The bug that lays the golden eggs: an insect's odd looks are nothing compared with its odd behavior

Natural History, March, 2002 by Arja Kaitala, Robert L. Smith

Stretching from the Pyrenees to the Mediterranean Sea, the Catalonian region of northeastern Spain is a sunlit land of flowering meadows and rocky crags, vineyards and ancient fieldstone walls, lollipop-like pines and spreading cork oaks. But to us, its main attraction is the golden egg bug (Phyllomorpha laciniata), a small, plant-sucking insect festooned with elaborate spines. Even the most jaded entomologist would concede that this bug looks pretty bizarre.

The fancy spines help the bug blend in with dried parts of its host plant, Paronychia argentea (sometimes called Algerian tea), a member of the carnation family. Finding golden egg bugs in the field can thus present a real challenge to the researcher. The more daunting task, however, is explaining their behavior. Most species of bugs lay their eggs on foliage or other locations in their habitat, and very few tend the eggs in any way. Female golden egg bugs, by contrast, usually lay their eggs on other adults of their own kind, which carry them around until the young nymphs hatch. Evolutionary theory would suggest that egg carrying has evolved in golden egg bugs because it ensures that more offspring survive. But exactly how does it help them? A further expectation is that the bugs would have evolved to provide care (in the form of egg carrying) for their own progeny, which perpetuate their genetic heritage, rather than for unrelated individuals. But is that the case?

The golden egg bug ranges over most of the Mediterranean countries; the first description of the species, from 1894, was based on observations in southern France. The early accounts of this "leaf-footed bug" include drawings of individuals carrying a few eggs haphazardly stuck to their back. The sketchy comments that accompany the drawings indicate that both males and females carry eggs. This pattern contrasts with the behavior documented among certain species of giant water bugs, in which only the male carries the eggs (as many as 140 can be neatly packed on his back). In the case of the water bug, the eggs a male carries are those he has fertilized; he therefore has a stake in their survival. The male not only carries the eggs but keeps them well aerated in the water, which is essential to the embryos' survival (see "Daddy Water Bugs," by Robert L. Smith, February 1980).

Golden egg bugs and giant water bugs are only distantly related, but the convergence of their unusual egg-carrying behavior makes them ripe for comparison. Because of our two specialties (Kaitala's being the golden egg bugs, Smith's the water bugs), we have collaborated on some recent golden egg bug research, which also involves other colleagues and Kaitala's students. We have set out to explore a number of questions: Is the attachment of eggs to bugs (instead of, say, to vegetation) inadvertent or deliberate, obligatory or optional? Are the egg carriers willing recipients, reluctant, or just plain oblivious? Are males or females more likely to carry eggs? What is the genetic relationship of bugs to the embryos they carry? Are costs associated with carrying eggs? Do carriers do anything special for the eggs? Can egg carrying be considered parental care, or is it something else? Are the offspring of females that attach their eggs to other bugs much more likely to survive?

Earlier work by the Kaitala team had determined how eggs were distributed within a population. The vast majority of bugs collected by the team carried between one and thirty eggs, with the average being five (counting still-attached empty shells). The eggs were attached with strong glue, most often to the bugs' backs but not infrequently to their undersides, legs, heads, and even antennae. Females carried almost one-third of the eggs, males slightly more than two-thirds.

Most of these eggs were gold colored, but some were white and a few pearly black. Tracking the eggs' development revealed that all white eggs soon turn yellow, then deepen in color to a golden sheen. Thus, white was the color of freshly laid eggs--a fact later confirmed by observing bugs depositing their eggs. A couple of weeks after being laid, a golden egg produces a tiny, cottony hatchling. Young bug nymphs hatch in the spring and abandon their carriers, leaving the empty eggshells behind, still attached. Nymphs feed on their host plant's flowers and molt five times. The fifth molt produces winged adults that spend the winter buried in plant litter. There they await the spring, dispersing widely at the beginning of the new reproductive season.

And what about a black egg? It gives rise to something quite different--a small wasp. What has happened here is that a parasitic hymenopteran has injected her tiny egg into a golden egg. The wasp larva has grown within the egg, feeding on and ultimately destroying the golden egg bug embryo.

Laboratory and field observations, together with some experiments, have thrown light on how and where eggs are deposited. Females ready to lay fertilized eggs always seem eager to lay them on other bugs, regardless of their sex. Potential female recipients are often able to resist being encumbered, and they can also simply avoid other females, but males, in their persistent attempts to copulate with females, find escaping this burden difficult. Despite his resistance, a courting male is apt to end up with an egg attached to him by the object of his advances, and even so, he will only infrequently be rewarded with copulation. Chances are that most or even all the eggs a male receives have been fertilized by rival males.