Abstract

BackgroundMaternally 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.ResultsMolecular 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.ConclusionsClonal 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.

Highlights

  • Inherited endosymbionts like Wolbachia pipientis are in linkage disequilibrium with the mtDNA of their hosts

  • Genetic variation estimates Three hundred and nine individuals from 38 different locations were screened for genetic variation in a 748 bp fragment of the Cytochrome Oxidase I (COI) gene

  • To investigate multiple infections within N. cervinus, we focused on 16 sampling sites, including weevils from both the “forest” and the “grassland” clades (Brazo Largo, Cerro Azul, Chajarí, El Palmar, Isla Talavera, Oberá, Pergamino, Río Cuarto, Salto Grande, Tandil and Yapeyú from Argentina, and Alegrete, Laranjeiras do Sul, Santa Maria, São Sepé and Toledo from Brazil, Figure 4)

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Summary

Introduction

Inherited endosymbionts like Wolbachia pipientis are in linkage disequilibrium with the mtDNA of their hosts. 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. Many cases have been reported in three different subfamilies: Scolytinae (bark beetles), Listroderinae and Entiminae (broad-nose weevils), especially in species from the Old World Apomixis was confirmed for several Old World broad-nosed weevils [3,10], nothing is known for South American species. The lack of meiosis could be detrimental in the short term [14,15,16], heterozygosity could explain the higher dispersion and adaptation ability of some parthenogenetic species over the sexual ones in the long term [1]

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