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extracellular. This compartmentalization may act as an obstacle to gene transfer from symbiont to host because persistent gene transfer can only occur in germ line cells.

HEREDITARY SYMBIOSIS IN ANIMALS

Before molecular methods were available, Paul Buchner and his students conducted extensive surveys of specialized symbiosis in animals; this work was summarized in a book translated into English in 1965 (Buchner, 1965). Because symbionts are mostly noncultivable under typical laboratory conditions, the approaches of Buchner and his coworkers relied primarily on microscopy to trace the diversity of associations with microbes found in different invertebrate groups, with particular attention to insects. Buchner’s central theses included the idea that symbiotic microorganisms shared long evolutionary histories with their host clades and also the premise that the main role of animal symbionts was to provide nutrients to hosts that used deficient diets. The bulk of his work was devoted to describing the complex developmental adaptations that have allowed hosts to maintain stable associations.

Of all of the groups that Buchner studied, he devoted most attention to the sap-feeding insects, some of which possess unusually elaborate symbiotic systems involving multiple microbes. This group of insects serves as an exemplar of the remarkable complexity and variety that can arise in the context of evolving symbioses. One basis of the abundance of symbiotic interactions in this group is the poor diet of most species: plant phloem sap and xylem sap are both particularly unbalanced nutritionally, lacking essential amino acids, and, in the case of xylem sap, vitamins and carbohydrates. Thus, a phloem sap- or xylem sap-feeding animal, while enjoying the advantage of a constant food supply, must collaborate with a microbial symbiont able to synthesize missing nutrients from precursors that are available.

The group of insects that includes cicadas, treehoppers, planthoppers, leafhoppers, and spittlebugs, corresponding to the suborder Auchenorrhyncha in the order Hemiptera, shows a remarkable diversity of symbiotic associations. Buchner referred to this group as “the fairy land of symbiosis,” and his student H. J. Müller studied hundreds of auchenorrhynchan species in attempting to reconstruct the evolution of this bewildering diversity of associations (summarized in Buchner, 1965). Individual insects can possess up to six symbiont types, with each symbiont transferred from mother to progeny and packaged during development by means of specialized mechanisms.

Molecular phylogenetic studies have greatly extended our understanding of the origins and evolution of animal symbioses, validating and



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