Reproductive cooperation between queens and their mated workers: the complex life history of an ant with a valuable nest.

The life history of Harpegnathos saltator is exceptional among ants because both queens and workers reproduce sexually. Recently mated queens start new colonies alone, but later some of the offspring workers also become inseminated and take over the egg-laying role. This alternation seems associated with the existence of very complex underground nests, which are designed to survive floods. Longevity of ponerine queens is low (a consequence of limited caste dimorphism in this "primitive" subfamily), and upon the death of an H. saltator foundress, the nest represents a substantial investment. The queen's progeny should thus be strongly selected to retain the valuable nests. Unlike the flying queens, the workers copulate with males from their own colonies, and, thus, their offspring are expected to be highly related to the foundress. Colony fission appears not to occur because a daughter fragment would lack an adequate nest for protection. Thus, the annual production of queens in colonies with reproductive workers remains essential for the establishment of new colonies. This contrasts with various other ponerine species in which the queens no longer exist.

Genetic control of social organization in an ant

A central issue in evolutionary biology is the extent to which complex social organization is under genetic control. We have found that a single genomic element marked by the protein-encoding gene Gp-9 is responsible for the existence of two distinct forms of social organization in the fire ant Solenopsis invicta. This genetic factor influences the reproductive phenotypes and behavioral strategies of queens and determines whether workers tolerate a single fertile queen or multiple queens per colony. Furthermore, this factor affects worker tolerance of queens with alternate genotypes, thus explaining the dramatic differences in Gp-9 allele frequencies observed between the two social forms in the wild. These findings reveal how a single genetic factor can have major effects on complex social behavior and influence the nature of social organization.

A nonspecific fatty acid within the bumblebee mating plug prevents females from remating

The best mating strategy for males differs from that of females, because females gain from mating with several males (polyandry), but males gain from monopolizing the females. As a consequence, males have evolved a variety of methods, such as the transfer of inhibitory substances from their accessory glands, to ensure exclusive paternity of the female's offspring, generally with detrimental effects on female fitness. Inhibitory substances have been identified as peptides or other specific molecules. Unfortunately, in social insects male-mating traits are investigated only poorly, although male social insects might have the same fundamental influence on female-mating behavior as found in other species. A recently developed technique for the artificial insemination of bumblebee queens allowed us to investigate which chemical compound in the mating plug of male bumblebees, Bombus terrestris L., prevents females (queens) from further mating. Surprisingly, we found that the active substance is linoleic acid, a ubiquitous and rather unspecific fatty acid. Contrary to mating plugs in other insect species, the bumblebee mating plug is highly efficient and allows the males to determine queen-mating frequencies.

Social evolution in a new environment: the case of introduced fire ants.

The inadvertent introduction of the fire ant Solenopsis invicta to the United States from South America provides the opportunity to study recent social evolution by comparing social organization in native and introduced populations. We report that several important elements of social organization in multiple-queen nests differ consistently and dramatically between ants in Argentina and the United States. Colonies in Argentina contain relatively few queens and they are close relatives, whereas colonies in the United States contain high numbers of unrelated queens. A corollary of these differences is that workers in the native populations are significantly related to the new queens that they rear in contrast to the zero relatedness between workers and new queens in the introduced populations. The observed differences in queen number and relatedness signal a shift in the breeding biology of the introduced ants that is predicted on the basis of the high population densities in the new range. An additional difference in social organization that we observed, greater proportions of permanently unmated queens in introduced than in native populations, is predicted from the loss of alleles at the sex-determining locus and consequent skewing of operational sex ratios in the colonizing ants. Thus, significant recent social evolution in fire ants is consistent with theoretical expectations based on the altered ecology and population genetics of the introduced populations.

Relatedness threshold for the production of female sexuals in colonies of a polygynous ant, Myrmica tahoensis, as revealed by microsatellite DNA analysis.

The genetic relationships of colony members in the ant Myrmica tahoensis were determined on the basis of highly polymorphic microsatellite DNA loci. These analyses show that colonies fall into one of two classes. In roughly half of the sampled colonies, workers and female offspring appear to be full sisters. The remaining colonies contain offspring produced by two or more queens. Colonies that produce female sexuals are always composed of highly related females, while colonies that produce males often show low levels of nestmate relatedness. These results support theoretical predictions that workers should skew sex allocation in response to relatedness asymmetries found within colonies. The existence of a relatedness threshold below which female sexuals are not produced suggests a possible mechanism for worker perception of relatedness. Two results indicate that workers use genetic cues, not queen number, in making sex-allocation decisions. (i) The number of queens in a colony was not significantly correlated with either the level of relatedness asymmetry or the sex ratio. (ii) Sex-ratio shifts consistent with a genetically based mechanism of relatedness assessment were seen in an experiment involving transfers of larvae among unrelated nests. Thus workers appear to make sex-allocation decisions on the basis of larval cues and appear to be able to adjust sex ratios long after egg laying.

The loss of female sex pheromone after mating in the corn earworm moth Helicoverpa zea: identification of a male pheromonostatic peptide.

Female moths often become depleted of sex pheromone after mating as the various components of virgin behavior are switched off. In examining a potential male contribution to these events in the corn earworm moth Helicoverpa zea, we have characterized a basic polypeptide from the tissues producing (accessory glands) and storing (duplex) the seminal fluids. The peptide evokes the depletion of sex pheromone when injected into virgin females. This pheromonostatic peptide (PSP) is 57 amino acids long and contains a single disulfide bridge. It is blocked at the N terminus with pyroglutamate and at the C terminus by amidation. As little as 23 ng of peptide evokes the near-complete depletion of pheromone in decapitated (neck-ligated) females that had been injected with pheromone biosynthesis-activating neuropeptide. Activity is approximately 15-fold less in intact virgins, showing that the head limits the expression of activity in these injected females. Females mated to surgically impaired males, capable of producing a spermatophore but not transferring spermatozoa or seminal fluids, are depleted of pheromone by injected peptide. Females whose abdominal nerve cords have been severed are not depleted of pheromone after mating. Thus, neural signals either descending or ascending via the nerve cord are required for the depletion of pheromone after mating. PSP, from the seminal fluids, may participate in this process by direct or indirect action on the glandular tissue; if so, it represents an unusual mechanism in insects for the regulation by seminal fluids of postmating reproductive behavior.