Academic journal article Genetics

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

Academic journal article Genetics

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

Article excerpt

ABSTRACT

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.

CHLOROPLAST 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 thespecies.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). Thismay 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 purposesmay 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 closely related and can form viable and fertile hybrids (except S. latifolia × S. diclinis crosses that rarely produce seeds; Prentice 1978) and are known to have cytologically distinguishable sex chromosomes. The range of S. latifolia in Eurasia stretches from Britain and Scandinavia down to northern Morocco reaching as far as the Black Sea to the south and Lake Baikal in the east (Baker 1947). S. dioica occurs throughout northern Europe, where its natural range broadly overlaps that of S. latifolia. S. heuffelii occurs in the northern Balkan region and the Carpathian Mountains at altitudes >700-800 m while S. marizii has an extremely disjunct distribution, occurring in central Spain and northern Portugal. S. diclinis is an endemic species, occupying an extremely restricted geographical range surrounding the town of Xativa in the Spanish province of Valencia (Prentice 1976).

The earlier studies of allozyme (Mastenbroek et al. …

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