Gender-biased bacteria throw off an evolutionary balance
Where's the evolution?
An evolutionary perspective explains another unusual quirk of this interaction: Rickettsia not only improve their hosts' reproductive capacity, they bias it as well towards having girls. Uninfected whiteflies produce about a 50/50 ratio of female to male offspring, while the offspring of infected whiteflies are around 70% female. In terms of the bacterium's fitness, this manipulation also makes sense. More females means that the whitefly population can increase more rapidly, giving a big boost to the Rickettsia population, and since the bacterium is only passed from mother to offspring (not father to offspring), the bias also generates more possible new infections in the future. It might seem far-fetched for a tiny bacterium to influence its host's reproduction like this, but in fact, nature is full of examples of microorganisms wielding enormous power over their hosts fungi that cause ants to climb to the top of blades of grass (facilitating the fungus's dispersal), a protozoan that causes rats to lose their fear of cats (allowing the microorganism to spread up the food chain), and many, even more bizarre cases.
Though the human sex ratio is close to 50/50 and our chromosomal system of XX and XY makes that seem natural, sex ratio is not set in stone. Whiteflies produce more females under the influence of Rickettsia, New Zealand parrots produce more males when food is plentiful, and buffalos produce more females during the dry season to name just a few exceptions to the 50/50 rule. For Rickettsia and the whitefly, biasing reproduction towards females seems to be a win-win situation. Why then, do whiteflies normally produce a 50/50 sex ratio? After all, wouldn't it be advantageous for them to produce more females all the time even when not infected by Rickettsia? Evolutionary theory explains why most species are comprised of half males and half females and why exceptions occur.
To understand why a 50/50 sex ratio is so common, consider a hypothetical population of whiteflies, uninfected with Rickettsia, with a 50/50 sex ratio. Imagine that a mutation occurs that causes an individual to produce more female than male offspring. The next generation would have more females than males, and there would be an increase in the gene versions that favor female offspring. Since this generation has excess females, each male has a higher chance of fathering offspring e.g., each male might father the offspring of 1.5 females on average. At this point, individuals with gene versions that cause them to produce more sons are at an advantage, since sons will likely get to mate more and pass more copies of their genes on to the next generation than daughters will. Now, natural selection will act to increase the frequency of gene versions that favor male offspring and in the next generation, there would be a corresponding increase in the frequency of males. This cycle can continue indefinitely: whenever females are more common in the population, male-producing gene versions are favored, and whenever males are more common, female-producing gene versions are favored. This is an example of frequency dependent selection, in which the advantage or disadvantage of a particular trait depends on how common that trait is in the population. The result of this see-saw of natural selection is that sex ratios tend to converge on 50/50.
Of course, the southwestern whitefly population now deviates from a 50/50 sex ratio not because of the whitefly's evolution, but because of Rickettsia's evolution. The symbiont has evolved to manipulate its host's sex ratio for its own advantage setting up an interesting evolutionary conflict. Rickettsia's fitness is maximized by maintaining control of the whitefly sex ratio and biasing it towards females. However, any whitefly that happened to have a genetic variant that would allow it to produce more sons (even while infected with Rickettsia) would have a big advantage! Just as in the see-saw of sex-ratio evolution described above, in a female biased whitefly population, having sons will get a mother or father whitefly more grandkids than having daughters. Because of this, the fitness of individual whiteflies would be maximized by shifting the sex ratio back towards 50/50. The outcome of this evolutionary tug-of-war between the whitefly and its symbiont is still unclear.
Biologists are monitoring the impact this interaction may have on agriculture in the Southwest. While farmers have not yet seen a spike in crop damage, the spreading Rickettsia infection (and the boost it gives its host's reproductive capacity) does seem to have poised the whitefly for a major infestation. However, ongoing research on Rickettsia and its host may yield new strategies to combat pests. Symbionts can exert such a powerful influence over their hosts that scientists have considered using them as an all-natural pest control mechanism. In fact, in 2009, scientists successfully infected mosquitoes with a symbiont strain that halves the lifespan of the mosquito! A better understanding of exactly how Rickettsia affects whitefly fitness and fecundity could help us develop new approaches to controlling the spread of this pest.
Discussion and extension questions
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Whiteflies photo by Stephen Ausmus, USDA; Rickettsia photo from CDC
Understanding Evolution © 2017 by The University of California Museum of Paleontology, Berkeley, and the Regents of the University of California