Seasonal variation and the co-occurrence of four pathogens and a group of parasites among monogyne and polygyne fire ant colonies

A year-long survey was conducted to determine the seasonality and co-occurrence of four pathogens and a group of parasites in colonies of the red imported fire ant, Solenopsis invicta, in north-central Florida. Solenopsis invicta colonies were sampled and examined for the presence of Pseudacteon spp. (P. curvatus, P. tricuspis, P. obtusus) parasitic phorid flies, a microsporidian pathogen (Kneallhazia solenopsae) and 3 S. invicta viruses (SINV-1, SINV-2, and SINV-3) by PCR or RT-PCR methods. In addition, the social form designation of each colony (single- or multiple-queen) was determined by genotyping worker ants at the Gp-9 locus to determine if the pathogens or parasites were associated with monogyne or polygyne fire ant colonies. Seasonal variability was observed in the prevalence of all pathogens/parasites examined, with SINV-1, SINV-3, and K. solenopsae exhibiting pronounced seasonality. SINV-1 and K. solenopsae infections were most prevalent among colonies during warmer periods of the year, while SINV-3 was most prevalent during the cooler periods. As hypothesized, pathogens were found more commonly in polygyne colonies than in monogyne colonies. Infection comparisons by social form revealed higher infection rates of K. solenopsae and SINV-2 in polygyne colony samples compared with monogyne colony samples. The overall colony infection and parasitism rate among the 360 colonies sampled, regardless of social form, was 60.3% (SINV-1), 8.9% (SINV-2), 10.8% (SINV-3), 22.5% (K. solenopsae), and 8.1% (Pseudacteon flies). An interesting pattern was observed between the number of different pathogens or parasites detected in monogyne and polygyne colonies. The majority of monogyne colonies (>80%) were either uninfected or infected or parasitized with only a single pathogen/parasite while the majority of polygyne colonies (>55%) were infected or parasitized with 2 or more pathogens/parasites simultaneously. Higher pathogen/parasite prevalence among polygyne colonies is attributed to lower genetic relatedness (among nestmates), increased colony longevity, and the proclivity of polygyne colonies to share workers, brood and queens among their interconnected colonies. Evaluation of pairwise co-occurrence data indicated that the pathogens and fly parasites were usually independently distributed among host colonies; however, unknown local factors did cause several significant deviations from expected values.