Indirect evidence from DNA sequence diversity for genetic degeneration of the Y‐chromosome in dioecious species of the plant Silene: the SlY4/SlX4 and DD44‐X/DD44‐Y gene pairs

Laporte, Valérie; Filatov, Dmitry A.; Kamau, Esther; Charlesworth, Deborah

doi:10.1111/j.1420-9101.2004.00833.x

Cited by 31 publications

(49 citation statements)

References 41 publications

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“…Indeed, Tajima's D (Tajima 1989) is consistently negative across each 1 of the 3 chloroplast genes, and neutrality can be rejected at the 5% level in Elisanthe and S. latifolia matK and joint matK and trnTLF data sets, as well as for Elisanthe rbcL, demonstrating an excess of low-frequency polymorphisms and indicating either a selective sweep in the chloroplast or population expansion. These results contrast with those observed for Y-linked genes, where high-frequency polymorphisms are in significant excess, with X-linked genes (Filatov et al 2000(Filatov et al , 2001Ironside and Filatov 2005;Laporte et al 2005) and with the autosomal Slop gene, where no significant frequency spectrum bias was detected in either of the species. These observations suggest that a demographic scenario is unlikely, as demographic processes are expected to affect all genes across all genomes.…”

Section: Dna Polymorphism In Silene Cpdna Andcontrasting

confidence: 55%

“…The frequency spectrum bias toward rare polymorphisms can be caused either by a population expansion or a selective sweep in the chloroplast genome. However, for the autosomal Slop gene Tajima's D is not significantly negative in either of the species and no bias toward rare polymorphisms was detected in S. latifolia Yor X-linked genes (Filatov et al 2000(Filatov et al , 2001Ironside and Filatov 2005;Laporte et al 2005), suggesting that a selective sweep scenario is a more likely explanation for the patterns observed in the chloroplast. The rate of loss of bias in the frequency spectrum depends on the effective population size, with larger populations taking longer to return to equilibrium (e.g., Przeworski 2002).…”

Section: Dna Polymorphism In Silene Cpdna Andmentioning

confidence: 87%

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A Selective Sweep in the Chloroplast DNA of Dioecious Silene (SectionElisanthe)

Muir

Filatov

2007

Genetics

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Gene flow occurs predominantly via pollen in angiosperms, leading to stronger population subdivision for maternally inherited markers, relative to paternally or biparentally inherited genes. In contrast to this trend, population subdivision within Silene latifolia and S. dioica, as well as subdivision between the two species, is substantially lower in maternally inherited chloroplast genes compared to paternally inherited Y-linked genes. A significant frequency spectrum bias toward rare polymorphisms and a significant loss of polymorphism in chloroplast genes compared to Y-linked and autosomal genes suggest that intra-and inter-specific subdivision in the chloroplast DNA may have been eroded by a selective sweep that has crossed the S. latifolia and S. dioica species boundary. C HLOROPLAST DNA (cpDNA) is widely used in studies of plant phylogeography. Often such studies do not use any additional data from nuclear genes (e.g., Taylor and Keller 2007) and thus implicitly or explicitly assume that the gene tree of chloroplast sequences reflects the history and population dynamics of the species. However, non-neutrality in chloroplast genes may significantly affect the tree structure and bias the inferences of biogeographic studies based on cpDNAlinked polymorphisms. The chloroplast genome includes many genes that may have a direct effect on plant growth. For example, the chloroplast gene rbcL that is often used in plant systematics encodes a large subunit of the RUBISCO enzyme that is a critical component of photosynthesis and one of the limiting steps in plant growth (Spreitzer and Salvucci 2002). It was recently demonstrated that positive selection in rbcL is fairly widespread in terrestrial plants (Kapralov and Filatov 2007). The spread of adaptive mutations in rbcL or any other chloroplast gene will affect the distribution of polymorphisms all over the chloroplast genome and may result in a strong bias for phylogeographic studies based only on cpDNA. Moreover, adaptive cytotypes may spread across several hybridizing species (e.g., Tsitrone et al. 2003; Seehausen 2004). This may create incongruencies between chloroplast-based phylogenies and the 'true' species phylogeny. For example, adaptive selection in the RUBISCO enzyme in the Hawaiian endemic genus Schiedea may have driven the spread and fixation of adaptive cytotypes in several Schiedea species inhabiting the same island of the archipelago. This in turn created a strong incongruence between the chloroplast gene tree and the phylogeny of the genus (Kapralov and Filatov 2006). Thus, using only chloroplast DNA for phylogenetic and phylogeographic purposes may be misleading.Here we report a study of a selective sweep in chloroplast DNA across the range of two dioecious Silene species, Silene latifolia and S. dioica (Caryophyllaceae). These two species are closely related and belong to a small cluster of dioecious Silene species (section Elisanthe), which includes S. latifolia, S. dioica, S. heuffelii, S. diclinis, and S. marizii. All these species are ...

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Section: Dna Polymorphism In Silene Cpdna Andcontrasting

confidence: 55%

Section: Dna Polymorphism In Silene Cpdna Andmentioning

confidence: 87%

A Selective Sweep in the Chloroplast DNA of Dioecious Silene (SectionElisanthe)

Muir

Filatov

2007

Genetics

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“…In addition, the diversity data were compared with published estimates from four other sex-linked genes, SlXY1 and SlXY4 and SlDD44 (Ironside & Filatov 2005;Laporte et al 2005), which used smaller samples of European S. latifolia, and SlSs (Filatov 2008), which used samples similar to those used here.…”

Section: (D) Sequence Analysesmentioning

confidence: 99%

“…Support for predictions that selection during the evolution of Y chromosomes will lower the effective population size (N e ) for Y-linked genes , beyond the effect of the lower numbers of Y chromosomes than X chromosomes in populations, has been the finding that several Y-linked genes in S. latifolia have low diversity, compared with the homologous X-linked genes (Filatov et al 2000Ironside & Filatov 2005;Laporte et al 2005). In nonrecombining Y chromosome regions, selection will reduce N e through hitch-hiking processes, including selective sweeps during the spread of advantageous alleles (causing selective sweeps that would lower diversity at linked silent sites, e.g.…”

Section: Introductionmentioning

confidence: 99%

Nucleotide diversity inSilene latifoliaautosomal and sex-linked genes

et al. 2010

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The plant Silene latifolia has separate sexes and sex chromosomes, and is of interest for studying the early stages of sex chromosome evolution, especially the evolution of non-recombining regions on the Y chromosome. Hitch-hiking processes associated with ongoing genetic degeneration of the nonrecombining Y chromosome are predicted to reduce Y-linked genes' effective population sizes, and S. latifolia Y-linked genes indeed have lower diversity than X-linked ones. We tested whether this represents a true diversity reduction on the Y, versus the alternative possibility, elevated diversity at X-linked genes, by collecting new data on nucleotide diversity for autosomal genes, which had previously been little studied. We find clear evidence that Y-linked genes have reduced diversity. However, another alternative explanation for a low Yeffective size is a high variance in male reproductive success. Autosomal genes should then also have lower diversity than expected, relative to the X, but this is not found in our loci. Taking into account the higher mutation rate of Y-linked genes, their low sequence diversity indicates a strong effect of within-population hitch-hiking on the Y chromosome.

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“…The distribution of FISH signal in the dioecious species is very similar to that in S. latifolia: the probe paints the autosomes and the X chromosome, but leaves the majority of the Y chromosome ''unpainted'' (Figure 1, c and d). These species are very closely related and are likely to have separated within the last 1-2 million years, since nuclear DNA divergence at silent sites does not exceed 2% (Ironside and Filatov 2005;Laporte et al 2005;Muir and Filatov 2007). Therefore, this result is not entirely unexpected.…”

mentioning

confidence: 99%