Distribution and transmission

Using the PCR-based identification techniques described above, facultative symbionts have been identified in a wide range of insects that often also harbor ancient obligate nutritional symbionts (Table 18 1) In almost all of the examples studied to date, the ancient obligate symbionts are found to evolve in strict concordance with their insect hosts This results from long-term matrilineal transmission—as a given insect group speciates, its symbiotic bacteria are carried into the descending lineages and generations Over evolutionary time, this leads to increased specialization and dependence for both partners in the symbiotic association At some point in time, the genomic and metabolic attributes of the symbiont become so highly specialized that it cannot "escape" and colonize a novel insect host

Not surprisingly, when we compare the phylogenetic trees of facultative symbionts and their insect hosts, there is often discordance Although we can find examples in which closely related facultative symbionts inhabit closely related insect hosts, further exploration often reveals that those symbionts have a more widespread distribution For example, almost identical strains of Sodalis glossinidius have been identified in five closely related tsetse species (Aksoy et al , 1997), but close relatives of these bacteria have also been identified in hippoboscid flies, grain weevils, and bird lice (Heddi et al ., 1998; Novakova and Hypsa, 2007; Fukatsu et al ., 2007). In other cases, closely related insect species are found to harbor a number of different facultative symbionts For example, aphids are known to harbor several distinct facultative symbionts from the family Enterobacteriaceae (Moran et al , 2005b) Finally, there are some examples of distantly related hosts that are known to harbor extremely very closely related symbionts For example, representatives of the candidate genus Arsenophonus (sharing c . 99% identity in 16S rRNA) have been identified in many different arthropods, including parasitoid wasps (Hymenoptera), triatomine bugs,

HOST TREE SYMBIONT TREE

Figure 18.1 Three conceptual scenarios illustrating evolutionary relationships between insect hosts and their symbiotic bacteria (A) Host and symbiont phylogenies show perfect congruence as a result of long-term cospeciation This relationship is expected in ancient associations involving obligate, maternally transmitted, nutritional symbionts (B) Partial congruence between host and symbiont phylogenies The symbiotic association is more recent in origin and there is evidence of horizontal symbiont transfer between distantly related insect hosts (illustrated by dotted line) (C) No congruence observed between host and symbiont phylogenies Symbionts have been horizontally transferred between all host species

Figure 18.1 Three conceptual scenarios illustrating evolutionary relationships between insect hosts and their symbiotic bacteria (A) Host and symbiont phylogenies show perfect congruence as a result of long-term cospeciation This relationship is expected in ancient associations involving obligate, maternally transmitted, nutritional symbionts (B) Partial congruence between host and symbiont phylogenies The symbiotic association is more recent in origin and there is evidence of horizontal symbiont transfer between distantly related insect hosts (illustrated by dotted line) (C) No congruence observed between host and symbiont phylogenies Symbionts have been horizontally transferred between all host species aphids, psyllids, whiteflies (Hemiptera), and ticks (Ixodida) (Gherna et al , 1991; Hypsa and Dale, 1997; Spaulding and von Dohlen, 2001; Grindle et al ., 2003; Thao and Baumann, 2004; Dale et al , 2006)

The apparent contrasts observed in the distribution profiles of facultative symbionts can readily be explained in the context of symbiont transmission Vertical (or maternal) transmission represents the predominant route by which facultative symbionts are transferred to the next generation The exact mechanism of vertical transmission varies according to the reproductive strategy of the host insect (sexual or parthenogenetic, viviparous or oviparous), but the general procedure involves the transfer of symbiotic bacteria from maternal reproductive structures into eggs, embryos, or larvae In the case of ancient, obligate symbionts, perfect vertical transmission over a long period of time gives rise to congruent host-symbiont phylogenies (Figure 18 .1A) . This occurs when an ancient symbiont infection event is followed by a period of host speciation—in the absence of horizontal transfer, the symbionts follow the same pattern of descent as their hosts . Facultative symbioses are typically more recent in origin, but it is not unprecedented for their phylogenies to demonstrate some degree of congruence . Often this limited level of congruence is coupled with evidence of horizontal symbiont transfer into more distantly related host lineages, as depicted in Figure 18 . 1B . More frequently however, the phylogenetic trees of facultative symbionts display little or no congruence in comparison with host trees (Figure 18 .1C). This is indicative of the recent acquisition of the symbiont by the insect host, and/or an increased frequency of horizontal transfer. Note that, over evolutionary time, only a very small number of horizontal transfer events are needed to abolish congruence between host and symbiont trees .

Several hypotheses have been proposed to explain the mechanics of horizontal symbiont transmission, but it seems likely that there is no single mechanism that accounts for this phenomenon in nature. One hypothesis states that facultative symbionts are horizontally transferred through host tissues during episodes of feeding (Darby et al., 2001) . An alternative hypothesis states that insect parasitoids (e .g., hymenopteran wasps) play a role in horizontal transmission, based on the observation that closely related facultative symbionts are found in parasitoids and their corresponding insect hosts (Hypsa and Dale, 1997; Russell et al ., 2003). Finally, in a recent study Moran and Dunbar (2006) provided experimental evidence of paternal symbiont transfer between aphids This mechanism of horizontal transmission could occur in any insect species that undertake sexual reproduction, regardless of diet, niche, or parasitism However, paternal transfer of symbionts is unlikely to account for the horizontal transmission of symbionts between distantly related insect species

The horizontal transmission of facultative symbionts is dependent upon the ability of these bacteria to infect naïve hosts—a characteristic that has likely been lost in ancient obligate symbionts Two lines of evidence indicate that facultative symbionts have the capability to colonize a (compatible) naïve host insect First, facultative symbionts have been successfully transferred from infected hosts into uninfected hosts by microinjection of symbiont-infected hemolymph (Oliver et al ., 2003; Russell and Moran, 2005, 2006) . Second, cultured recombinant strains of S. glossinidius have been microinjected into tsetse flies and found to be maintained in subsequent host generations (Dale et al ., 2001; Weiss et al ., 2006). Interestingly, these studies have also identified a number of genes that symbionts use to facilitate host cell invasion (Dale et al , 2001, 2005; Moran et al , 2005a)

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