Natural History: Just lookin' for a home

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Just lookin' for a home

Arthur E. Weis

Like the boll weevil in the old folk song, a mother goldenrod gall fly is determined to give her young a good start in life.

A parent struggling to stay awake for the 2:00 A.M. feeding of her month-old baby or a tree swallow staring into the gaping mouths of his five featherless, chicks might be tempted to envy insects, whose parenting duties generally end with the laying of the last egg. But the life of an insect parent, or rather parent-to-be, is not carefree. Ecologists have found that for many insects, actions taken by the mother before the birth of her young are as vital to their survival (and ultimately their reproductive success) as is postnatal care in mammals and birds. Over the last twenty years, in the course of studying the goldenrod gall fly, Eurosta solidaginis--one of North America's most abundant but least-noticed insects--we have observed just how important these maternal preparations can be. Along the way, we have uncovered a complex set of relationships involving the insect, the plant on which it lays its eggs, and its several predators and parasites.

Perhaps it is misleading to say the goldenrod gall fly goes unnoticed. The quarter-inch-long fly itself is rarely seen, but any observant person driving through the countryside of the eastern or midwestern United States or walking through a weedy vacant lot in winter is likely to spot the insect's eponymous trademark: a gall on the stem of its host plant, goldenrod. A curiosity of nature, galls are abnormal growths of plant tissue induced by the larvae of various species of aphids, wasps, and flies. The insect's relationship to the plant is parasitic, for while the tumorlike growth supplies the larva with food and shelter, the plant receives no benefit in return; in fact, it produces slightly fewer seeds than an unaflicted plant and grows more slowly.

The bright green gall induced by Eurosta is a prominent spherical swelling, typically about an inch in diameter, halfway up the goldenrod stem. Inside, a single fly larva feeds on the gall's inner tissues and bides its time. It pupates in early spring and emerges in May as a tawny, speckle-winged adult, quite handsome as flies go. The male seeks out the tip of a nearby, newly growing goldenrod stem, where he flicks his wings in a way females find irresistible. After mating, the female goes off in search of her own goldenrod plant. When she finds a suitable stem, she inserts her ovipositor (an egg-laying structure that works much like a hypodermic needle) into the stem's terminal bud and injects a single egg. Over the course of her adult life--which lasts, at most, two weeks--a female goes without food and may lay a hundred eggs. Each egg hatches four to seven days later, and the tiny larva burrows its way down through the bud and into the stem. There it stimulates the plant to begin producing a gall, which consists of an inner tissue rich in protein and starch and an outer, protective tissue that soon becomes dry and corky. (Just how the fly induces a gall is unknown.) As the larva grazes on the nutritious inner tissue, the host produces more of it, guaranteeing a steady food supply. The developing insect remains in the gall's small central chamber for the next fifty weeks, emerging as an adult fly to begin the cycle over again.

An emerging adult female Eurosta fly has some crucial decisions to make. First, she must find a goldenrod plant, and not just any one will do. Throughout the eastern United States, the fly lays its eggs on Solidago altissima, or tall goldenrod. Four related, similar-looking plants--the Canadian, rough, early, and late golden-rods--also grow in this region. A gall fly mother, as we learned from a series of experiments, will land on other species of goldenrod, but a quick walk over the developing flower is enough for the "taste buds" on her feet to persuade her to move on. We found that when we wrapped leaves from S. altissima around the bud of another species of goldenrod, we could trick a female into inserting her ovipositor into the bud, but she would quickly realize her mistake; microscopic receptors on the tip of her ovipositor enable her to "taste" potential hosts with her reproductive organs as well as with her feet. Additional experiments showed why it is adaptive to be choosy: when we fooled a few females into injecting eggs into the wrong goldenrod, nearly all the resultant larvae failed to induce galls.

Not all tall goldenrods are created equal, however, so mother gall flies must be even more discriminating. Some plants in our study area never carry more than a few galls, year after year, while others only yards away consistently carry many. We could tell that females had investigated the seemingly resistant plants; their exploratory probes left small scars on the buds. To find out how these plants managed to discourage the flies, we first cloned equal numbers of resistant and susceptible plants. Experiments showed that newly hatched larvae stimulate both types of plants to begin producing galls, but the resistant plants soon kill off the abnormal tissue. The larvae, left without food, die. A mother gall fly can detect--at least some of the time--the plants that are likely to starve her young. In our experiments, females probed resistant plants less often than they did susceptible ones. And the probes into resistant plants were less likely to end with the injection of an egg.

Gall or no gall, that's one question. Beyond that lies the question of gall size. This, too, is a complicated issue, with equally significant ramifications for the larva. The gall's inner chamber is fairly constant in size, but the thickness of its outer tissue varies, determining the gall's eventual girth. This corky covering is all that separates the defenseless larva from a challenging set of predators that includes insectivorous wasps, beetles, and birds. Big galls can provide complete protection from one of the Eurosta larva's worst enemies--the parasitoid wasp Eurytoma gigantea. Despite its Latin name, this wasp is minuscule in comparison with the gall fly. It makes its living by injecting its own eggs into goldenrod galls. After hatching, the wasp larva consumes the fly larva and then eats the inner gall tissues as well. If the outer layer is thick enough, however, the wasp's ovipositor cannot reach the central chamber, and the developing fly is spared.

Unfortunately for the little fly larva nestled in its corky home, large gall size is no protection against some other predators. During the winter months, the downy woodpecker comes out of the woods in search of food. Pecking a narrow hole in a goldenrod gall and extracting the larva inside is easy work for this master excavator. In fact, woodpeckers and, in some areas, black-capped chickadees (whose efforts leave behind a cruder, conical-shaped hole) show a marked preference for big galls. This preference is understandable, since the smaller ones are likely to contain the parasitic wasp larvae, which--at one-tenth the size of Eurosta larvae--are a much less rewarding meal.

For other predators, gall size is simply not an issue. The beetle Mordellistena convicta, which evolved from stem-boring ancestors, lays its eggs on the outside of the gall. The larvae then chew right through the gall to get at the nutritious meal inside. And some of Eurosta's enemies don't even wait for the goldenrod gall to form. Eurytoma obtusiventris, another species of parasitoid wasp, seeks out goldenrod buds with Eurosta eggs and injects its own egg into the fly embryo before it hatches. Like a time bomb, the tiny wasp larva waits inside its developing host until the end of summer, by which time the fly larva will make a good-sized meal.

With so many enemies, what is a Eurosta mother to do? If she injects her eggs into plants with a weak response to the larva, small galls will result, and her offspring are liable to be eaten by wasps. If she injects her eggs into a highly reactive plant, the resultant large galls are attractive to birds. If the decision process is controlled by genes--as has been shown in many other insect species--the mothers that happen to make the right choice will pass those "decision" genes on to the next generation. Selection usually favors gall fly mothers that choose reactive plants, since in most places, and in most years, wasp attack is more prevalent than bird attack. This may explain why most mothers prefer fast-growing goldenrods, which on average produce slightly larger galls. But natural selection can be capricious, and where goldenrod grows near woodlots, birds can be a bigger problem. Slightly different "decision" genes may be favored in these locations.

A wise parent knows that, ultimately, a child is responsible for its own success. Goldenrod gall fly mothers can get their eggs to the right plant, but the larvae must stimulate the galls by themselves. Selection acts here, too. We have found that genes expressed in the larva can alter gall size. This means that where wasp attack is heavy, more of the larvae that stimulate big galls will survive to become adults and pass on those "stimulus" genes to the next generation. Where woodpecker and chickadee presence is heavy, larval fortunes, and the attendant selection pressures on gall size, are reversed. This patchwork quilt of conflicting selection pressures may prevent the evolution of a single best set of decision genes in mothers and stimulus genes in their offspring.

The Eurosta plot thickened still more when we began looking at the flies in other parts of the country. In the mid-Atlantic states, where we have done most of our research, the gall fly lays its eggs exclusively on tall goldenrod. Across the northern tier of states, however, from New England to the Great Plains and up into Canada, galls are also found on late goldenrod. Evidence suggests that we may be witnessing one insect species beginning to split into two. Working with postdoctoral colleagues, we investigated some gall flies from Minnesota and New England. The adults that emerged from the two species of goldenrod looked identical, but analysis of their mitochondrial DNA showed clear differences. At the very least, Eurosta has split into two races. The split appears to be driven, at least in part, by mutations of genes controlling host-plant choice. The adults that emerge from tall goldenrod galls overwhelmingly seek out that species as a rendezvous for mating and later for egg laying. Flies emerging from late goldenrod display the same sort of fidelity to their chosen host plant. These strong plant preferences, combined with a ten-day difference in the emergence dates of the two flies, virtually eliminate genetic mixing of the two populations.

Given sufficient time and the maintenance of barriers to interbreeding, a truly new species of fly may emerge. If it does, we hope to be around to document it. This small ecological community, centered on an inconspicuous insect and a coarse plant growing in undistinguished habitats, continues to offer opportunities to explore a broad slice of evolutionary biology. If we ever find ourselves wondering why we have spent so many years investigating such a seemingly mundane system, all we have to do is remember Charles Darwin. His few months on the Galapagos Islands may have set in motion much of his thinking about evolution, but he refined those thoughts during many subsequent years of observing and experimenting with earthworms and bumblebees in his own backyard.