Multiple endosymbionts in populations of the ant Formica cinerea

Abstract

BackgroundMany insects, including ants, are infected by maternally inherited Wolbachia endosymbiotic bacteria though other secondary endosymbionts have not been reported in ants. It has been suggested that the ability of Wolbachia to invade and remain in an ant population depends on the number of coexisting queens in a colony. We study the genetic and social structure of populations in the ant Formica cinerea which is known to have populations with either monogynous or polygynous colonies. We screen populations for several endosymbiotic bacteria to evaluate the presence of different endosymbionts, possible association between their prevalence and the social structure, and the association between endosymbiont prevalence and genetic differentiation of ant populations.ResultsWe found three endosymbiotic bacteria; 19% of the nests were infected by Wolbachia, 3.8% by Cardinium and 33% by Serratia. There was significant variation among the populations regarding the proportion of nests infected by Serratia, Wolbachia and the pooled set of all the endosymbionts. Some individuals and colonies carried two of the bacteria, the frequency of double infections agreeing with the random expectation. The proportion of infected ants (individuals or colonies) did not correlate significantly with the population level relatedness values. The difference in the prevalence of Wolbachia between population pairs correlated significantly with the genetic distance (microsatellites) of the populations.ConclusionsThe discovery of several endosymbionts and co-infections by Wolbachia and Cardinium demonstrate the importance of screening several endosymbionts when evaluating their possible effects on social life and queen-worker conflicts over sex allocation. The low prevalence of Wolbachia in F. cinerea departs from the pattern observed in many other Formica ants in which all workers have been infected. It is likely that the strain of Wolbachia in F. cinerea differs from those in other Formica species. The correlation between the difference in Wolbachia prevalence and the pair-wise genetic distance of populations suggests that spreading of the bacteria is restricted by the isolation of the host populations.

A Veritable Menagerie of Heritable Bacteria from Ants, Butterflies, and Beyond: Broad Molecular Surveys and a Systematic Review

“…Overall, ants harbored heritable symbionts from six, and possibly eight, lineages of heritable symbionts ( Arsenophonus , Blochmannia , Spiroplasma , and Wolbachia —shown here; Cardinium hertigii and Serratia symbiotica —shown elsewhere [53], [54]; and two candidate symbionts from fire ants [55]; see Figures 4 and S1). The presence of bacteria clustering within clades of other heritable bacteria from the Enterobacteriaceae (Figure S2) suggests that this number could be even higher.…”

“…This is true for ticks (Ixodida), for example, which harbor Arsenophonus [52]. It is also true for ants (Formicidae), where at least one species is known to harbor Cardinium [53].…”

“…Studies on these insects have also focused on heritable symbionts. Facultative heritable symbionts such as Wolbachia , Spiroplasma , Cardinium , Serratia , and Arsenophonus have been documented from ants [47], [53], [54], [75]–[78], with only the former two groups being reported from lepidopdterans [79], [80].…”

Diversity and Phylogeny of Cardinium (Bacteroidetes) in Armored Scale Insects (Hemiptera: Diaspididae)

“…Co-infections with different strains of the same bacterium or different reproductive parasites are known to occur across arthropods (Weeks et al 2003;Goodacre et al 2006;Gotoh et al 2006;Duron et al 2008a;Skaljac et al 2010;Goodacre and Martin 2012). This problem has been the focus of theoretical (e.g., Engelstädter et al 2008;Vautrin et al 2008) and empirical study focusing specifically on interactions between Cardinium and the widespread Wolbachia (Gotoh et al 2006;Ros and Breeuwer 2009;White et al 2009;Sirviö and Pamilo 2010). …”

“…Cardinium infections were first observed in ticks (Kurtti et al 1996), and are found in a wide range of spiders, mites, and other arachnids Chigira and Miura 2005;Groot and Breeuwer 2006;Enigl and Schausberger 2007;Duron et al 2008b;Gruwell et al 2009;Martin and Goodacre 2009;Chang et al 2010;Breeuwer et al 2012). Although this microbe seems to be more common in arachnids, it is also known to infect insects Provencher et al 2005;Bigliardi et al 2006;Marzorati et al 2006;Sirviö and Pamilo 2010).…”