Phylogeographic support for horizontal gene transfer involving sympatric bruchid species

<br><b>Background</b><br> We report on the probable horizontal transfer of a mitochondrial gene, <i>cytb</i>, between species of Neotropical bruchid beetles, in a zone where these species are sympatric. <br> The bruchid beetles <i>Acanthoscelides obtectus</i>, <i>A. obvelatus</i>, <i>A. argillaceus</i> and <i>Zabrotes subfasciatus</i> develop on various bean species in Mexico. Whereas <i>A. obtectus</i> and <i>A. obvelatus</i> develop on <i>Phaseolus vulgaris</i> in the Mexican Altiplano, <i>A. argillaceus</i> feeds on <i>P. lunatus</i> in the Pacific coast. The generalist <i>Z. subfasciatus</i> feeds on both bean species, and is sympatric with <i>A. obtectus</i> and <i>A. obvelatus</i> in the Mexican Altiplano, and with <i>A. argillaceus</i> in the Pacific coast. In order to assess the phylogenetic position of these four species, we amplified and sequenced one nuclear (<i>28S rRNA</i>) and two mitochondrial (<i>cytb, COI</i>) genes. <br><b>Results</b><br> Whereas species were well segregated in topologies obtained for <i>COI</i> and <i>28S rRNA</i>, an unexpected pattern was obtained in the <i>cytb</i> phylogenetic tree. In this tree, individuals from <i>A. obtectus</i> and <i>A. obvelatus</i>, as well as <i>Z. subfasciatus</i> individuals from the Mexican Altiplano, clustered together in a unique little variable monophyletic unit. In contrast, <i>A. argillaceus</i> and <i>Z. subfasciatus</i> individuals from the Pacific coast clustered in two separated clades, identically to the pattern obtained for <i>COI</i> and <i>28S rRNA</i>. An additional analysis showed that <i>Z. subfasciatus</i> individuals from the Mexican Altiplano also possessed the <i>cytb</i> gene present in individuals of this species from the Pacific coast. <i>Zabrotes subfasciatus</i> individuals from the Mexican Altiplano thus demonstrated two <i>cytb</i> genes, an "original" one and an "infectious" one, showing 25% of nucleotide divergence. The "infectious" <i>cytb</i> gene seems to be under purifying selection and to be expressed in mitochondria. <br><b>Conclusion</b><br> The high degree of incongruence of the <i>cytb</i> tree with patterns for other genes is discussed in the light of three hypotheses: experimental contamination, hybridization, and pseudogenisation. However, none of these seem able to explain the patterns observed. A fourth hypothesis, involving recent horizontal gene transfer (HGT) between <i>A. obtectus</i> and <i>A. obvelatus</i>, and from one of these species to <i>Z. subfasciatus</i> in the Mexican Altiplano, seems the only plausible explanation. The HGT between our study species seems to have occurred recently, and only in a zone where the three beetles are sympatric and share common host plants. This suggests that transfer could have been effected by some external vector such as a eukaryotic or viral parasite, which might still host the transferred fragment. <br><b>Reviewers</b><br> This article was reviewed by Eric Bapteste, Adam Eyre-Walker and Alexey Kondrashov.