Insights into Wolbachia Obligatory Symbiosis - Insect Symbiosis - page 210

We believe that these cases could occur rapidly in the course of evolution, without the need
for long coevolution and sophisticated coadaptation between partners. Indeed, this mode of evolu-
tion is based on mutational events. Moreover, gene loss and genome degradation have often been
evoked to explain the total host dependence of several strictly intracellular bacteria. Indeed, genome-
size reduction was recently recognized to be a general phenomenon observed in many obligate
intracellular bacteria. The strict adaptation to a constant environment, such as that provided by the
cytoplasm of a eukaryotic cell, may allow the bacteria to abolish many of the adaptive responses
that are required by free-living bacteria and may also allow them to reduce their anabolic capacity
if they succeed in recruiting metabolic precursors from the host cellÔs metabolism. As a consequence
of the loss of essential characteristics, bacteria therefore become wholly dependent on their hosts
(Andersson and Kurland, 1998; Andersson and Andersson, 1999; Ochman and Moran, 2001).
Following the same principle, we believe that the reverse situation has occurred in parthenogenetic
wasps and A. tabida , where the hosts themselves have lost an essential function for their own
reproduction, thereby becoming wholly dependent on Wolbachia .
W OLBACHIA O BLIGATORY S YMBIOSIS : M UTUALISM OR T RICKERY ?
Is obligatory symbiosis mutualistic? This question has previously been underlined by Douglas and
Smith (1989). These authors do not believe that two interdependent symbiotic partners necessarily
form a mutualistic association, in the sense that each partner does not necessarily beneÝt from the
other. In numerous cases, it is accepted that the host beneÝts from the association by utilizing
products of its symbiont metabolism (essential nutrients in insects, photosynthetic activity in some
invertebrates, cellulose degradation in ruminants, etc.). However, there is little evidence that the
symbiont also beneÝts from its host. Some authors even argue that in certain cases the symbiont
could be considered Ña slave,Ò which produces some beneÝcial products for its ÑproslaverÒ host.
Why, therefore, are most symbionts strictly symbiotic and unable to survive in a free-living state?
From an evolutionary point of view, we can speculate that, at the beginning of the association, the
host would have developed some features to capture some ÑinterestingÒ free-living bacteria. In the
course of evolution, adaptations would have allowed the hosts to conserve their symbionts during
life and would also have acquired the ability to transmit them to offspring. In such a situation,
where the symbiont is now in a permanent relationship with its host, we could expect it to lose
metabolic capabilities, as mentioned in the above paragraph, becoming wholly dependent on its
host habitat. In this way, each partner is entirely dependent on the other. However, can we consider
this obligatory symbiosis mutualistic? The answer is evident if we consider the association at the
present time: each partner requires the presence of the other to survive. However, we can also
consider that only the host actually beneÝts from the association in the course of evolution. In other
words, Douglas and Smith (1989) described these associations as Ñslavery,Ò where the host captures
bacteria for its own beneÝt.
Can we expect such ÑslaveryÒ associations in obligatory Wolbachia symbiosis? This question is
not easy to answer. However, we can expect a possible unbalanced beneÝt between the two interde-
pendent protagonists, at least in insects. Indeed, while Wolbachia is believed to beneÝt from the
association, the existence of such beneÝt for the host remains uncertain. In parthenogenetic wasps,
the effect induced procures an evolutionary advantage for Wolbachia by accelerating the invasion of
host populations (Stouthamer, 1997). However, what is the advantage for the host to be obligatorily
linked with such bacteria? Does the host beneÝt from its asexual mode of reproduction? In A. tabida ,
the total dependence of host reproduction assures the maintenance of Wolbachia infection through
evolutionary times. However, what is the interest for females to be wholly Wolbachia dependent to
produce their eggs? Does this dependence confer better egg production, associated with a more
effective fecundity? Of course, we cannot exclude the possibility that Wolbachia provides other
metabolic capabilities that have thus far eluded detection. However, the highly speciÝc inhibition of
oogenesis in aposymbiotic A. tabida females makes this hypothesis unlikely.