Extreme Population Structure and High Interspecific Divergence of the Silene Y Chromosome

Ironside, Joseph E.; Filatov, Dmitry A.

doi:10.1534/genetics.105.041210

Cited by 40 publications

(57 citation statements)

References 56 publications

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“…Gene introgression after hybridization between cross-compatible species is thus predicted to be lower for the Y chromosome than the X chromosome (and should be highest for the autosomes). Indeed, isolation between S. latifolia and S. dioica (assessed by F ST for DNA sequence variants in two genes), is significantly stronger on the non-recombining Y chromosome, compared with the recombining X chromosome, even taking into account the lower within-population variability of Y than X sequences (Ironside and Filatov, 2005).…”

Section: Reproductive Isolation and Species Boundariesmentioning

confidence: 99%

Silene as a model system in ecology and evolution

et al. 2009

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The genus Silene, studied by Darwin, Mendel and other early scientists, is re-emerging as a system for studying interrelated questions in ecology, evolution and developmental biology. These questions include sex chromosome evolution, epigenetic control of sex expression, genomic conflict and speciation. Its well-studied interactions with the pathogen Microbotryum has made Silene a model for the evolution and dynamics of disease in natural systems, and its interactions with herbivores have increased our understanding of multi-trophic ecological processes and the evolution of invasiveness. Molecular tools are now providing new approaches to many of these classical yet unresolved problems, and new progress is being made through combining phylogenetic, genomic and molecular evolutionary studies with ecological and phenotypic data. The model role of a non-model organismThe genus Silene (Caryophyllaceae), with a tradition of genetical and ecological studies dating back to Mendel and Darwin, has remarkably many interesting features. First, the species in the genus vary widely in their breeding systems and ecology. Second, several members of this mainly holarctic genus can be easily bred, and have short life cycles, and are thus convenient for experimental and field studies. Genomic resources are now becoming increasingly available in Silene, making genetic, quantitative genetic and molecular studies possible. A strength of Silene as a model system, compared with many classical model organisms, is that researchers can rely on a large number of ecological studies encompassing biotic interactions with sexually transmitted fungi, pollinators and herbivores. It is the wealth of ecological and other earlier knowledge that makes the genus Silene important for studying many biological questions, including the suppression of recombination during sex chromosome evolution, sexually antagonistic selection in an organism that is not an animal, epigenetic processes in flower development, speciation and reproductive isolation, multi-trophic interactions, disease ecology and biological invasions.Thanks to the classical genetic and ecological work on Silene, new progress can now be made in studying some of these important unresolved questions in biology with the aid of modern molecular tools. That new model systems with accessible and well-studied ecology open fruitful avenues for investigation is illustrated also by Mimulus (Wu et al., 2008) and the ongoing efforts to develop genomic resources in an increasing number of different systems. In the following, we outline the unique features of the Silene system, and describe active research areas and future directions, highlighting new advances and work in progress. Evolution of sexual systemsPlants show remarkable diversity in their sexual and mating systems, ranging from hermaphroditism to dioecy, from self-incompatible hermaphroditism to hermaphroditism in which individuals possess a capacity to self-fertilize, but which often show complex mechanisms to promote outcrossing (Darwin, 18...

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Section: Reproductive Isolation and Species Boundariesmentioning

confidence: 99%

Silene as a model system in ecology and evolution

et al. 2009

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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%

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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“…In structured populations, background selection reduces the DNA polymorphism within populations, but does not reduce between population differentiation (Charlesworth et al, 1997), leading to stronger population subdivision in non-recombining regions (for example, Ironside and Filatov, 2005)). This could negate the difference in the overall DNA polymorphism between recombining and non-recombining regions.…”

Section: Dna Polymorphismmentioning

confidence: 99%

DNA polymorphism in recombining and non-recombing mating-type-specific loci of the smut fungus Microbotryum

Votintseva

Filatov

2010

Heredity

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The population-genetic processes leading to the genetic degeneration of non-recombining regions have mainly been studied in animal and plant sex chromosomes. Here, we report population genetic analysis of the processes in the non-recombining mating-type-specific regions of the smut fungus Microbotryum violaceum. M. violaceum has A1 and A2 mating types, determined by mating-type-specific 'sex chromosomes' that contain 1-2 Mb long non-recombining regions. If genetic degeneration were occurring, then one would expect reduced DNA polymorphism in the non-recombining regions of this fungus. The analysis of DNA diversity among 19 M. violaceum strains, collected across Europe from Silene latifolia flowers, revealed that (i) DNA polymorphism is relatively low in all 20 studied loci (pB0.15%), (ii) it is not significantly different between the two mating-type-specific chromosomes nor between the non-recombining and recombining regions, (iii) there is substantial population structure in M. violaceum populations, which resembles that of its host species, S. latifolia, and (iv) there is significant linkage disequilibrium, suggesting that widespread selfing in this species results in a reduction of the effective recombination rate across the genome. We hypothesise that selfing-related reduction of recombination across the M. violaceum genome negates the difference in the level of DNA polymorphism between the recombining and non-recombining regions, and may possibly lead to similar levels of genetic degeneration in the mating-type-specific regions of the non-recombining 'sex chromosomes' and elsewhere in the genome.

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Extreme Population Structure and High Interspecific Divergence of the Silene Y Chromosome

Cited by 40 publications

References 56 publications

Silene as a model system in ecology and evolution

Silene as a model system in ecology and evolution

Nucleotide diversity inSilene latifoliaautosomal and sex-linked genes

DNA polymorphism in recombining and non-recombing mating-type-specific loci of the smut fungus Microbotryum

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