Aphids with Attitude

It’s not often that Arnold Schwarzenegger gets compared to an aphid. An ant, maybe–many ants spend all day lifting heavy weights and defending the homeland. Unlike ants, bees, or Hollywood heroes, most of the world’s 4,000 or so aphid species aren’t by any stretch of the definition self-sacrificing social animals. Most aphids spend their lives as independent, pinhead-scale, six-legged versions of cows. They’re specialized for grazing but not much else–high throughput, low drama.

Yet a few aphid species turn out to be more like killer bees than like cows. These aphids live together in colonies, each founded by a highly fertile, queenlike female. While her daughters are still adolescents, they grow the outsized fighting legs that earned them a favorable comparison to Schwarzenegger in a scientific journal.

The armed youngsters risk their lives defending the colony against predatory insects, such as a lacewing larva. Such a marauder can easily outweigh the tiny aphid soldiers, but defense en masse brings it down. In some species, the military daughters never mature or reproduce, living out their lives as part of a sacrificial teen army.

Researchers are studying diverse sides of this miniature military life, from soldierly housekeeping to the recruits’ tendency to goof off. To scientists interested in the conditions that favor group living, these aphids make an especially interesting addition to the short list of social species. Unlike the fighters among social bees, ants, or even plant-sucking thrips, a Schwarzeneggerlike teenage-aphid army consists entirely of clones.

Plant vamps

Aphids live basically as vampires of plants. The insect families that scientists lump together as aphids belong to the huge order of true bugs, which typically deploy sucking mouthparts much like built-in soda straws. Aphids manage to make a living in one of the more challenging versions of this lifestyle, by feeding on plant sap rather than on pollen or other bugs. Sap’s abundant and loaded with sugars. Unfortunately, it offers only small amounts of essential amino acids.

Most aphid species reproduce both sexually and asexually, sometimes producing several cloned generations one after another. “They hardly ever have sex,” says Patrick Abbot of the University of Texas, Austin. “Aphids are basically little plants with legs.”

The first report of a social aphid, a species with specialized soldiers risking their lives for the colonial good, came from Southeast Asia in 1977. Shigeyuki Aoki, now of Rissho University in Kumagaya, Japan, and his colleagues described an aphid species in a group called pemphigids. A mother and her daughters cluster, and when an intruder appears, the daughters swarm over it, piercing its body–sometimes fatally–with their mouthparts.

Today, researchers recognize some 50 species of group-living aphids with heroic defenders. In 1991, Nancy Moran of the University of Arizona in Tucson discovered the first North American aphid with a soldier class, again one of the pemphigid species. This aphid, Pemphigus obesinymphae, turned out to be a good species for studying a soldier’s life.

The species has a soap-opera life. In spring, fertilized aphid eggs hatch under the bark of a cottonwood tree. All sexually produced eggs are females. Each dot of a hatchling makes an epic crawl under the loose bark until she comes to a leaf bud.

She stabs the growing tissue and settles down to feed. The leaf bud responds by forming a living chamber called a gall around her. The aphid will spend the rest of her life inside this gall.

Genetically identical embryos were already developing inside the aphid as she crawled toward her new home. Inside each of these clones, yet another generation was growing. This nesting of embryos within embryos permits rapid population growth.

The gall-founding female doesn’t lay eggs but gives birth to already developing daughters. These are the soldiers, which spend much of the summer in a state of arrested development and fight whatever threatens their gall. In the Oct. 9, 2001 Proceedings of the National Academy of Sciences (PNAS), Joan Strassmann and David Queller of Rice University in Houston say, “Evolution has endowed them with bulked-up Schwarzenegger arms (six of them, of course) and turned their soda straws into lethal weapons.”

Eventually, the soldiers return to civilian girlhood, grow into a new shape that includes wings, and fly away.

These dispersers next alight on plants in the mustard family, work their way below ground, and spread along the root. Without forming galls, they give birth to the daughters already formed within them.

Before winter comes, the youngest generation migrates back to a cottonwood. There, at last, these aphids produce a few sons as well as a few daughters. The new two-sex generation finds mates, sometimes among siblings, and females lay sexually formed eggs. All is ready for the cycle to start up again in the spring.

Clone rangers

Some aphid observers have suspected that aphid soldiers can shift allegiance and move to another gall. However, the residents of neighboring galls are so hard to distinguish that clone mixing has been a difficult idea for scientists to test.

Abbot, Moran, and their colleagues finally managed to work out genetic methods for identifying clones within cottonwood aphids. The researchers sampled soldiers from galls late in the summer. Typically, about 40 percent of aphid daughters in a gall came from an outside nest, the researchers reported in the Oct. 9, 2001 PNAS.

To see how these newcomers behave in their adopted galls, the team set up fake attacks with “invading” fruit fly larvae. The larvae can’t hurt an aphid, but the soldiers attack anyway. After the gall defenders had clustered around the supposed menace, the scientists checked which aphids were doing the work. A disproportionate number of the attackers were native to the gall, with the newcomers more likely to evade guard duty.

The tendency to shirk when living in an alien gall confirms predictions, says Abbot. Taking risks to benefit close kin offers a way, albeit a roundabout one, of spreading one’s genes. Gambling life and limb for the sake of hosts that share fewer genes doesn’t offer as much evolutionary payoff.

Aphid armies take risks for the good of the colony even when they aren’t fighting. They do “altruistic housekeeping,” in the words of Tim Benton of the University of Stirling in Scotland and William Foster of Cambridge University in England.

The huge volume of plant sap that aphids process can create a major housekeeping challenge for creatures confined inside a gall with growing numbers of relatives. Aphid galls often have a small opening for waste disposal and the insects’ eventual departure, even though the hole invites predators to invade. That breach in defenses is well worth it, say the researchers, or else aphids would drown in their own honeydew excretions.

That’s exactly what happened in an experiment with aphid colonies of a European species that feeds on poplar trees. Benton and Foster turned the galls upside down so the entrance hole no longer allowed easy drainage, and the colonies perished from sewage backup.

The researchers found that in a properly oriented gall, soldiers in this species double as sanitation workers, clearing out the honeydew. Soldiers on latrine duty may make the ultimate sacrifice for the good of the colony. Many of the aphids fall out of the gall along with waste, says Foster.

Remarkable details of the aphid soldier’s housekeeping became clear last year after a group of physicists described a phenomenon that they called “liquid marbles,” water droplets coated with a water-repellant powder so they roll around without wetting a surface (SN: 7/28/01, p. 57: Available to subscribers at Having gathered moss, water drops roll.). Foster says that as soon as he saw the physics article, he realized that aphid soldiers make honeydew marbles. The aphids coat their liquid waste with a layer of wax, then roll it out of the gall.

On Nov. 8, 2001, Nature published a short item acknowledging that aphids had beaten physicists in developing the technology. Foster and his Cambridge colleague Nathan Pike teamed up with another group of physicists to describe the insect system in a paper entitled “How aphids lose their marbles” in the June 22 Proceedings of the Royal Society of London B.

Aphids may also engage in altruistic home repair, according to work in progress from Utako Kurosu of Tokyo University of Agriculture, Takema Fukatsu of Japan’s National Institute of Advanced Industrial Science and Technology in Tsukuba, and their colleagues. At the 6th International Symposium on Aphids in Rennes, France, last year, the research team described Asian aphids that repair rips in their galls with a gluey substance that comes out of their bodies. In the process of releasing the glue, many of the repair aphids essentially explode and die.

All together now

Just how soldier-making aphids fit into the array of social animals depends on who’s doing the fitting. To pick a recent categorization, though, Bernard Crespi of Simon Fraser University in Burnaby, British Columbia, divides the soldier-making aphids between two of his major groups of social animals.

He calls the aphids with temporary soldiers–those that eventually grow up to reproduce–”cooperative breeders.” In contrast, Crespi categorizes aphids with permanently sterile armies, known mostly in Asia, as “truly social,” in the group with bees and ants.

Theorists expect close kinship to favor self-sacrificing social behavior, and many of the world’s aphid galls outstrip anthills and beehives in terms of close kinship. At first glance, the aphids’ widespread cloning seems to provide “an ideal situation in terms of social evolution,” says Crespi. Yet so far, only about 1 percent of aphid species turns out to have social leanings. Clearly, researchers need to look beyond kinship for other factors that might push animals into group living.

One of those factors could be a taste for high-value real estate. So far, soldiering has turned up only in aphids that at some point in their lives cluster in galls. To insects that feed on plants, these hollow swellings are gingerbread castles that both protect and nourish. Crespi compares them to the fortress-food combos of such social species as termites that feed on the wood of their home tunnels or mole rats that eat tubers they find as they expand their burrow network.

There’s no reason to leave home to forage and lots of reason to cooperate in defending such a dream abode.

Crespi has also studied Australian thrips that raise young inside galls. There, too, he finds soldier sons and daughters.

More evidence for the importance of galls, Crespi says, is in their durability: Some of the fiercest soldiers show up in thrips with galls that last unusually long, sometimes up to a year. Perhaps the long-lasting galls are worth an extra-hard fight.

Foster and his colleagues are finishing an analysis of a similar pattern in aphids. Among three related Pemphigus species in Europe, the one that spends only a brief period in its gall doesn’t field soldiers, the intermediate gall dweller produces mildly aggressive soldiers, and the aphid with the longest-lasting gall fields an army of highly specialized, very aggressive soldiers. Foster and Philip Rhoden describe the system in an upcoming Insectes Sociaux.

Researchers have barely begun to discover the ways of social aphids. The Japanese laboratories in particular have ambitious research underway. Fukatsu, for example, is working on the chemistry of soldiering. His lab has found a protein abundant in soldiers that they seem to inject into their quarry.

The reputation of aphids has come a long way in recent years from the image of mindless minicows. In their PNAS article, Strassmann and Queller sum up social sap suckers of the 21st century: “Not only are the aphids fierce, but they are also sneaky and clever.”