Abstract
A novel form of biological control is being applied to the dengue virus. The agent is the maternally transmitted bacterium Wolbachia, naturally absent from the main dengue vector, the mosquito Aedes aegypti. Three Wolbachia-based control strategies have been proposed. One is suppression of mosquito populations by large-scale releases of males incompatible with native females; this intervention requires ongoing releases. The other interventions transform wild mosquito populations with Wolbachia that spread via the frequency-dependent fitness advantage of Wolbachia-infected females; those interventions potentially require just a single, local release for area-wide disease control. One of these latter strategies uses Wolbachia that shortens mosquito life, indirectly preventing viral maturation/transmission. The other strategy uses Wolbachia that block viral transmission. All interventions can be undermined by viral, bacterial or mosquito evolution; viral virulence in humans may also evolve. We examine existing theory, experiments and comparative evidence to motivate predictions about evolutionary outcomes. (i) The life-shortening strategy seems the most likely to be thwarted by evolution. (ii) Mosquito suppression has a reasonable chance of working locally, at least in the short term, but long-term success over large areas is challenging. (iii) Dengue blocking faces strong selection for viral resistance but may well persist indefinitely at some level. Virulence evolution is not mathematically predictable, but comparative data provide no precedent for Wolbachia increasing dengue virulence. On balance, our analysis suggests that the considerable possible benefits of these technologies outweigh the known negatives, but the actual risk is largely unknown.
Highlights
Wolbachia is a maternally transmitted bacterial symbiont of many insects [1, 2] and has several unusual properties that make it suitable for novel approaches to biological control of vector-borne diseases [3,4,5]
What can we expect or predict about evolutionary responses to such a wide-scale intervention? Will dengue virus evolve to dodge the suppression? Will the virus evolve in ways that affect disease severity? How might Wolbachia be expected to evolve in this new host and how will the host evolve in response to this novel infection?
Wolbachia-bearing males No apparent standing variation for cytoplasmic incompatibility’ (CI) resistance in D. simulans Wild Drosophila have not evolved to suppress incompatibility in the short term but have in the long term; Hypolimnas bolina evolved to resist male killing within a century, whereas D. innubila has not Population suppression will likely remain effective over a decade or more; long-term success will be diminished by the combination of accidental releases of females from the suppressing strain, paternal transmission of Wolbachia, and evolution of mating discrimination
Summary
Evolutionary responses to life-shortening: a clear expectation of reduced impact. Selection in response to a life-shortening maternal symbiont is aligned for both the symbiont and its host (Table 1). Selection for Wolbachia to benefit their female carriers is supported by other observations: defending hosts against other microbes and the obligate or near-obligate symbioses observed in many taxa (e.g. filarial nematodes [41], the parasitic wasp Asobara tabida [42] and various Drosophila [43, 44]) Those direct observations from Drosophila suggest that a measurable reduction in life shortening may well occur in a decade or less. The fact that a relatively long EIP persists in nature suggests either that a short EIP is impossible or entails a sharp decline in transmission rate; the latter alternative is supported by recent observations of short EIPs [46] From these considerations, it seems that DENV could evolve to decrease its EIP in response to life-shortening Wolbachia, but we infer that it would reduce its transmission rate to do so. There are too many unknowns about such a process to make informed predictions, but the direction of evolution for DENV, Wolbachia, and the mosquito all coincide with intervention failure
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Free) 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a call
