A new paper in The American Naturalist, by Jonathan Storm and Steven Lima, shows that pregnant female crickets exposed to predatory wolf spiders can somehow “warn” the eggs they carry about the presence of those spiders, so that the offspring of those spider-exposed crickets show antipredator behavior. This sort of looks like a case of “Lamarckian” inheritance—that is, the inheritance of an acquired trait—but it’s almost certainly not.
The authors used field crickets (Gryllus pennsylvanicus) bred in the laboratory, testing them with the wolf spider Hogna helluo. To prevent the spiders from actually eating the crickets, they were fed to satiation before the trials, and their fangs were covered with wax. Pregnant female crickets were placed in a terrarium with the spiders; the terrarium had also been “conditioned” by allowing the spider to inhabit it for two days before the trials, allowing the beast to leave scent and silk deposits in the arena. The crickets remained exposed for ten days, while a control group was unexposed. The offspring of both groups were then tested for “predator wariness”: the proportion of time that the crickets spent mobile or immobile in the presence of a spider. Storm and Lima also measured the offspring’s chances of actually being eaten by a hungry spider.
Surprisingly, they found a difference—a difference in the adaptive direction. The crickets whose moms had been exposed to spiders spent significantly more time being immobile than did control crickets. This difference translated into survival: “exposed” crickets were eaten at a significantly lower rate than “unexposed” ones, though in this case the differences were small. (The difference apparently resulted from “exposed” crickets spending more time in refuges in the terrarium, making them less visible to the spider.)
Exposing the laid eggs and nymphs to the spider and spider-cues themselves showed no effect, suggesting that the mother actually does something to the eggs that changes the behavior of the crickets who hatch from them.
Finally, the authors wanted to see if this effect might apply not just in the laboratory, but in the field. They collected pregnant female crickets from three sites in Indiana that had wolf spiders, and three nearby sites that had no wolf spiders. Again, offspring of mothers from the “spider sites” showed significantly higher immobility in the presence of spiders (in the lab) than did offspring from “nonspider sites.” This latter result may, however, simply reflect local natural selection: that is, the mothers in this case aren’t really “warning” their eggs about spiders, but the localities may simply show differential adaptation, so that “spider site” crickets have been selected to be more wary of predators. There might be no warning needed: all crickets from spider sites could simply have evolved wariness. (The authors do note this possibility.)
What does this mean? Well, it’s one of a few studies in which there are facultative, adaptive “maternal effects” allowing an adaptation to be activated before it’s “needed.” A similar result has been found in Daphnia cucullata: mother Daphnia exposed to predatory midges produce offspring having a “helmet” morphology that makes them more resistant to being eaten than are offspring of nonexposed Daphnia.
The study raises four questions:
Exactly how do mother crickets warn their eggs? Answer: we don’t yet know. The authors suggest that exposed crickets might affect their eggs by releasing hormones that induce the antipredator behavior. As their experiments show, though, it’s clearly something that the mother does, since exposing eggs or young nymphs to the crickets themselves shows no effect.
How could this result from natural selection? That is, how can an adaptation start to arise before it’s “needed”? Well, this isn’t really a problem for natural selection, at least conceptually. If there is a reliable environmental cue that persists between parent and offspring generations, any gene that permits a mother to induce her offspring to behave adaptively will be favored. There are lots of traits for which the expression begins before the relevant selection pressure appears. Birds begin to fly south before the winter comes. Plants use daylight cues to prepare for winter. It’s easy to see how natural selection could favor using reliable environmental cues to trigger an adaptive behavior so it’s in place when it’s needed. What is cute about Storm and Lima’s study is that the parents actually provide the cues for their young.
Could this be Lamarckian? That is, perhaps the adaptive behavior is simply an acquired trait passed from parents to offspring,a trait that somehow got embedded into the genes—as if parents who worked out in a gym would produce more muscular babies. Some evolutionists, like Eva Jablonka and Marion Lamb, have suggested that a form of Lamarckian inheritance could be important in evolution. I don’t think they’re right, simply because we have little evidence that acquired traits can be inherited, and for many adaptations it’s even hard to envision how their initial appearance could be induced by the environment.
But here’s a way to test this in the spider case: use a form of “family selection,” something common in animal breeding. Simply take a bunch of cricket families, and expose one member of each family to a spider. For the individuals who are more wary, breed the next generation from their unexposed brothers and sisters. Then again construct a bunch of family groups from those individuals, test one individual from each new family, breed from the nonexposed relatives of the warier crickets, and so on.
After a few generations, see if this form of family selection has produced increased wariness of spiders. If it has, it shows that you can accumulate hereditary factors promoting resistance to predation without ever having being exposed to spiders. That is, while spiders are the selective factor promoting predator resistance in crickets, you can build up that resistance without ever having seen a cricket. In other words, the trait is not Lamarckian.
This is the kind of experiment that was done, half a century ago, to show that mutations conferring antibiotic resistance in bacteria were not actually induced by the antibiotic, but were there to begin with in unexposed populations. (You may have heard of “replica plating,” devised by Joshua and Esther Lederberg in the 1950s.)
Is it epigenetic? The idea of “epigenetic inheritance”—inheritance based on things other than change in the base sequences of genes—is also a popular criticism of the neo-Darwinian “paradigm”. (Jablonka and Lamb have been especially vocal proponents of this view.) Things like DNA methylation, for instance, can be transmitted from parents to offspring (that’s how “imprinting” of genes occurs), and there’s some evidence that such effects can persist for more than one generation.
Well, some of this epigenetic inheritance almost certainly reflects evolution based on real DNA changes. For example if it’s adaptive to mark parental versus maternal chromosomes differentially, as David Haig at Harvard suggests, then that differential marking itself is probably coded by the DNA.
Regardless, though, we can test whether this “adaptive maternal effect” in crickets is purely epigenetic or DNA-based. Simply take those two populations of crickets from Indiana that show differential response to spiders, and hold them in the laboratory for about three generations without exposure to spiders. Since non-DNA-based epigenetic differences are known to disappear after one or two generations, the populations should quickly lose not only their difference in adaptive “imprinting,” but the phenomenon of adaptive maternally-based wariness itself. If, on the other hand, the population difference (or the trait itself) is based on changes in the DNA, the behavior will decay much more slowly (if at all) when selection maintaining the trait is relaxed.
Storm and Lima’s study has been reported widely in the press and, to their credit, journalists have avoided touting their results as somehow disproving Darwinism or DNA-based adaptation. Lamarckism and epigenetic inheritance remain formal possibilities here, but in the absence of any evidence that they’ve been important in the evolution of adaptations, it’s hardly worth looking for them.
Fig. 1. Wolf spider, Hogna helluo
Storm, J. J. and S. L. Lima. 2010. Mothers forewarn offspring about predators: a transgenerational maternal effect on behavior. Amer. Natur. DOI: 10.1086/650443