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Independent origins and horizontal transfer of bacterial symbionts of aphids

Authors

  • Jonas P. Sandström,

    1. Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721, USA
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      Present address: Department of Evolutionary Biology, Uppsala University, Norbyvägen 18 C, SE-752 36 Uppsala Sweden.

  • Jacob A. Russell,

    1. Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721, USA
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  • Joshua P. White,

    1. Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721, USA
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  • Nancy A. Moran

    Corresponding author
    1. Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721, USA
      Nancy A. Moran. Fax: +520–621–9190; E-mail:nmoran@u.arizona.edu
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Nancy A. Moran. Fax: +520–621–9190; E-mail:nmoran@u.arizona.edu

Abstract

Many insect groups have obligate associations with primary endosymbionts: mutualistic bacteria that are maternally transmitted and derived from an ancient infection. Often, the same insects are hosts to ‘secondary’ bacterial symbionts which are maternally transmitted but relatively labile within host lineages. To explore the dynamics of secondary symbiont associations in aphids, we characterized bacteria infecting 15 species of macrosiphine aphids using DNA sequencing, diagnostic polymerase chain reaction (PCR), diagnostic restriction digests, phylogenetic analyses, and electron microscopy to examine aphids from nature and from laboratory colonies. Three types of bacteria besides Buchnera were found repeatedly; all three fall within the Enterobacteriaceae. The R-type has a 16S rDNA less than 0.1% different from that of the secondary symbiont previously reported from Acyrthosiphon pisum and is related to Serratia species. The T-type includes a symbiont previously reported from a whitefly; the U-type comprises a new cluster near the T-type. The T-type was found in every one of 40 Uroleucon ambrosiae clones collected throughout the United States. In contrast, A. pisum individuals were infected by any combination of the three symbiont types. Secondary symbionts were maternally transmitted for 11 months within laboratory-reared A. pisum clones and were present in sexually produced eggs. PCR screens for a bacteriophage, APSE-1, indicated its presence in both A. pisum and U. ambrosiae containing secondary symbionts. Electron microscopy of R-type and T-type bacteria in A. pisum and in U. ambrosiae revealed rod-shaped organisms that attain extremely high densities within a few bacteriocytes.

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