Forewarned is Fore-armed: Crickets Exposed to Predators Have More Cautious Offspring

Organisms respond to their environment in a variety of ways, and natural selection operates by preserving the variations best suited to surviving and reproducing in a particular environment. In some cases, however, the environment itself acts to shape the next generation. One example is the fall field cricket (Gryllus pennsylvanicus); in 2010, a pair of researchers at Indiana State University showed that young G. pennsylvanicus develop differently depending on whether or not their mother was exposed to predation.

Jonathan Storm and Steven Lima placed mated female fall field crickets in a container for 10 days with or without a wolf spider (Hogna helluo); the spider's fangs were covered with wax to prevent it from killing the cricket. The crickets were then removed and allowed to lay eggs; the researchers collected the offspring and put them into containers which had previously contained H. helluo. Juvenile crickets born of mothers who had been exposed to a spider behaved more cautiously; they froze for significantly longer than crickets whose mother had never met a spider. Their mother's experience with a spider forewarned the juveniles, changing the way they responded; somehow, information was being passed from one generation to the next even though the mothers didn't take care of their young.

Next, the team tested whether these behavioural differences affected the crickets' chance of surviving in the presence of a spider. Crickets and spiders were placed together in an enclosure with several hiding places and with cricket food out in the open, forcing the crickets to choose between food and safety. The team used an infrared camera to record what happened over the course of several days. They found that the "forewarned" offspring evaded capture better and survived significantly longer.

A crucial question is whether these differences are also present in wild populations. To answer this, Storm and Lima captured gravid female G. pennsylvanicus from different sites in Indiana with and without predation by H. helluo and measured their offsprings' response to chemical cues from the spiders. Offspring from sites where the spider was common froze for longer in response to the cues, showing that the behavioural differences aren't limited to the lab.

How do the mothers pass information to their offspring in the absence of parental care? We don't know. One possibility is that the stress of encountering a predator causes hormonal changes in the mother which affect the development of her young. We do know that these findings aren't isolated to this pair of species; similar results have been found in several other organisms, including sticklebacks, great tits, and radish plants.

Whatever the mechanism mediating them, it's important to consider the role of these maternal effects in evolution. By influencing an organism's development in response to its mother's environment, they allow for morphological and behavioural flexibility in the face of potentially costly decisions. This flexibility enables populations to readily respond to changes in their environment, enhancing the range of conditions to which they are adapted. While maternal effects are probably based on regulating existing genetic variation (so the process isn't strictly Lamarckian evolution), they certainly provide a means for the maternal environment to shape the next generation, adding an important dimension to our understanding of the ecology and evolution of life on Earth.


Further reading
Agrawal, A. A., Laforsch, C, and Tollrian, R.. (1999) Transgenerational induction of defences in animals and plants. Nature 401:60–63.
Coslovsky, M and Richner, H. (2011) Predation risk affects offspring growth via maternal effects. Functional Ecology 25:878-888. doi:10.1111/j.1365-2435.2011.01834.x
Giesing, E.R., Suski, C.D., Warner, R.E., and Bell, A.M. (2011) Female sticklebacks transfer information via eggs: effects of maternal experience with predators on offspring. Proceedings of the Royal Society B 278:1753-1759 doi:10.1098/rspb.2010.1819
Storm, J. and Lima, S. (2010) Mothers Forewarn Offspring about Predators: A Transgenerational Maternal Effect on Behavior. The American Naturalist 175:382-390. doi:10.1086/650443

Image credit
The wolf spider image is by Sedeer el-Showk.