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Mito-nuclear genetic comparison in a Wolbachia infected weevil: insights on reproductive mode, infection age and evolutionary forces shaping genetic variation.

Rodriguero MS, Lanteri AA, Confalonieri VA - BMC Evol. Biol. (2010)

Bottom Line: Our results demonstrate lack of recombination in the nuclear fragment, non-random association between nuclear and mitochondrial genomes and the consequent coevolution of both genomes, being an indirect evidence of apomixis.Wolbachia probably had great influence in shaping the genetic diversity of N. cervinus.However, it would have not caused the extinction of males, since sexual and asexual infected lineages coexisted until recent times.

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Affiliation: Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, 1428, Ciudad Autónoma de Buenos Aires, Provincia de Buenos Aires, Argentina. rodriguero@ege.fcen.uba.ar

ABSTRACT

Background: Maternally inherited endosymbionts like Wolbachia pipientis are in linkage disequilibrium with the mtDNA of their hosts. Therefore, they can induce selective sweeps, decreasing genetic diversity over many generations. This sex ratio distorter, that is involved in the origin of parthenogenesis and other reproductive alterations, infects the parthenogenetic weevil Naupactus cervinus, a serious pest of ornamental and fruit plants.

Results: Molecular evolution analyses of mitochondrial (COI) and nuclear (ITS1) sequences from 309 individuals of Naupactus cervinus sampled over a broad range of its geographical distribution were carried out. Our results demonstrate lack of recombination in the nuclear fragment, non-random association between nuclear and mitochondrial genomes and the consequent coevolution of both genomes, being an indirect evidence of apomixis. This weevil is infected by a single Wolbachia strain, which could have caused a moderate bottleneck in the invaded population which survived the initial infection.

Conclusions: Clonal reproduction and Wolbachia infection induce the coevolution of bacterial, mitochondrial and nuclear genomes. The time elapsed since the Wolbachia invasion would have erased the traces of the demographic crash in the mtDNA, being the nuclear genome the only one that retained the signal of the bottleneck. The amount of genetic change accumulated in the mtDNA and the high prevalence of Wolbachia in all populations of N. cervinus agree with the hypothesis of an ancient infection. Wolbachia probably had great influence in shaping the genetic diversity of N. cervinus. However, it would have not caused the extinction of males, since sexual and asexual infected lineages coexisted until recent times.

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Nuclear diversity. Cladogram of ITS1 haplotypes. Numbers above the branches are 50% or higher bootstrap values.
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Figure 2: Nuclear diversity. Cladogram of ITS1 haplotypes. Numbers above the branches are 50% or higher bootstrap values.

Mentions: Forty-four segregating sites were identified for ITS1 (only four singletons) yielding eight different nuclear haplotypes (arbitrarily named I-VIII [GenBank: GQ406818 - GQ406825]). Unlike COI, insertion/deletion events were frequent in this dataset. However, based on a gap insertion:substitution cost ratio 10:1, primary homologies could be unambiguously established. Nuclear haplotype distribution depicted a pattern similar to COI (e.g. haplotypes VI and VII are widely distributed, and haplotypes I, II and III are restricted to a single site, Table 1). The following values of genetic variability were obtained: θπ = 0.026 ± 0.001, θW = 0.013 ± 0.002 and Hd = 0.574 ± 0.028. The Hd value was remarkably lower than that obtained for COI, in agreement with the minor number of ITS1 haplotypes. Maximum parsimony search yielded one most parsimonious tree 153 steps long (Figure 2). In agreement with the mitochondrial dataset, two divergent clades were recovered: one from open vegetation areas ("grassland clade") and the other from forests ("forest clade"), although the later includes a single haplotype (VI) from the transition zone previously mentioned.


Mito-nuclear genetic comparison in a Wolbachia infected weevil: insights on reproductive mode, infection age and evolutionary forces shaping genetic variation.

Rodriguero MS, Lanteri AA, Confalonieri VA - BMC Evol. Biol. (2010)

Nuclear diversity. Cladogram of ITS1 haplotypes. Numbers above the branches are 50% or higher bootstrap values.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2992525&req=5

Figure 2: Nuclear diversity. Cladogram of ITS1 haplotypes. Numbers above the branches are 50% or higher bootstrap values.
Mentions: Forty-four segregating sites were identified for ITS1 (only four singletons) yielding eight different nuclear haplotypes (arbitrarily named I-VIII [GenBank: GQ406818 - GQ406825]). Unlike COI, insertion/deletion events were frequent in this dataset. However, based on a gap insertion:substitution cost ratio 10:1, primary homologies could be unambiguously established. Nuclear haplotype distribution depicted a pattern similar to COI (e.g. haplotypes VI and VII are widely distributed, and haplotypes I, II and III are restricted to a single site, Table 1). The following values of genetic variability were obtained: θπ = 0.026 ± 0.001, θW = 0.013 ± 0.002 and Hd = 0.574 ± 0.028. The Hd value was remarkably lower than that obtained for COI, in agreement with the minor number of ITS1 haplotypes. Maximum parsimony search yielded one most parsimonious tree 153 steps long (Figure 2). In agreement with the mitochondrial dataset, two divergent clades were recovered: one from open vegetation areas ("grassland clade") and the other from forests ("forest clade"), although the later includes a single haplotype (VI) from the transition zone previously mentioned.

Bottom Line: Our results demonstrate lack of recombination in the nuclear fragment, non-random association between nuclear and mitochondrial genomes and the consequent coevolution of both genomes, being an indirect evidence of apomixis.Wolbachia probably had great influence in shaping the genetic diversity of N. cervinus.However, it would have not caused the extinction of males, since sexual and asexual infected lineages coexisted until recent times.

View Article: PubMed Central - HTML - PubMed

Affiliation: Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, 1428, Ciudad Autónoma de Buenos Aires, Provincia de Buenos Aires, Argentina. rodriguero@ege.fcen.uba.ar

ABSTRACT

Background: Maternally inherited endosymbionts like Wolbachia pipientis are in linkage disequilibrium with the mtDNA of their hosts. Therefore, they can induce selective sweeps, decreasing genetic diversity over many generations. This sex ratio distorter, that is involved in the origin of parthenogenesis and other reproductive alterations, infects the parthenogenetic weevil Naupactus cervinus, a serious pest of ornamental and fruit plants.

Results: Molecular evolution analyses of mitochondrial (COI) and nuclear (ITS1) sequences from 309 individuals of Naupactus cervinus sampled over a broad range of its geographical distribution were carried out. Our results demonstrate lack of recombination in the nuclear fragment, non-random association between nuclear and mitochondrial genomes and the consequent coevolution of both genomes, being an indirect evidence of apomixis. This weevil is infected by a single Wolbachia strain, which could have caused a moderate bottleneck in the invaded population which survived the initial infection.

Conclusions: Clonal reproduction and Wolbachia infection induce the coevolution of bacterial, mitochondrial and nuclear genomes. The time elapsed since the Wolbachia invasion would have erased the traces of the demographic crash in the mtDNA, being the nuclear genome the only one that retained the signal of the bottleneck. The amount of genetic change accumulated in the mtDNA and the high prevalence of Wolbachia in all populations of N. cervinus agree with the hypothesis of an ancient infection. Wolbachia probably had great influence in shaping the genetic diversity of N. cervinus. However, it would have not caused the extinction of males, since sexual and asexual infected lineages coexisted until recent times.

Show MeSH
Related in: MedlinePlus