The body of a caterpillar is the site of both a great feast and a gruesome familial struggle. But unlike even the most dys-functional holiday dinners, this fight for food erupts into bloodbath, with sisters killing sisters and brothers alike. The slaughter, as damaging to killer as to killed, exemplifies an ugly facet of evolution – the role of spite.

Some have described spiteful behavior in Copidosoma floridanum . These wasps lay their eggs in the egg of moth, Trichoplusia ni. The host larva as a fourth instar is shown at top. Copidosoma fight for resources as they consume the caterpillar. Some differentiate into sterile soldiers foregoing reproduction to preferentially kill less-related larvae. In the so-called mummy (middle) the outlines of reproductive larvae are visible as they pupate. Eventually, they emerge as adults (bottom). Soldier larvae, in contrast, die inside the mummy.

ROOTS OF EVIL Social behavior is organized conventionally into four classes, characterized by the costs and benefits to actors and recipients. Selfishness and mutualism are relatively straightforward: The actor benefits from its own behavior. Altruism and spite, in which the actor's fitness is impaired by its actions, have proven more problematic. Not until the 1960s did Oxford's Bill Hamilton show that genes for altruism can boost an individual's inclusive fitness, proliferating in the relatives that benefit, provided that the advantage to the recipient multiplied by its coefficient of relatedness to the actor (0.5 for full siblings, 0.25 for nephews, etc.) is greater than the cost incurred. Hamilton also recognized spite as a theoretical possibility, if the recipient is negatively related to the actor, that is, less related than a random member of the population. But he also recognized an important difference with altruism: When a spiteful actor removes a negatively-related recipient, all the remaining individuals benefit, not just the actor's kin. Selection for spite is, therefore, relatively weak. Harvard University's E.O. Wilson offered a solution by suggesting that spite could be favored without negative relatedness if the act also specifically benefits positively related individuals. While nature seemed rife with examples of altruism, however, spite was elusive. "It got to the stage in the literature where people were saying there are no examples of spite at all," says Kevin Foster of Berlin's Institute for Advanced Studies. "So we went back to the original definitions and tried to work out where they applied." Foster identified three cases of spite among social insects. The first, worker policing, is widespread among ants, bees, and wasps. Workers invest time and energy to kill the male offspring (the actors' nephews) produced by rogue workers. In the second case, the Argentine ant (among others) displays sex allocation biasing; workers kill brothers to shift the colony sex ratio in favor of females. And in a unique third case, red fire ant workers kill queens that do not share an allele at a particular locus ( Gp-9 ). Foster interprets these as Wilsonian spite, because they indirectly benefit a more closely related third party: respectively, brothers, sisters, and queens, with the same Gp-9 allele. But he also considers the fire ant example to have a Hamiltonian flavor, in that the spiteful Gp-9 allele is negatively related to that of the victim. "[Hamilton] saw it as very hard to get situations where you could get appreciable negative relatedness," says West. "He argued that that needed really small population sizes." But West says that negative relatedness can arise if competition for resources is highly localized.

BAD THINGS IN SMALL PACKAGES <p>SPITE AT WORK:</p> Courtesy Scott Bauer/ARS According to E.O. Wilson's definition, spiteis selected for when c A + c R r R > b X r X where c and b denote costs and benefits, and r denotes the actor's (A) relatedness to both recipient (R) and a third party (X). Such models assume competition at the scale of the species population. If colony members are viewed as competing amongst themselves these systems fit Bill Hamilton's definition of spite, driven by negative relatedness. Negative relatedness comes into play in fire ant workers that carry a certain allele at the Gp-9 locus (also known as a green beard gene) which identify and kill queens in the colony that don't have the allele. (adapted from K.R. Foster et al., Ann Zool Fennici, 38:229–38, 2001.) In the closed world of a fig, for example, where male fig wasps compete intensely for access to a limited number of females, males are as aggressive towards brothers as towards unrelated males. "There's no point helping one brother if the extra benefit they get comes at the cost of another brother," says West. So, for social interactions, relatedness is not absolute; it is relative, depending on who the competition is. When West's doctoral student, Andy Gardner, applied standard fitness equations to social behavior under local competition, what popped out at the end was Hamilton's rule with a negative relatedness and a negative benefit: Hamiltonian spite. "We haven't put negative relatedness into the analysis," says Gardner. "That's something that falls out naturally." So, in the case of Copidosoma , larvae compete for resources within a caterpillar host, not with the global wasp population. Average relatedness between competitors is zero, so the presence of clonal siblings indicates significant negative relatedness between other individuals, and even between nonclonal relatives. Foster says that in taking scale of competition into account, his examples of Wilsonian spite become Hamiltonian. "Everything [West and colleagues] say stands, so long as it's OK to change the scale at which you measure relatedness." But not everyone says it's OK. "Yes, competition is occurring on a very local scale within generations," says Michael Strand, a professor of entomology who works on Copidosoma at the University of Georgia, Athens. But the larvae will eventually disperse as adults when "there's plenty of opportunity for mixing between individuals of different generations," Strand says. West maintains that the scale of competition to consider is that which encompasses the trait being studied. Nevertheless, for the moment, Strand prefers to view the murderous soldiers as "indirect altruists."