Alternative Social Structures and Modes of Reproduction in Fire Ants

Summary

The invasive fire ants Solenopsis geminata and S. invicta are serious pest species worldwide; new management methods likely will rely on detailed comparative knowledge of the social and reproductive biology of both species. A rich literature of such information exists for S. invicta but is lacking for S. geminata. Therefore, we conducted detailed genetic analyses of S. geminata to reveal a highly unusual mode of reproduction that differs significantly from what has been found previously in S. invicta, suggesting the two species may not be susceptible to identical control measures.

Situation

Invasive fire ants such as the Tropical Fire Ant (Solenopsis geminata) and the Red Imported Fire Ant (S. invicta) have been spread across the globe unintentionally by human activity in the past century and currently cause enormous economic damage in terms of costs of control, medical treatment, and damage to property in their newly established ranges. Current methods of control have done little to alleviate impacts of the rapid expansion and enormous population buildups of these invasive pest insects, leading to an urgent need for new control strategies based on detailed knowledge of fire ant biology. Comparative data that reveal similarities and differences in social behavior and modes of reproduction between these invasive species will become especially relevant for preventing future introductions to currently uncolonized areas and for designing and implementing novel methods for fire ant management.

Response

Newly conceived management strategies for invasive fire ants will make use of information about the social biology and reproductive physiology of these insects, including the social structure of colonies (i.e., number of reproductive queens) and the mode of reproduction of individual queens. Worker fire ants regulate the number and identity of queens in their colonies, nurturing those they deem acceptable and killing unacceptable queens, so understanding the processes by which regulation of queen number occurs in different species may provide important clues on how to disrupt this system of natural regulation of reproduction. Ants not only commonly display variation in the number of queens maintained within a colony, but the specific mode by which these queens reproduce can vary; for instance, queens may produce some offspring via normal sexual reproduction and some via clonal (asexual) reproduction. This type of variation in individual mode of reproduction may be linked to variation in colony social structure in ants, so we are interested in the general question of how such variation arises in invasive fire ants and how it may impact colonization potential and management approaches. Fire ants live in one of two highly distinct types of colonies: monogyne colonies contain a single reproductive queen, whereas polygyne colonies contain many reproductive queens. In S. invicta, worker regulation of queen number is under the control of a single major genetic element, raising the question of whether similar genetic control underlies variation in colony queen number in S. geminata. If not, are there any obvious reproductive features that distinguish polygyne from monogye S. geminata and that could shed light on the origin and maintenance of polygyny in this species? Aswers in the form of comparative data from the two species my yield general insights into the molecular and physiological pathways involved in regulation of reproduction in invasive fire ants, ultimately providing information that could be used to disrupt these pathways in newly conceived control strategies. We conducted an extensive genetic study of both monogyne and polygyne S. geminata to comprehensively characterize colony social structure and mode of reproduction for comparison with the well studied S. invicta. Nests of both types were collected from multiple locations in Gainesville, Alachua County, Florida and returned to UGA for rearing in the laboratory. Samples of males, young virgin queens, workers, and sperm from mated reproductive queens (contained in their sperm-storage organs) were obtained from the reared colonies for genetic analysis. Also, some reproductive queens from polygyne colonies were isolated individually with workers to study their known progeny genetically. All collected individuals were genotyped at thirteen highly variable microsatellite genetic markers.

Impact

Multilocus genotypes scored from workers and virgin queens sampled from single monogyne S. geminata colonies revealed that these two female castes were produced sexually by a single diploid queen mated to a single haploid male. Thus, monogyne colonies have the typical “simple family” structure characteristic of other monogyne fire ants, in which all female offspring are full siblings sharing the same mother and father. Multilocus genotypes of individuals sampled from polygyne S. geminata colonies revealed a different picture. The reproductive queens from each colony and site typically possessed very few distinct multilocus genotypes, and typically those genotypes were homozygous (lacked any variation); moreover, virgin queen genotypes almost always were identical to those of the reproductive queens from the same colony. These genotypic patterns are hallmarks of clonal production of these females, a highly unusual pattern of reproduction in ants (and unprecedented in fire ants). Remarkably, the worker genotypes identified from these same colonies indicated that they invariably were produced sexually, that is, via the normal mode of production of females in ants whereby queens use the sperm from a mating to produce a fertilized diploid egg. Even more remarkable, the genotype distributions for these polygyne workers and for sperm genotyped from the sperm-storage organs of polygyne reproductive queens revealed that these queens always had mated with a male from a monogyne rather than a polygyne colony. The results of this genetic study thus reveal a highly unusual pattern of colony social structure and mode of reproduction in S. geminata that differs significantly from what has been found previously in extensive research on S. invicta. In the latter species, normal sexual reproduction produces females, both workers and queens, and this mode of reproduction characterizes both the monogyne and polygyne social forms, which evidently are determined by a single major genetic element unrelated to reproductive mode. In contrast, social structure and mode of reproduction differ concordantly between monogyne and polygyne S. geminata, and thus evidently are closely linked in this species. Whereas the monogyne type exhibits modes of reproduction of workers and queens typical of ants and other Hymenoptera, the polygyne type has a distinct mode of reproduction of each caste that appears quite unique among ants. Specifically, queens are produced by clonal reproduction, whereas workers are produced by normal sexual reproduction. As an added twist, these sexually produced workers in polygyne S. geminata colonies have polygyne mothers but monogyne fathers. Our findings are noteworthy in an evolutionary sense because they demonstrate the interrelatedness of multiple levels of biological complexity, with a profound shift in colony social structure associated with an equally significant shift in reproductive mode in polygyne S. geminata. Equally noteworthy are the practical implications for control of these invasive pests: the polygyne types of the two species, which, because of their high population densities and numerous reproductive queens per colony pose more serious economic problems and management concerns than the monogyne types, clearly originate and spread by different processes and thus may not be susceptible to identical control measures. Future studies will aim to determine the evolutionary routes by which polygyny and clonal reproduction arose in S. geminata. Prior studies failed to find a major genetic component underlying polygyny, as is known for S. invicta, so the question arises whether the origin of clonal queen production in S. geminata drove the development of polygyny. If this can be shown to be the case, then future genomic, physiological, and behavioral studies will address the genetic and regulatory changes involved in these shifts in the social and reproductive biology of this species in the hopes of uncovering key biochemical targets for disruption or modification, perhaps using novel gene-drive technologies. An important consideration during development of such approaches will be whether S. invicta shares similar genetic and regulatory changes associated with a shift in social structure and thus would be susceptible to similar manipulations.

State Issue

Conservation & Management of Natural Resources

Details

• Year: 2017
• Geographic Scope: International
• County: Clarke
• Program Areas:
  • Agriculture & Natural Resources