Polygyne Form Research Articles

Sex investment ratios in monogyne and polygyne populations of the fire ant Solenopsis invicta

AbstractBoth monogyne (single queen per colony) and polygyne (multiple queens per colony) populations of the fire ant Solenopsis invicta are good subjects for tests of kin selection theory because their genetic and reproductive attributes are well‐characterized, permitting quantitative predictions about the degree to which sex investment ratios should be female‐biased if workers and not queens control reproductive allocation. In the study populations, an investment ratio of 3 females: 1 male is predicted (a proportional investment in females of 0.75) in the monogyne form, whereas a proportional investment in females between 0.637 and 0.740 is expected in the polygyne form. To test these predictions, colonies from a single population of each social form were collected and censused during three different seasons. Consistent with their alternative modes of colony founding, monogyne colonies invested more in reproduction (sexual production) and less in growth/maintenance (worker production) than did the polygyne colonies. Overall, the sex investment ratios were female‐biased in both forms, although there was considerable seasonal variation. After adjusting for sex‐specific energetic costs, the proportional investment in females was 0.607 in the monogyne population, a value in between those expected under complete control by either the queen or the workers. However, when combined with data from four other previously studied monogyne populations in the U.S.A., the mean investment ratio did not differ significantly from the value predicted if workers have exclusive control. In the polygyne population, the proportional investment in females of 0.616 was consistent with the level of female bias expected under partial to complete worker control, although the potential influence of two confounding factors — possible contact with monogyne colonies and the preponderance of sterile diploid males — weakens this conclusion somewhat. Taken as a whole, the sex investment ratios of monogyne and polygyne populations of S. invicta are consistent with at least partial worker control. Of several ultimate and proximate explanations that have been proposed to explain inter‐colonial variation in the sex investment ratio, only the effect of the primary sex ratio (female‐determined eggs: male‐determined eggs) laid by the queen appears to account for the observed variation among monogyne colonies. In the polygyne population, there is limited support for the hypothesis that greater resource abundance favors investment in females.

Gene by Environment Interaction: Effects of a Single Gene and Social Environment on Reproductive Phenotypes of Fire Ant Queens

1. The gene Pgm-3 (or a closely linked gene) influences the phenotype and reproductive success of queens in multiple-queen (polygynous) colonies but not single-queen (monogynous) colonies of the Fire Ant Solenopsis invicta. 2. We investigated the mechanisms of differential phenotypic expression of Pgm-3 in these alternate social forms. Mature winged queens with the homozygous genotype Pgm-3 a/a averaged 26% heavier than queens with the genotypes Pgm-3 a/b and Pgm-3 b/b in the polygynous form. Heterozygotes were slightly heavier (2%) than Pgm-3 b/b queens in this form, demonstrating that the allele Pgm-3 a is not completely recessive in its effects on weight. 3. There was no significant difference in weight among queens of the three Pgm-3 genotypes in the monogynous form, with the mean weight of monogynous queens slightly greater than that of polygynous Pgm-3 a/a queens. Differences in weight between queens of the two social forms and among queens of the three genotypes in the polygynous form are not evident at the pupal stage and thus appear to develop during sexual maturation of the adults. This suggests that some component of the social environment of polygynous colonies inhibits weight gains during queen maturation and that Pgm-3 a/a queens are relatively less sensitive to this factor. 4. To test whether the high cumulative queen pheromone level characteristic of polygynous colonies is the factor responsible for the differential queen maturation, we compared phenotypes of winged queens reared in split colonies in which pheromone levels were manipulated by adjusting queen number. Queens produced in colony fragments made monogynous were heavier than those produced in polygynous fragments, a finding consistent with the hypothesis that pheromone level affects the reproductive development of queens. However, genotype-specific differences in weights of queens were similar between the two treatments, suggesting that pheromone level was not the key factor of the social environment responsible for the gene-environment interaction. 5. To test whether limited food availability to winged queens associated with the high brood/worker ratios in polygynous colonies is the factor responsible for this interaction, similar split-colony experiments were performed. Elevated brood/worker ratios decreased the weight of winged queens but there was no evidence that this treatment intensified differential weight gains among queens with different Pgm-3 genotypes. Manipulation of the amount of food provided to colonies had no effect on queen weight. 6. The combined data indicate that cumulative pheromone level and brood/worker ratio are two of the factors responsible for the differences in reproductive phenotypes between monogynous and polygynous winged queens but that these factors are not directly responsible for inducing the phenotypic effects of Pgm-3 in polygynous colonies.

Nest site selection by fire ant queens

We examined nest site selection by foundresses of the polygyne form ofSolenopsis invicta. In the laboratory, foundresses were allowed to nest in control soil vs. soil inoculated with refuse from a colony ofPheidole dentata, a natural enemy. In a second experiment foundresses chose between control andS. invicta soil. More foundresses (100%) avoided the soil of a natural enemy than the soil of a conspecific colony (79%) that may accept them into the nest. Foundresses from this polygyne ant appear to avoid other colonies in general, but avoid heterospecific colonies more.

Phenotypic plasticity and ?cultural transmission? of alternative social organizations in the fire ant Solenopsis invicta

We investigated the process of sexual maturation in winged queens of the fire ant Solenopsis invicta, a species with two distinct forms of social organization. We found that queens of the monogynous social form (single reproductive queen per colony) differ little or not at all from queens of the polygynous form (multiple reproductive queens per colony) in weight and fat content when these are pupae or newly-eclosed adults. Furthermore, the size of a sclerotized region of the adult thorax, which is set during larval growth, does not differ between queens of the two forms. In contrast, winged queens of the two social forms differ dramatically in their physiological phenotypes once they have matured, with monogynous queens weighing more and having greater fat reserves than polygynous queens. A crossfostering experiment revealed that the different maturation processes of queens of the two forms are induced largely by the type of colony in which a queen matures (monogynous or polygynous) rather than being due to intrinsic genetic differences between the forms. However, genetic variation at a single locus does appear to play some role in determining physiological phenotype in queens of the polygynous form, providing an example of genotype-environment interaction in the expression of these physiological traits. Differences between the social forms in the mature phenotypes that are produced constrain the reproductive options of queens, so that the characteristic social organization of a colony is perpetuated by virtue of the social environment in which new queens are reared.

Alternative adaptations, sympatric speciation and the evolution of parasitic, inquiline ants

Inquiline ant species are workerless social parasites whose queens reproduce in colonies of other species alongside the host queens. Inquilines arise either when one non-parasitic species evolves into an inquiline parasite of another non-parasitic species (the interspecific hypothesis), or by the speciation of intraspecific inquilines from their host stock (the intraspecific hypothesis): it is unlikely that inquilines evolve from other forms of social parasite. This paper reviews the evidence for and against the inter-and intraspecific hypotheses. All inquilines are close phylogenetic relatives of their host species (loose ‘Emery's rule’), and some are their host's closest relative (strict ‘Emery's rule’). A problem for the interspecific hypothesis is how to explain the strict Emery's rule, because phylogenetic constraints on host choice are probably quite weak. By contrast, the intraspecific hypothesis has difficulty accounting for the parasites' sympatric reproductive isolation. Facultative polygyny, in which queens may found colonies alone or by adoption into an existing multi-queen colony, should promote the evolution of small intraspecific inquilines. This is because small colony-founding queens should preferentially seek adoption, which provides the opportunity to produce a sexual-only brood. We suggest that microgynes, i.e. miniature queens found in some polygynous ants, represent such parasites. We review the evidence that inquiline species have evolved intraspecifically from microgynes in Myrmica ants. The coexistence within a species of a monogynous (singly-queened) and a polygynous form is probably a phenomenon usually unconnected with inquiline evolution. The reproductive isolation of intraspecific inquilines plausibly arises from divergent breeding behaviour associated with the parasites' small size. Such divergence could involve either a temporal separation in mating episodes, with small parasites maturing early, or a spatial separation, with small males being sexually-selected to mate near the nest with small queens seeking adoption, instead of in mating aggregations. We conclude that inquiline species strictly following Emery's rule could have evolved by the intraspecific route. If so, such species provide evidence for West-Eberhard's “alternative adaptation” hypothesis that between-species diversity frequently stems from diversity within species. They also represent likely cases of sympatric speciation. We suggest work on the parasites' phytogeny, genetics, behaviour and mating biology to test these conclusions further.

Distribution and Density of Polygyne Fire Ants (Hymenoptera: Formicidae) in Texas

Multiple-queen or "polygyne" Solenopsis invicta Buren colonies are a serious economic and environmental concern because they occur in much higher densities than the monogyne form. Polygyne colonies have been found at numerous locations in the United States; nevertheless, the frequency and distribution of this form are poorly known. Almost 700 roadside sites in 168 Texas counties were surveyed. Polygyny was discovered at 54% of the infested sites. Polygyne populations were scattered in a mosaic across Texas. The frequency of polygyny varied somewhat with geographic region, but the pattern was generally unrelated to habitat and environmental conditions. Polygyne sites averaged more than twice as many mounds per hectare as monogyne sites. Populations of monogyne and polygyne forms were slightly lower in cooler and drier portions of the state. Mounds of both forms were about the same size. Polygyny was correlated with lower rates of sexual production and reduced numbers of native ants. The high frequency of polygyny in Texas indicates that the fire ant problem in the state is much greater than previously realized.

Behavioral differences of queens in monogynous and polygynous nests of theCamponotus nawai complex (Hymenoptera: Formicidae)

Behavioral differences of queens of the obligately monogynous and facultatively polygynous forms ofCamponotus nawai complex were examined. Queens of the monogynous form were groomed by and received food from workers more frequently but they walked about inside nests less frequently than queens of the polygynous form. Hierarchical relationships were not observed among queens of polygynous nests. In general, those queens were equally cared for by workers, aggregated around the center of nests, and showed no hostility toward each other.

Comparisons between two apparently distinct forms ofCamponotus nawai ITO (Hymenoptera: Formicidae)

Obligately monogynous and facultatively polygynous forms ofCamponotus nawai Ito was compared. The seasonal changes of colony composition were similar in the two forms except for the season in which alates were found in nests. Collection data suggested that new colonies are founded only by single foundresses in the monogynous form, but mainly by colony budding in the polygynous form. All or most queens in polygynous nests were fertile, thus polygyny is functional. The body size and ovarian volume of queens were larger in the monogynous forms. Queens of the polygynous form showed bimodal size distribution, though smaller queens were less frequent. In the polygynous form, the number of queens was positively correlated with the number of immatures, but negatively correlated with the number of immatures per queen. It seems that the polygynous form occupies more northern regions than the monogynous one and their ranges contact parapatrically. The monogynous and polygynous forms ofC. nawai may be different species because of the differing mating seasons.

Colony Reproduction by Budding in the Polygyne Form of Solenopsis invicta (Hymenoptera: Formicidae)

Indirect evidence has suggested that polygyne colonies of the red imported fire ant, Solenopsis invicta Buren, reproduce by budding. To verify directly the occurrence of budding, queens in polygyne colonies were marked with fine wire and introduced to two field sites previously cleared of fire ant mounds. After 4-5 mo, all mounds were mapped and collected. Marked queens originating from the same colony were found distributed among three to eight different mounds separated by up to 50 m. Marked queens from different colonies were not recovered in the same mound, suggesting that queens do not move freely among established mounds which lack some former connection. The total weights of the colonies increased about four times during the course of the study, indicating substantial growth of colonies in addition to active budding.

Adoption of Newly-Mated Queens: A Mechanism for Proliferation and Perpetuation of Polygynous Red Imported Fire Ants, Solenopsis invicta Buren

The polygynous form of the red imported fire ant, Solenopsis invicta Buren was first reported from Mississippi in 1973; however, the source of the numerous fertile queens in polygynous colonies has remained an enigma. In 1987, 400 queens from a mating flight were marked with a durable paint and released in an area heavily populated with the polygynous form. None were recaptured after one week, but 9 months later, 4 clearly-marked queens were found in a nest 65 meters from their release point. This finding clearly points to adoption. About 5 weeks later, 37 of 107 fertile queens collected from 37 polygynous nests, were found to have partially histolyzed wing muscles and undeveloped ovaries. Mating flights had occurred a few days prior to the queen collections, thus it was apparent that these queens were newly adopted. This observation was verified following a second mating flight one week later. The results of our 3 studies clearly indicate that polygynous S. invicta can proliferate and perpetuate their colonies by queen adoption.

COMPARATIVE BIOCHEMICAL GENETICS OF THREE FIRE ANT SPECIES IN NORTH AMERICA, WITH SPECIAL REFERENCE TO THE TWO SOCIAL FORMS OF SOLENOPSIS INVICTA (HYMENOPTERA: FORMICIDAE).

An electrophoretic study of the genetics of three fire ant species in North America was undertaken with the primary objective of further clarifying the genetic relationship between two social forms of Solenopsis invicta. Such social forms are common in many groups of ants and may, in some cases, represent significant intermediate stages in the speciation process. The monogyne and polygyne forms of S. invicta, while differing in a number of important biological traits, are genetically indistinguishable, in contrast to the substantial genetic differentiation observed between S. invicta and a second, closely related, introduced species, S. richteri. The native fire ant, S. geminata, is genetically the most distinct of the three species studied, in accord with its taxonomic placement in a different species complex. Hypotheses concerning the derivation of the polygyne form of S. invicta from the monogyne form which invoke their long-term reproductive isolation in South America and separate introductions to North America appear unfounded. Although S. invicta and S. richteri are known to hybridize in North America, our study provided no evidence of gene introgression between S. invicta and the native species, S. geminata, in areas where our samples were collected. Analyses of population structure in S. invicta failed to reveal significant differentiation of populations or local inbreeding. Levels of genetic diversity in the three species studied, although not significantly different, were in the order predicted from knowledge of the population biology and recent history of the taxa, with S. richteri exhibiting the least diversity, S. geminata the greatest, and S. invicta having an intermediate level.

Diploid male production ? a significant colony mortality factor in the fire ant Solenopsis invicta (Hymenoptera: Formicidae)

Two forms of the fire ant, Solenopsis invicta, occur in North America; the monogyne form has colonies with a single functional queen while the polygyne form has colonies containing many functional queens. Field surveys indicate that diploid males are common in natural populations of the polygyne form but absent from monogyne populations, in contrast to laboratory data showing that similar frequencies of queens producing such males occur in the two types of populations. Our results show that mature monogyne colonies with adopted queens rear diploid males in the laboratory, so it is unlikely that the absence of these males from monogyne colonies in the field is due to discrimination against them by monogyne workers. On the other hand, incipient monogyne colonies that produce diploid males exhibit significantly higher mortality and significantly slower rates of growth (Figs. 1–3) than colonies producing workers only. These results suggest that the observed distribution of male diploidy in S. invicta can be explained by differential mortality of diploid male producing colonies of the two forms, with such colonies of the monogyne form experiencing 100% mortality early in development. The mortality differences due to this factor are shown to be related to the different social structures and modes of colony founding characterizing the two forms.

Females ofFormica rufa L. (Hym., Formicidae) with enlarged labial glands

Females with enlarged labial glands were found in two colonies of the polygynous form ofFormica rufa L. They were distinguishable from normal females by more or less extensive brown patches on otherwise black scutums, and by slightly enlarged pronotums. They mated in the ordinary way; afterwards they were found to have their spermathecas full of living sperm and later produced normal workers and workers with enlarged labial glands (Wasmann's «pseudogynes», Novak's «secretergates»). There were indications that the power of flight, if any, was poorer than that of normal females.