An Ancient Mitochondrial Polymorphism in Adalia bipunctata Linked to a Sex-Ratio-Distorting Bacterium

Abstract

Sex-ratio-distorting microbes are common parasites of arthropods. Although the reasons they have invaded and spread though populations are well understood, their subsequent dynamics within those populations are virtually unknown. We have found that different strains of a male-killing Rickettsia bacterium infecting the beetle Adalia bipunctata are associated with distinct mitochondrial haplotypes, which is expected as both the mitochondria and the bacteria are maternally transmitted. These mitochondrial haplotypes shared a common ancestor .2 million years ago, and their overall diversity is significantly greater than expected under neutrality from comparisons with a nuclear gene. Furthermore, a variety of statistical tests show strong deviations from neutrality in mitochondrial but not in nuclear genes. We therefore conclude that natural selection is probably maintaining a polymorphism of different Rickettsia strains in this species. Despite the age of the different mitochondrial haplotypes, there is very little genetic diversity within them. Furthermore, there is considerable variation in mitochondrial haplotype and bacterial strain frequency between populations, despite it being thought that this species has fairly low levels of population structure. We conclude that the fitness of these male killers may be negatively frequency dependent or different strains may be favored in different populations. These hypotheses await experimental confirmation.

How closely does genetic diversity in finite populations conform to predictions of neutral theory? Large deficits in regions of low recombination

“…For example, Drosophila recens infected with the maternally transmitted Wolbachia shows much lower mtDNA variation than predicted by neutrality, whereas the closely related uninfected Drosophila quinaria has more normal levels of mtDNA. Conversely, Adalia bipunctata is infected with three endosymbiont strains and has highly elevated mtDNA levels, overall, but very low mtDNA levels in beetles infected with a particular endosymbiont strain (Jiggins and Tinsley, 2005).…”

The Impact of Male-Killing Bacteria on Host Evolutionary Processes

“…One aspect that has attracted attention recently is the impact of male-killing infections on the hosts' population genetics. However, almost all studies conducted so far have focused on the population genetics of the mitochondrial genome, because of the obvious impact of disequilibrium with any other maternally inherited agents ( Johnstone and Hurst 1996;Schulenburg et al 2002;Jiggins 2003;Dyer and Jaenike 2004;Hurst and Jiggins 2005;Jiggins and Tinsley 2005). To our knowledge, there is only one study on the impact of male-killing bacteria on the population genetics of nuclear genes (Telschow et al 2006).…”

Comparative study of mtDNA in species of the genus Adalia (Coleoptera: Cocinellidae) and origin of ancient mitochondrial haplotypes in the gene pool of Adalia bipunctata

“…The mitochondrial haplotype H9, reported in populations of A. bipunctata in the northern part of Europe (Schulenburg et al, 2002;Jiggins & Tinsley, 2005), was found by us in St. Petersburg and Arkhangelsk (Fig. 2).…”

“…These mitochondrial haplotypes, H9 and H10, were considerably different from the other. An attempt to evaluate the time of divergence of the mitochondrial haplotype H10 by Jiggins & Tinsley (2005) gave an age of 2-2.5 million years. Consequently, this mitochondrial polymorphism is referred to as ancient.…”

“…Circles denote A. bipunctata and the coloured sectors in the pie diagrams correspond to mitochondrial haplotypes H1 (in H1 we include H1 and all other mitochondrial haplotypes, except H9 and H10), H9 and H10. Haplotypes recorded for Moscow (Russia) and Bielefeld (Germany) (Schulenburg et al, 2002) and Cambridge (England) (Schulenburg et al, 2002;Jiggins & Tinsley, 2005). Triangles mark the sites where A. frigida was collected, squares -A. tetraspilota, diamonds -A. decempunctata.…”