Shaping the Balance of the Sexes

We tend to think that offspring are just as likely to be male as female, but that's not necessarily true. In many reptiles, for example, sex isn't randomly determined, but depends on the temperature at a specific stage of development. Social insects like ants and bees often don't produce even numbers of males and females; the odds depend on a host of environmental and demographic factors. How selection shapes sex ratios and sex determination systems is a fascinating subject, but sometimes other organisms also play a major role. Parasites and symbionts can manipulate their host's reproduction and shifting the sex ratio to their advantage.

Perhaps the most famous example of this sort of reproductive manipulation is the bacteria genus Wolbachia, which infects insects and other arthropods and deserves a post to itself. Briefly, though, Wolbachia can only be transmitted to the next generation in eggs, so it skews the sex ratio in favour of females in order to spread further. Wolbachia doesn't have much use for males, so it disposes of them in a variety of ways. It can kill or feminize males early in development, and it also modifies their sperm, making them unable to reproduce with females that aren't carrying Wolbachia — or even females with a different strain of Wolbachia.

Alexander Gorischek and his colleagues wanted to know if the same thing happened in plants. To find out, they measured the effect of the symbiotic fungus Epichlöe elymi on the sex ratio of its host, Virginia wildrye (Elymus virginicus). Like most plants, wildrye is monoecious; individual plants have both male and female reproductive organs, often in the same flower. Despite the absence of separate sexes, the plants can decide to invest more in reproduction as a female (seed) or male (pollen). Environmental factors like light and nutrient ability are known to affect how plants allocate their reproductive resources, and the team wanted to investigate whether the symbiotic fungus could also influence the decision.

They predicted that plants infested with E. elymi would shift their reproduction towards seeds, since the fungus, like Wolbachia, is transmitted maternally. The fungus isn't always passed on to offspring, and researchers took advantage of this by comparing siblings with and without E. elymi; this helped to minimize the role of any genetic effects on reproductive allocation. When the team measured the amount of seed and pollen produced by the plants, they found that the difference they were looking for. Plants which had the fungal symbiont produced more seeds than pollen, while those that lacked it did the reverse. In other words, E. elymi makes the plants invest more heavily in female reproduction, though it's not yet clear how.

The fungus had about as strong an effect as some environmental factors did, but in this case the plant isn't simply responding to abiotic factors. Instead, the sex ratio of these plants is being determined by the interaction of two different biological systems, the plant and the fungus. This means that the sex ratio isn't determined by the plants' optimal response to their environment, but by the evolutionary give and take between these two organisms, each with their own evolutionary history, interests, and future.

Reproductive manipulators like Wolbachia and Epichlöe elymi can have a major impact on the evolution of their hosts. In many cases, Wolbachia is deeply embedded in its host's evolution and life history, sometimes leading the relationship to become symbiotic rather than parasitic. Its manipulation of sex ratios and reproduction has consequences ranging from altered sex-roles to the emergence of parthenogenesis or even speciation. Evolution never happens in isolation, but these critters have managed to gain an unusual amount of leverage over their hosts by manipulating the process at the core of evolution — reproduction itself.

Further reading
Gorischek, A.M., Afkhami, M.E., Seifert, E.K., Rudgers, J.A. (2012) Fungal Symbionts as Manipulators of Plant Reproductive Biology. The American Naturalist 181(4):562-570.
Jiggins, F.M., Hurst, G.D., and Majerus, M.E. (2000) Sex-ratio-distorting Wolbachia causes sex-role reversal in its butterfly host. Proceedings of the Royal Society B 267(1438): 69–73.
Werren, J.H. (1997). Biology of Wolbachia. Annual Review of Entomology 42: 587–609. doi:10.1146/annurev.ento.42.1.587
Zimmer, Carl (2001). Wolbachia: A Tale of Sex and Survival. Science 292(5519): 1093–5. doi:10.1126/science.292.5519.1093

Image credit
The Elmus virginicus image is from the University of Richmond Landscape Design Program.