Individual vs. Combined Short-Term Effects of Soil Pollutants on Colony Founding in a Common Ant Species

Insects are integral to terrestrial life and provide essential ecosystem functions such as pollination and nutrient cycling. Due to massive declines in insect biomass, abundance, or species richness in recent years, the focus has turned to find their causes. Anthropogenic pollution is among the main drivers of insect declines. Research addressing the effects of pollutants concentrates on aquatic insects and pollinators, despite the apparent risk of contaminated soils. Pollutants accumulating in the soil might pose a significant threat because concentrations tend to be high and different pollutants are present simultaneously. Here, we exposed queens of the black garden ant Lasius niger at the colony founding stage to different concentrations and combinations of pollutants (brake dust, soot, microplastic particles and fibers, manure) to determine dose-dependent effects and interactions between stressors. As proxies for colony founding success, we measured queen survival, the development time of the different life stages, the brood weight, and the number of offspring. Over the course of the experiment queen mortality was very low and similar across treatments. Only high manure concentrations affected the colony founding success. Eggs from queens exposed to high manure concentrations took longer to hatch, which resulted in a delayed emergence of workers. Also, fewer pupae and workers were raised by those queens. Brake dust, soot and plastic particles did not visibly affect colony founding success, neither as single nor as multiple stressors. The application of manure, however, affected colony founding in L. niger negatively underlining the issue of excessive manure application to our environment. Even though anthropogenic soil pollutants seem to have little short-term effects on ant colony founding, studies will have to elucidate potential long-term effects as a colony grows.

The evolution of social parasitism in Formica ants revealed by a global phylogeny

Studying the behavioral and life history transitions from a cooperative, eusocial life history to exploitative social parasitism allows for deciphering the conditions under which changes in behavior and social organization lead to diversification. The Holarctic ant genus Formica is ideally suited for studying the evolution of social parasitism because half of its 172 species are confirmed or suspected social parasites, which includes all three major classes of social parasitism known in ants. However, the life history transitions associated with the evolution of social parasitism in this genus are largely unexplored. To test competing hypotheses regarding the origins and evolution of social parasitism, we reconstructed a global phylogeny of Formica ants. The genus originated in the Old World ∼30 Ma ago and dispersed multiple times to the New World and back. Within Formica, obligate dependent colony-founding behavior arose once from a facultatively polygynous common ancestor practicing independent and facultative dependent colony foundation. Temporary social parasitism likely preceded or arose concurrently with obligate dependent colony founding, and dulotic social parasitism evolved once within the obligate dependent colony-founding clade. Permanent social parasitism evolved twice from temporary social parasitic ancestors that rarely practiced colony budding, demonstrating that obligate social parasitism can originate from a facultative parasitic background in socially polymorphic organisms. In contrast to permanently socially parasitic ants in other genera, the high parasite diversity in Formica likely originated via allopatric speciation, highlighting the diversity of convergent evolutionary trajectories resulting in nearly identical parasitic life history syndromes.

The secrets to domestic bliss – Partner fidelity and environmental filtering preserve stage-specific turtle ant gut symbioses for over 40 million years

BackgroundGut microbiomes can vary across development, a pattern often found for insects with complete metamorphosis. With varying nutritional need and distinct opportunities for microbial acquisition, questions arise as to how such ‘holometabolous’ insects retain helpful microbes at larval and adult stages. Ants are an intriguing system for such study. In a number of lineages adults digest only liquid food sources, while larvae digest solid foods. Like some other social insects, workers and soldiers of some ant species engage in oral-anal trophallaxes, enabling microbial transfer among siblings. But do queens, the typical colony founding caste, obtain symbionts through such transfer? Does this enable transgenerational symbiont passage? And does the resulting partner fidelity promote the evolution of beneficial symbionts? Furthermore, how might such adult-centric biology shape larval microbiomes? To address these questions, we characterized symbiotic gut bacteria across 13 species of Cephalotes turtle ants, with up to 40-million years of divergence. Adding to the prior focus on workers we, here, study underexplored castes and stages including queens, soldiers, and larvae, by performing 16S rRNA qPCR, amplicon sequencing, and phylogenetic classification.ResultsWe show that adult microbiomes are conserved across species and largely across castes. Nearly 95% of the bacteria in adults have, thus far, been found only in Cephalotes ants. Furthermore, the microbiomes from most adults exhibit phylosymbiosis, a trend in which microbiome community similarity recapitulates patterns of host relatedness. Additionally, an abundant, adult-enriched symbiont cospeciates with some Cephalotes. Evidence here suggests that these partner fidelity patterns extend from transgenerational symbiont transfer through alate gyne dispersal and subsequent colony-founding by queens. Like adults, larvae of Cephalotes species exhibit strong microbiome conservation. Phylosymbiosis patterns are weaker, however, with further evidence elevating environmental filtering as a primary mechanism behind such conservation. Specifically, while adult-enriched symbionts are found in most larvae, symbionts of older larvae are highly related to free-living bacteria from the Enterobacteriaceae, Lactobacillales, and Actinobacteria.ConclusionsOur findings suggest that both partner fidelity and conserved environmental filtering drive stable, stage-specific, social insect symbioses. We discuss the implications for our broader understanding of insect microbiomes, and the means of sustaining a beneficial microbiome.

Genomic architecture and evolutionary dynamics of a social niche polymorphism in the California harvester ant,Pogonomyrmex californicus

The societies of social insects are highly variable, including variation in the number of reproductives in a colony. In the California harvester ant,Pogonomyrmex californicus(Buckley 1867), colonies are commonly founded by a single queen (haplometrosis, primary monogyny). However, in some populations in California (USA), two or more queens cooperate in colony founding (pleometrosis) and continue to share a nest over several years (primary polygyny). Here, we use population genomics and linkage mapping to study the evolutionary dynamics and genetic architecture of this social niche polymorphism. Our analyses show that both populations underwent consecutive bottlenecks over the last 100,000 generations, particularly decreasing population size in the P-population and that the two populations diverged until 1,000 generations ago, after which gene flow increased again and we found signs of recent genetic admixture between the two populations. We further uncover an 8 Mb non-recombining region segregating with the observed social niche polymorphism, showing characteristics of a supergene comparable to the ones underlying social niche polymorphism in other ant species. In addition, 57 genes in five genomic regions outside the supergene show signatures of a selective sweep in the P-population, some of which are differentially expressed between haplo- and pleometrotic queens during colony founding. Our findings expose the social niche polymorphism inP. californicusas a polygenic trait involving a supergene.