Linkage disequilibrium and phylogenetic congruence between chloroplast and mitochondrial haplotypes inSilene vulgaris

Abstract

Both the chloroplast and mitochondrial genomes are used extensively in studies of plant population genetics and systematics. In the majority of angiosperms, the chloroplast DNA (cpDNA) and mitochondrial DNA (mtDNA) are each primarily transmitted maternally, but rare biparental transmission is possible. The extent to which the cpDNA and mtDNA are in linkage disequilibrium is argued to be dependent on the ¢delity of co-transmission and the population structure. This study reports complete linkage disequilibrium between cpDNA and mtDNA haplotypes in 86 individuals from 17 populations of Silene vulgaris, a gynodioecious plant species. Phylogenetic analysis of cpDNA and mtDNA haplotypes within 14 individuals supports a hypothesis that the evolutionary histories of the chloroplasts and mitochondria are congruent within S. vulgaris, as might be expected if this association persists for long periods. This provides the ¢rst documentation of the evolutionary consequences of long-term associations between chloroplast and mitochondrial genomes within a species. Factors that contribute to the phylogenetic and linkage associations, as well as the potential for intergenomic hitchhiking resulting from selection on genes in one organellar genome are discussed.

Mathematical Consequences of the Genealogical Species Concept

“…In Drosophila simulans, for example, the genealogy of mtDNA reflects the spread of Wolbachia rather than the relatedness of populations as assessed by nuclear DNA (Ballard et al 2002). Similarly, cytoplasmic male sterility in plants can be caused by genes in mitochondria, and can spread rapidly via selection, dragging both mitochondrial and chloroplast genes along with it (Olson and McCauley 2000).…”

Nonneutral Evolution of Organelle Genes in Silene vulgaris

“…Strict co-inheritance of genomes is expected to generate congruent phylogenetic histories between genes in different genomes, whereas the absence of congruence implies at least somewhat independent histories (Desplanque et al 2000;Olson and McCauley 2000). Pairwise partition-homogeneity tests (Farris et al 1994) indicated incongruence between the pairwise histories of matK and atp1 (P ¼ 0.003), matK and atp9 (P ¼ 0.001), and atp1 and atp9 (P ¼ 0.001).…”

“…However, studies of species wherein multiple CMS genes have been identified have shown that CMS variants are not allelic, but rather each is constructed from different sets of genes to create a novel chimeric open reading frame (Schnable and Wise 1998). Nonetheless, some researchers have posited that since the mitochondrial genome is inherited as a single linkage unit and the chloroplast and mitochondria are co-inherited, these genomes may harbor signals of past balancing selection or epidemics via hitchhiking (Olson and McCauley 2000;Ingvarsson and Taylor 2002;Cho et al 2004). …”

“…With rare exceptions (Reboud and Zeyl 1994), the mitochondria and chloroplast in angiosperms are thought to be primarily maternally inherited (Birky 2001;McCauley et al 2005). Phylogenetic patterns among co-inherited genes or genomes are expected to be congruent, due to a process akin to linkage disequilibrium (Olson and McCauley 2000). The absence of such congruence implies independent transmission histories perhaps resulting from horizontal transfer (Bergthorsson et al 2003) or paternal leakage , producing heteroplasmic individuals.…”

“…As heteroplasmy is a necessary precondition for recombination among divergent genes or genomes, the presence of recombination within or among cytoplasmic genomes not only indicates that cytoplasmic genes may have the potential to evolve as independent units, but also indicates that transmission dynamics may be much less constrained than previous studies have indicated. S. vulgaris is an excellent candidate for better understanding the mitochondrial and chloroplast evolution as previous studies have identified high levels of mitochondrial polymorphism within small populations (Olson and McCauley 2000;Štorchová and Olson 2004), and small samples have indicated that sequence diversity at coding regions may also be elevated relative to that in other taxa .…”