al 2013). But genetic incompatibilities should not be necessarily directly involved in male sterility.…”

“…An individual's assignment to W1 or E1 plastid groups was based on a combination of six plastid SNPs developed from the intergenic spacer sequences psbA-trnH and the matK gene fragment of S. nutans representative samples (Lahiani et al 2013) and described in Martin et al (2016). An individual's assignment to W1 or E1 plastid groups was based on a combination of six plastid SNPs developed from the intergenic spacer sequences psbA-trnH and the matK gene fragment of S. nutans representative samples (Lahiani et al 2013) and described in Martin et al (2016).…”

On the importance of balancing selection in plants

“…A recent comparison of sequence variability between these three genomes in S. nutans and a closely related dioecious species, S. otites , found more haplotypes and more nucleotide diversity in the two cytoplasmic genomes of the gynodioecious species, but no difference for nuclear gene diversity between the species (Lahiani et al ., 2013). This result was found in spite of a likely higher rate of mitochondrial mutations in the dioecious species, discounting mutation rate differences as being responsible, and supporting the conclusion that balancing selection was operating.…”

Phylogeographic pattern of range expansion provides evidence for cryptic species lineages in Silene nutans in Western Europe

“…Plastid diversity was investigated using SNPs recently developed from plastid sequences (pDNA) of S. nutans representative samples (Lahiani et al, 2013). Plastid SNPs were defined based on six polymorphic pDNA nucleotides in the intergenic spacer sequences psbA-trnH, named Cp 42, and the matK gene fragment, named Cp 397, Cp 540, Cp 656, Cp 730 and Cp 804.…”