The significance of molecular phylogenetics for insect symbiont research

Investigation into prokaryote evolution is one of the areas of biology most deeply affected by the advent of molecular phylogenetics (Pace, 1997) . In the field of insect-bacteria symbiosis, this new approach not only generated an immense amount of knowledge, but also fundamentally changed the whole framework of this field: bacterial symbionts are now mostly viewed and analyzed in terms of phylogenetic lineages. This situation contrasts with the premolecular era, when morphological and functional characterization provided the only base for symbiont classification . Until the late 1980s, studies on insect bacterial symbionts were either purely descriptive or focused on functional rather than evolutionary aspects (Buchner, 1965; Hill and Campbell, 1973; Griffiths and Beck,

1974; Nogge, 1978; Ishikawa, 1982; Eberle and McLean, 1983); when tackling evolutionary issues at all, they were largely speculative and could rely on only indirect evidence (Buchner, 1965) . The new phylogeny-based way of looking at the symbionts allowed for addressing many previously inapproachable issues, such as the origin of various symbiotic lineages in frame of the whole prokaryote diversity, degree of vertical versus horizontal transfers, or continuous acquisitions and losses of various symbiotic lineages by their hosts On the other hand, this new approach introduced into the symbiosis field a variety of methodological problems related to the intricacy of phylogenetic inference and coevolutionary reconstructions

Within less than two decades, a substantial number of analyses have been performed and published From a formal point of view, this process resulted in identification and taxonomic description of many symbiotic lineages (Table 1 1) More importantly, several interesting patterns began to emerge from the accumulated data In Figure 1 1, we provide a rough picture of insect-symbiont diversity mapped onto a phylogenetic background Because there is little agreement on the overall phylogenetic arrangement of bacterial symbionts, this topology is meant as a reference scheme for the following discussions rather than as an attempt to achieve consensus of the current views Despite the high degree of uncertainty and subjectivity, it demonstrates several important facts At broad phylogenetic scale, the expected polyphyly of bacterial symbionts was well established It is now clear that symbiotic lineages have originated multiple times within many groups of prokaryotes On the other hand, hot spots giving rise to multiple symbiotic lineages can be identified within some taxa For example, many of the major symbiotic lineages seem to stem from a particularly prominent spot within y-Proteobac-teria (the node P in Figure 1 1) This issue, however, remains highly controversial and will be discussed later

Another outcome of phylogenetic studies is the apparent versatility of bacterial lineages . Closely related bacteria can rapidly evolve into a highly specialized mutualist as well as parasites/commensals loosely associated with their hosts (nodes P, A, and S in Figure 1 .1 show such diverse groups) . This versatility has even been experimentally demonstrated by functional replacement of obligate long-established mutualists with other symbiotic bacteria (Koga et al , 2003) Several recent studies indicate that at least some of the symbiotic lineages previously believed to have originated by only a single and unique transition from a free-living bacterium to symbiosis, may in fact represent abundant and widely distributed symbionts (e .g., the genera Sodalis and Arsenophonus). An increasing tempo of identification and characterization of new symbiotic lineages will certainly lead to an even more complex picture and therefore higher demands on coevolutionary reconstruction and its evolutionary interpretation Consequently, the methods originally restricted to parasito-logical research, such as tree-based and data-based coevolutionary reconstructions, have begun to penetrate the field of symbiosis

In this chapter, we highlight the main questions and methodological problems that arose from the current view on insect-bacteria symbiosis In the first section, we show that the phylogenetic information accumulated during the last years of molecular research has changed some of the previous conceptions of the field and puts insect-bacteria symbiosis into an entirely new perspective . In this context, we highlight the importance of unprejudiced and rigorous interpretation of phylogenetic relationships for evolutionary inferences In the following sections, we focus on two major methodological problems, namely, the inference of phylogenetic signal from degenerated symbiotic genomes and the reconstruction of coevolutionary history between insects and their symbionts

Table 1.1 List of Symbiotic Bacteria Included in the Tree in Figure 1. 1 Taxon Designation Classification Host References

Arsenophonus sp.

Baumannia cicadellinicola

Bemisia tabaci* Blochmania sp.

Gamma

Gamma

Gamma

Gamma

Buchnera aphidicola Gamma Carsonella ruddii Gamma

Cimex lectularius* Gamma Columbicola columbae* Gamma

Craterina malbae* Gamma

Euscilidius variegatus* Gamma

Hamiltonella defensa Gamma

Hematomizus Gamma elephantis*

Hematopinus sp.* Gamma

Ishikawaella Gamma capsulata

Mealybugs A* Gamma

Mealybugs C Gamma

Mealybugs D* Gamma

Mealybugs E* Gamma

Nardonella Gamma

Polyplax sp.* Gamma

Portiera Gamma aleyrodidarum

Pseudolynchia Gamma canariensis*

Various arthropods

Various spp . of sharpshooters

Various spp . of carpenter ants

Aphids

Psyllids

Various spp . of aphids and psyllids

Various spp . of stinkbugs

Various spp . of mealybugs

Various spp of mealybugs

Various spp of mealybugs

Various spp of mealybugs

Various spp of weevils **

Whiteflies

(Gherna et al ., 1991; Hypsa and Dale, 1997; Thao and Baumann, 2004b)

(Zchori-Fein and Brown, 2002)

(Spaulding and von Dohlen, 1998; Clark et al . , 2001; Nakabachi et al . , 2006)

(Hypsa and Aksoy, 1997)

(Campbell and Purcell, 1993)

(Hypsa and KrĂ­zek, 2007) (Thao and Baumann, 2004a)

Continued.

Table 1.1 List of Symbiotic Bacteria Included in the Tree in Figure 1. 1 (Continued) Taxon Designation Classification Host References

Psyllids 1*

Psyllids 2*

Regiella insecticola Riesia pediculicola Serratia symbiotica Sitophilus sp.*

Sodalis glossinidius

Trichobius sp.*

Weevils*

Wigglesworthia glossinidia

Asaia sp.

Bartonella sp.

Diaphorina citri A*

Rickettsia sp.

Wolbachia pipientis

Diaphorina citri B* Tremblaya princeps

Adonia variegata*

Blattabacterium cuenoti

Cardinium sp.

Coleomegilla maculata* Cryptococcus ulmi* Icerya sp.* Sulcia muelleri

Gamma

Gamma

Gamma Gamma Gamma Gamma Gamma

Gamma

Gamma

Gamma

Alpha Alpha Alpha Alpha

Alpha

Beta Beta

Bacteroidetes Bacteroidetes

Bacteroidetes

Bacteroidetes Bacteroidetes Bacteroidetes Bacteroidetes

Various spp . of psyllids

Various spp . of psyllids

Various spp of aphids Primate lice

Various spp of aphids **

Glossina sp.

Various spp of bat flies

Various spp of weevils

Glossina sp.

Anopheles stephensi

Various insect species **

Various arthropods

Various arthropods and nematodes **

Mealybugs **

Various spp of cockroaches and termites

Various arthropods

Various spp of cicadas, leafhoppers, spittlebugs, treehoppers

(Dale and Maudlin, 1999; Dale et al ., 2001; Toh et al ., 2006)

(Subandiyah et al , 2000)

(Zchori-Fein and Perlman, 2004; Marzorati et al ., 2006)

(Hurst et al ., 1997) (Gruwell et al ., 2007) (Gruwell et al ., 2007) (Moran et al , 2005b)

Continued .

Table 1.1 List of Symbiotic Bacteria Included in the Tree in Figure 1. 1 (Continued)

Taxon Designation Classification Host References

Uzinura diaspidicola Bacteroidetes Various spp . of (Gruwell et al ., 2007)

armored scale insects

Zigia versicolor* Bacteroidetes ** (Zchori-Fein and Perlman,

2004)

Spiroplasma sp. Firmicutes Various arthropods (Tsuchida et al ., 2006)

Note: P-symbionts are printed in bold. The alpha, beta, and gamma terms stand for individual subdivisions of Proteobacteria . As in Figure 1. 1, the taxa are designated by either the names of symbiotic bacteria or those of the host taxa labeled with an asterisk . For the latter case, asterisks are used within the Host column instead of repeating the host name

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