Wolbachia Associations with Insects: Winning or Losing Against a Master Manipulator

Abstract

Wolbachia are intracellular, maternally inherited bacteria with an impressive history of adaptation to intracellular lifestyles. Instead of adapting to a single host lineage, Wolbachia evolved ways to jump across host species and establish relatively stable associations maintained through vertical transmission. Wolbachia are capable of manipulating the reproduction of infected hosts in a remarkable way. Traditionally, such reproductive manipulations have been regarded as the general mechanism by which Wolbachia spread through host populations. Recent evidence suggests that Wolbachia-host interactions are more complex than previously thought and may be driven by the onset and resolution of conflicts of interest. Here, we discuss how reproductive manipulation phenotypes may be transient. As the host adapts to infection, manipulation phenotypes attenuate and the continuity of the symbioses may rely on the physiological advantages Wolbachia may confer to their host. For facultative symbionts, such benefits are likely to be dependent on the environment. Here, we also review evidence that supports the view of environment-dependent facultative mutualism as a stable evolutionary outcome of Wolbachia infections beside extinction and obligate symbioses. Finally, our current understanding of the biology of mitochondria and Wolbachia unravels remarkable parallels in the way they interact with the nuclear genome. Great insights into both the Wolbachia and mitochondrial research fields can be revealed if such fields are considered to be overlapping, rather than independent from each other.

Mosquito Microbiome Dynamics, a Background for Prevalence and Seasonality of West Nile Virus

“…This likely extends beyond Wolbachia , the dominant seasonal member in C. pipines/restuans , and current focus for disease mitigation against Flaviviruses (Dutra et al, 2016). Indeed, extended immunity provided directly by microbiota may be a trait under selection (Correa and Ballard, 2016; Faria et al, 2016), particularly if harboring pathogens has a fitness cost to the mosquitoes, as it does for WNV (Ciota et al, 2013). With increasing prevalence of mosquito-borne viruses there will be increased selection pressure on mosquitoes for symbiotic microbiota that increase resistance to viruses.…”

The evolution of the host microbiome as an ecosystem on a leash

“…Wolbachia can benefit the host by providing metabolites 82 , but it also impairs host reproduction. For example, Wolbachia kills male offspring of hosts in order to promote its transmission, which occurs cytoplasmically only through females 83 . Another example is the fungal parasite Ophiocordyceps unilateralis , which induces its ant host to climb into the forest canopy and bite down on a plant, whereupon the fungus kills the ant and makes a fruiting body to disperse its spores 84 (Fig.…”

Microbiome‐Germline Interactions and Their Transgenerational Implications

“…Since, we require the phenotype‐causing bacteria to influence somatic tissues (i.e., not influence the state and function of the germline), this mode is based primarily (if not exclusively) to bacteria that is not transferred through the germline. This would typically exclude germline‐residing endosymbiotic bacteria . Transmission of gut bacteria has been reported in diverse species, including human, potentially supporting inheritance of host phenotypes by a soma‐to‐soma transfer of bacterial influence.…”

“…This would typically exclude germline-residing endosymbiotic bacteria. [58][59][60] Transmission of gut bacteria has been reported in diverse species, including human, [61,62] potentially supporting inheritance of host phenotypes by a soma-to-soma transfer of bacterial influence. Note that this mode of inheritance does not necessarily require a change in the environment, because the contribution of bacteria to host phenotypes and functions is not limited to varying environments.…”