Independent origins and horizontal transfer of bacterial symbionts of aphids

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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 besidesBuchnerawere 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 fromAcyrthosiphon pisumand is related toSerratiaspecies. 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 40Uroleucon ambrosiaeclones collected throughout the United States. In contrast,A. pisumindividuals were infected by any combination of the three symbiont types. Secondary symbionts were maternally transmitted for 11 months within laboratory‐rearedA. pisumclones and were present in sexually produced eggs. PCR screens for a bacteriophage, APSE‐1, indicated its presence in bothA. pisumandU. ambrosiaecontaining secondary symbionts. Electron microscopy of R‐type and T‐type bacteria inA. pisumand inU. ambrosiaerevealed rod‐shaped organisms that attain extremely high densities within a few bacteriocytes.

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