Liselotte Sundström’s research while affiliated with University of Helsinki and other places

Cooperative breeding entails conflicts over reproductive shares that may be settled in different ways. In ants, where several queens simultaneously reproduce in a colony, both queens and workers may influence the reproductive apportionment and offspring quality. Queens may vary in their intrinsic fecundity, which may influence the size of the worker entourage attending individual queens, and this may eventually dictate the reproductive output of a queen. We tested whether the reproductive success of queens is affected by the size of their worker entourage, their fecundity at the onset of the reproductive season, and whether the queen cuticular hydrocarbon profile carries information on fecundity. We show that in the ant Formica fusca both queen fecundity and egg hatching success increase with the size of their entourage, and that newly hatched larvae produced by initially highly fecund queens are smaller. Furthermore, higher relatedness among workers increased queen fecundity. Finally, the queens that received a large worker entourage differed in the cuticular chemistry from those that received a small worker entourage. Our results thus show that workers play a pivotal role in determining queen fitness, that high intracolony relatedness among workers enhances the overall reproductive output in the colony, and that queen fecundity is reflected in their cuticular hydrocarbon profile.

In this study, we investigated the bacterial and fungal microbiomes of the ant Formica exsecta (Hymenoptera, Formicidae), and assessed whether the microbial communities inside the ants differ from those in their nest material. Furthermore, we investigated whether the microbial communities inside the ants are conserved across time. To achieve this, we sequenced the bacterial 16S rRNA, and the fungal ITS region in entire adult worker ants and their nest material by Illumina MiSeq. We found that both the bacterial, and the fungal microbiomes form communities discrete from those in the surrounding nest material. In addition to the differences in species composition, we also found that bacterial species diversity, species richness, ζ diversity, and evenness were lower in ants than in the nest material. For fungi, only species richness was lower in the ants than in the nest material. The rate of within‐colony species turnover across sampling events was not statistically significant for bacteria, but highly significant for fungi. This suggests that the fungal communities in the ants are less stable than the bacterial ones. Four bacterial taxa ( Alphaproteobacteria , Proteobacteria , Staphylococcus , and Streptococcus ), and two fungal taxa ( Davidiella and Cryptococcus ) formed a core microbiome, being consistently present and more abundant in the ants, but absent in the nest material. In all other cases differences in community composition and structure were due to taxa that were more consistently present and more abundant in the nest material, and frequently absent in the ants. Furthermore, we found 36 unique OTUs identified as Proteobacteria, and 82 unique OTUs identified as Alphaproteobacteria in the ants, representing 2.5% and 5.8% of all bacterial OTUs and 24.6% and 41% of the total number of bacterial sequences. This suggests that F. exsecta harbours a considerable bacterial diversity that so far remains unexplored.

Reproductive sharing in animal groups with multiple breeders, insects and vertebrates alike, contains elements of both conflict and cooperation, and depends on both relatedness between co-breeders, as well as their internal and external conditions. We studied how queens of the ant Formica fusca adjust their reproductive efforts in response to experimental manipulations of the kin competition regime in their nest. Queens respond to the presence of competitors by increasing their egg laying efforts, but only if the competitors are highly fecund and distantly related. Such a mechanism is likely to decrease harmful competition among close relatives. We demonstrate that queens of Formica fusca fine-tune their cooperative breeding behaviors in response to kinship and fecundity of others in a remarkably precise and flexible manner.

Reproductive sharing in animal groups with multiple breeders, insects and vertebrates alike, contains elements of both conflict and cooperation, and depends on both relatedness between co-breeders, as well as their internal and external conditions. We studied how queens of the ant Formica fusca adjust their reproductive efforts in response to experimental manipulations of the kin competition regime in their nest, as well as their own reproductive status. Queens respond to the presence of competitors by increasing their egg laying efforts, but only if the competitors are highly fecund and distantly related. Furthermore, queens only engage in cannibalism of eggs when the risk of erroneously destroying own offspring is absent. We demonstrate that queens of Formica fusca fine-tune their behaviours in response to kinship and fecundity of others as well as their own physiological state in an unusually precise manner.

Social insects depend on communication to regulate social behaviour. This also applies to their larvae, which are commonly exposed to social interactions and can react to social stimulation. However, how social insect larvae sense their environment is not known. Using RNAseq we characterized expression of sensory‐related genes in larvae of the ant Formica fusca, upon exposure to two social environments: isolation without contact to other individuals, and stimulation via the presence of other developing individuals. Expression of key sensory‐related genes was higher following social stimulation, and larvae expressed many of the same sensory‐related genes as adult ants and larvae of other insects, including genes belonging to the major insect chemosensory gene families. Our study provides first insights into the molecular changes associated with social information perception in social insect larvae.

We have previously shown that the fungal and bacterial communities in nests of ants Formica exsecta are distinct from those in the surrounding soil. Now, the results from our three-year study show that the nests also provide a temporally stable environment, where microbial taxa, less tolerant of climatic fluctuations, could survive through unfavorable seasons. The nest could thus act as a reservoir for such microbial inocula, promoting the divergence of the nest communities over time. Abstract In a subarctic climate, the seasonal shifts in temperature, precipitation, and plant cover drive the temporal changes in the microbial communities in the topsoil, forcing soil microbes to adapt or decline. Many organisms, such as mound-building ants, survive the cold winter owing to the favorable microclimate in their nest mounds. We have previously shown that the microbial communities in the nest of the ant Formica exsecta are significantly different from those in the surrounding bulk soil. In the current study, we identified taxa, which were consistently present in the nests over a study period of three years. Some taxa were also significantly enriched in the nest samples compared with spatially corresponding reference soils. We show that the bacterial communities in ant nests are temporally stable across years, whereas the fungal communities show greater variation. It seems that the activities of the ants contribute to unique biochemical processes in the secluded nest environment, and create opportunities for symbiotic interactions between the ants and the microbes. Over time, the microbial communities may come to diverge, due to drift and selection, especially given the long lifespan (up to 30 years) of the ant colonies.

Chemical communication is common across all organisms. Insects in particular use predominantly chemical stimuli in assessing their environment and recognizing their social counterparts. One of the chemical stimuli used for recognition in social insects, such as ants, is the suite of long-chain, cuticular hydrocarbons. In addition to providing waterproofing, these surface hydrocarbons serve as a signature mixture, which ants can perceive, and use to distinguish between strangers and colony mates, and to determine caste, sex, and reproductive status of another individual. They can be both environmentally and endogenously acquired. The surface chemistry of adult workers has been studied extensively in ants, yet the pupal stage has rarely been considered. Here we characterized the surface chemistry of pupae of Formica exsecta, and examine differences among sexes, castes (reproductive vs. worker), and types of sample (developing individual vs. cocoon envelope). We found quantitative and qualitative differences among both castes and types of sample, but male and female reproductives did not differ in their surface chemistry. We also found that the pupal surface chemistry was more complex than that of adult workers in this species. These results improve our understanding of the information on which ants base recognition, and highlights the diversity of surface chemistry in social insects across developmental stages.

Supergenes, clusters of tightly linked genes, play a key role in the evolution of complex adaptive variation [1, 2]. Although supergenes have been identified in many species, we lack an understanding of their origin, evolution, and persistence [3]. Here, we uncover 20-40 Ma of evolutionary history of a supergene associated with polymorphic social organization in Formica ants [4]. We show that five Formica species exhibit homologous divergent haplotypes spanning 11 Mbp on chromosome 3. Despite the supergene's size, only 142 single nucleotide polymorphisms (SNPs) consistently distinguish alternative supergene haplotypes across all five species. These conserved trans-species SNPs are localized in a small number of disjunct clusters distributed across the supergene. This unexpected pattern of divergence indicates that the Formica supergene does not follow standard models of sex chromosome evolution, in which distinct evolutionary strata reflect an expanding region of suppressed recombination [5]. We propose an alternative "eroded strata model" in which clusters of conserved trans-species SNPs represent functionally important areas maintained by selection in the face of rare recombination between ancestral haplotypes. The comparison of whole-genome sequences across 10 additional Formica species reveals that the most conserved region of the supergene contains a transcription factor essential for motor neuron development in Drosophila [6]. The discovery that a very small portion of this large and ancient supergene harbors conserved trans-species SNPs linked to colony social organization suggests that the ancestral haplotypes have been eroded by recombination, with selection preserving differentiation at one or a few genes generating alternative social organization.

Biotic and abiotic characteristics shape the microbial communities in the soil environment. Manipulation of soil, performed by ants when constructing their nests, radically changes the soil characteristics and creates a unique environment, which differs in its composition, frequency and abundance of microbial taxa, from those in the reference soils. We sampled nests of the mound-building ant Formica exsecta, and the surrounding reference soils over a three-month period, and generated NGS (Illumina MiSeq), and T-RFLP data of the bacterial and fungal communities. We used ordination techniques and network analysis to disclose the community structure, and we assessed the variation in diversity, evenness and enrichment of taxa between the two environments. We also used indicator analysis to identify the potential core microbiome of the nests. Our results show that the bacterial and fungal communities, in the rigorously curated nest environment, are significantly different from those in the reference soils, in terms of community structure and enrichment of characteristic indicator taxa. We demonstrate that the nests represent a niche, where microbial species can adapt and diverge from the communities in the surrounding soils. Our findings contribute to our understanding of the composition and function of microbiomes in fragmented habitats.

Eusocial insects, such as ants, have access to complex disease defenses both at the individual, and at the colony level. However, different species may be exposed to different diseases, and/or deploy different methods of coping with disease. Here, we studied and compared survival after fungal exposure in 12 species of ants, all of which inhabit similar habitats. We exposed the ants to two entomopathogenic fungi (Beauveria bassiana and Metarhizium brunneum), and measured how exposure to these fungi influenced survival. We furthermore recorded hygienic behaviors, such as autogrooming, allogrooming and trophallaxis, during the days after exposure. We found strong differences in autogrooming behavior between the species, but none of the study species performed extensive allogrooming or trophallaxis under the experimental conditions. Furthermore, we discuss the possible importance of the metapleural gland, and how the secondary loss of this gland in the genus Camponotus could favor a stronger behavioral response against pathogen threats.