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Introduction: Insects share intimate relationships with microbes that play important roles in their biology. Yet our understanding of how host-bound microbial communities assemble and perpetuate over evolutionary time is limited. Ants host a wide range of microbes with diverse functions and are an emerging model for studying the evolution of insect microbiomes. Here, we ask whether phylogenetically related ant species have formed distinct and stable microbiomes. Methods: To answer this question, we investigated the microbial communities associated with queens of 14 Formica species from five clades, using deep coverage 16S rRNA amplicon sequencing. Results: We reveal that Formica species and clades harbor highly defined microbial communities that are dominated by four bacteria genera: Wolbachia, Lactobacillus, Liliensternia, and Spiroplasma. Our analysis reveals that the composition of Formica microbiomes mirrors the phylogeny of the host, i.e., phylosymbiosis, in that related hosts harbor more similar microbial communities. In addition, we find there are significant correlations between microbe co-occurrences. Discussion: Our results demonstrate Formica ants carry microbial communities that recapitulate the phylogeny of their hosts. Our data suggests that the co-occurrence of different bacteria genera may at least in part be due to synergistic and antagonistic interactions between microbes. Additional factors potentially contributing to the phylosymbiotic signal are discussed, including host phylogenetic relatedness, host-microbe genetic compatibility, modes of transmission, and similarities in host ecologies (e.g., diets). Overall, our results support the growing body of evidence that microbial community composition closely depends on the phylogeny of their hosts, despite bacteria having diverse modes of transmission and localization within the host.

Selection and demography are fundamental processes that affect the genetic diversity of a species, but the interaction of these processes with the life history traits of a species ultimately shapes the observed patterns of genetic diversity. Life history traits such as mating system and dispersal strategy can contribute to efficient gene flow, which can buffer against the loss of genetic diversity. Having a lengthy haploid stage in the life cycle may contribute to efficient purging of deleterious mutations. In this thesis, analyses of gene expression in tissues with different ploidy levels identified hundreds of genes with patterns of tissue-specificity in Pinus sylvestris growing under natural conditions. Comparing the efficacy of selection on haploid and diploid tissue-specific genes demonstrated that purifying selection on genes expressed specifically in the female derived haploid tissues of P. sylvestris is strong. The work presented here is the first report of haploid selection in a tree, and one of the few studies to demonstrate the efficacy of purifying selection on the female gametophyte in plants. Last, reconstruction of the demographic history of seven outcrossing, wind pollinated European trees showed that their effective population size has been relatively stable through time, and that these tree species have retained high levels of genetic diversity through the climatic oscillations of the Pleistocene. The findings of the work done in this thesis highlight the influence of the life cycle and life history traits in shaping levels of genetic diversity as a response to purifying selection and demographic events., Tiivistelmä Luonnonvalinta ja demografinen historia ovat lajin geneettiseen monimuotoisuuteen vaikuttavia keskeisiä voimia, mutta vasta niiden yhteisvaikutus elinkierto-ominaisuuksien kanssa lopullisesti määrittää havaitun geneettisen muuntelun piirteet. Elinkierto-ominaisuudet, kuten lisääntymis- ja leviämisjärjestelmä vaikuttavat geenivirran määrään, mikä voi ehkäistä geneettisen muuntelun vähentymistä. Pitkä haploidi elämänvaihe voi vaikuttaa siihen miten tehokkaasti valinta poistaa haitalliset mutaatiot populaatiosta. Tässä työssä eri ploidiatason solukoiden geeniekspressioanalyysejä käytettiin satojen solukkospesifisten geenien tunnistamiseen luontaisissa oloissa kasvavista männyistä. Luonnonvalinnan tehokkuuden määrittäminen haploideissa ja diploideissa männyn solukoissa paljasti, että puhdistava valinta oli erityisen voimakasta äidiltä peräisin olevassa haploidissa solukossa. Tässä työssä osoitetaan ensimmäisen kerran haploidia valintaa puissa, ja työ on yksi harvoista tutkimuksista, joissa on määritetty puhdistavan valinnan tehokkuus äidiltä peräisin olevassa kasvin gametofyytissä. Lisäksi seitsemälle eri tuulipölytteiselle eurooppalaiselle puulajille rekonstruoidut populaatiohistoriat osoittivat, että puiden teholliset populaatiokoot ovat olleet historiallisesti suhteellisen stabiileja ja että niissä on säilynyt runsaasti geneettistä muuntelua läpi pleistoseenikauden ilmastovaihtelujen. Yhteenvetona, työ korostaa elinkierto-ominaisuuksien osuutta siinä, miten puhdistava valinta ja populaatiohistoria vaikuttavat geneettiseen muunteluun.

For many animals, nests are essential for reproductive success. Nesting individuals need to carry out a range of potentially challenging tasks, from selecting an appropriate site and choosing suitable materials to constructing the nest and defending it against competitors, parasites and predators. Given the high fitness stakes involved, and the diverse impacts both the abiotic and social environment can have on nesting success, we might expect cognition to facilitate nesting efforts. This should be especially true under variable environmental conditions, including those changing due to anthropogenic impacts. Here, we review, across a wide range of taxa, evidence linking cognition to nesting behaviours, including selection of nesting sites and materials, nest construction, and nest defence. We also discuss how different cognitive abilities may increase an individual’s nesting success. Finally, we highlight how combining experimental and comparative research can uncover the links between cognitive abilities, nesting behaviours and the evolutionary pathways that may have led to the associations between them. In so doing, the review highlights current knowledge gaps and provides suggestions for future research.

The masking theory states that genes expressed in a haploid stage will be under more efficient selection. In contrast, selection will be less efficient in genes expressed in a diploid stage, where the fitness effects of recessive deleterious or beneficial mutations can be hidden from selection in heterozygous form. This difference can influence several evolutionary processes such as the maintenance of genetic variation, adaptation rate, and genetic load. Masking theory expectations have been confirmed in single-cell haploid and diploid organisms. However, in multicellular organisms, such as plants, the effects of haploid selection are not clear-cut. In plants, the great majority of studies indicating haploid selection have been carried out using male haploid tissues in angiosperms. Hence, evidence in these systems is confounded with the effects of sexual selection and intraspecific competition. Evidence from other plant groups is scarce, and results show no support for the masking theory. Here, we have used a gymnosperm Scots pine megagametophyte, a maternally derived seed haploid tissue, and four diploid tissues to test the strength of purifying selection on a set of genes with tissue-specific expression. By using targeted resequencing data of those genes, we obtained estimates of genetic diversity, the site frequency spectrum of 0-fold and 4-fold sites, and inferred the distribution of fitness effects of new mutations in haploid and diploid tissue–specific genes. Our results show that purifying selection is stronger for tissue-specific genes expressed in the haploid megagametophyte tissue and that this signal of strong selection is not an artifact driven by high expression levels.

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.

Ants face unique challenges regarding pathogens, as the sociality which has allowed them to form large and complex colonies also raises the potential for transmission of disease within them. To cope with the threat of pathogens, ants have developed a variety of behavioral and physiological strategies. One of these strategies is self-medication, in which animals use biologically active compounds to combat pathogens in a way which would be harmful in the absence of infection. Formica fusca are the only ants that have previously been shown to successfully self-medicate against an active infection caused by a fungal pathogen by supplementing their diet with food containing hydrogen peroxide. Here, we build on that research by investigating how the prevalence of disease in colonies of F. fusca affects the strength of the self-medication response. We exposed either half of the workers of each colony or all of them to a fungal pathogen and offered them different combinations of diets. We see that workers of F. fusca engage in self-medication behavior even if exposed to a low lethal dose of a pathogen, and that the strength of that response is affected by the prevalence of the disease in the colonies. We also saw that the infection status of the individual foragers did not significantly affect their decision to forage on either control food or medicinal food as uninfected workers were also foraging on hydrogen peroxide food, which opens up the possibility of kin medication in partially infected colonies. Our results further affirm the ability of ants to self-medicate against fungal pathogens, shed new light on plasticity of self-medication and raise new questions to be investigated on the role self-medication has in social immunity.

Supercolonies of ants are perhaps the largest non-human animal societies, at their largest spanning several millions of individuals and thousands of nests and in invasive species even crossing oceans. Supercolonies have convergently evolved in several ant groups, and they all share a syndrome of key features. First, their colonies spread by budding, which leads to extensive polydomy and inter-nest movement of individuals. Second, local mating and recruitment of queens lead to extensive polygyny. Their ecological dominance is clear, but their evolutionary maintenance is enigmatic due to low relatedness among cooperating individuals and the lack of clear functional organization above local polydomous units. This review takes a multi-level look at the social evolution of supercolonies in an inclusive fitness perspective, outlining key behavioural, ecological, and genetic processes as well as open questions. Such consideration of cooperation and competition from the gene level to the level of populations of supercolonies is necessary for understanding the history and future of supercolonies.

Ants are among the most successful organisms on Earth. It has been suggested that forming symbioses with nutrient-supplementing microbes may have contributed to their success, by allowing ants to invade otherwise inaccessible niches. However, it is unclear whether ants have evolved symbioses repeatedly to overcome the same nutrient limitations. Here, we address this question by comparing the independently evolved symbioses in Camponotus, Plagiolepis, Formica and Cardiocondyla ants. Our analysis reveals the only metabolic function consistently retained in all of the symbiont genomes is the capacity to synthesise tyrosine. We also show that in certain multi-queen lineages that have co-diversified with their symbiont for millions of years, only a fraction of queens carry the symbiont, suggesting ants differ in their colony-level reliance on symbiont-derived resources. Our results imply that symbioses can arise to solve common problems, but hosts may differ in their dependence on symbionts, highlighting the evolutionary forces influencing the persistence of long-term endosymbiotic mutualisms.

It is well known that green urban commons enhance mental and physical well-being and improve local biodiversity. We aim to investigate how these outcomes are related in an urban system and which variables are associated with better outcomes. We model the outcomes of an urban common—box gardening—by applying the Social-Ecological Systems (SES) framework. We expand the SES framework by analyzing it from the perspective of social evolution theory. The system was studied empirically through field inventories and questionnaires and modeled quantitatively by Structural Equation Modeling (SEM). This method offers powerful statistical models of complex social-ecological systems. Our results show that objectively evaluated ecological outcomes and self-perceived outcomes are decoupled: gardening groups that successfully govern the natural resource ecologically do not necessarily report many social, ecological, or individual benefits, and vice versa. Social capital, box location, gardener concerns, and starting year influenced the changes in the outcomes. In addition, the positive association of frequent interactions with higher self-perceived outcomes, and lack of such association with relatedness of group members suggests that reciprocity rather than kin selection explains cooperation. Our findings exemplify the importance of understanding natural resource systems at a very low “grassroot” level.

The application of demographic history modelling and inference to the study of divergence between species has become a cornerstone of speciation genomics. Speciation histories are usually reconstructed by analysing single populations from each species, assuming that the inferred population history represents the actual speciation history. However, this assumption may not be met when species diverge with gene flow, for example, when secondary contact may be confined to specific geographic regions. Here, we tested whether divergence histories inferred from heterospecific populations may vary depending on their geographic locations, using the two wood ant species Formica polyctena and F. aquilonia. We performed whole-genome resequencing of 20 individuals sampled in multiple locations across the European ranges of both species. Then, we reconstructed the histories of distinct heterospecific population pairs using a coalescent-based approach. Our analyses always supported a scenario of divergence with gene flow, suggesting that divergence started in the Pleistocene (c. 500 kya) and occurred with continuous asymmetrical gene flow from F. aquilonia to F. polyctena until a recent time, when migration became negligible (2–19 kya). However, we found support for contemporary gene flow in a sympatric pair from Finland, where the species hybridise, but no signature of recent bidirectional gene flow elsewhere. Overall, our results suggest that divergence histories reconstructed from a few individuals may be applicable at the species level. Nonetheless, the geographical context of populations chosen to represent their species should be taken into account, as it may affect estimates of migration rates between species when gene flow is spatially heterogeneous.

The diversity of genetic and non-genetic processes that make offspring resemble their parents are increasingly well understood. In addition to genetic inheritance, parent–offspring similarity is affected by epigenetic, behavioural and cultural mechanisms that collectively can be referred to as non-genetic inheritance. Given the generality of the Price equation as a description of evolutionary change, is it not surprising that the Price equation has been adopted to model the evolutionary implications of non-genetic inheritance. In this paper, we briefly introduce the heredity perspectives on which those models rely, discuss the extent to which these perspectives make different assumptions and place different emphases on the roles of heredity and development in evolution, and the types of empirical research programmes they motivate. The existence of multiple perspectives and explanatory aims highlight, on the one hand, the versatility of the Price equation and, on the other hand, the importance of understanding how heredity and development can be conceptualized in evolutionary studies.

Understanding how social groups function requires studies on how individuals move across the landscape and interact with each other. Ant supercolonies are extreme cooperative units that may consist of thousands of interconnected nests, and their individuals cooperate over large spatial scales. However, the inner structure of suggested supercolonial (or unicolonial) societies has rarely been extensively studied using both genetic and behavioral analyses. We describe a dense supercolony‐like aggregation of more than 1,300 nests of the ant Formica (Coptoformica ) pressilabris. We performed aggression assays and found that, while aggression levels were generally low, there was some aggression within the assumed supercolony. The occurrence of aggression increased with distance from the focal nest, in accordance with the genetically viscous population structure we observe by using 10 DNA microsatellite markers. However, the aggressive interactions do not follow any clear pattern that would allow specifying colony borders within the area. The genetic data indicate limited gene flow within and away from the supercolony. Our results show that a Formica supercolony is not necessarily a single unit but can be a more fluid mosaic of aggressive and amicable interactions instead, highlighting the need to study internest interactions in detail when describing supercolonies.

Social insects live in highly complex societies with efficient communication systems. Begging is one display commonly used by offspring to signal their nutritional state, however begging behavior has received very little attention in social insects. Theory predicts that begging can be either an honest (i.e., honest-signaling strategy) or a dishonest (i.e., scrambling competition) signal of need, with dishonest signals expected to be more likely when relatedness within the group is low. To investigate the presence and honesty of begging, as well as the nature of the involved signals, we used a comparative approach with four species of the ant genus Formica known to differ in the degree of intra-colony relatedness. We investigated the behavior of starved and non-starved larvae of F. aquilonia, F. pressilabris (both low intra-colony relatedness), F. exsecta (intermediate relatedness), and F. fusca (high relatedness). In addition, we assessed the attraction of conspecific workers toward odors extracted from these two classes of larvae and analyzed the larval cuticular hydrocarbon profiles. We found that in F. fusca and F. exsecta, larvae signaled significantly more when starved. In contrast, larvae of F. aquilonia signaled significantly more when they were non-starved, while there was no significant difference in the behavior of starved vs. non-starved larvae in F. pressilabris. Our results show that workers were not preferentially attracted to the odor of starved larvae, and we also did not detect any differences between the cuticular hydrocarbon profiles of starved and non-starved larvae. Overall, this study demonstrates among species variation in larval hunger signaling in Formica ants, and encourages further studies to confirm the link between kin structure variation and the honesty of begging signals.

Evolution of altruistic behavior was a hurdle for the logic of Darwinian evolution. Soon after Hamilton formalized the concept of inclusive fitness, which explains how altruism can evolve, he suggested that the high sororal relatedness brought by haplodiploidy could be why Hymenopterans have a high prevalence in eusocial species, and why helpers in Hymenoptera are always female. Later it was noted that in order to capitalize on the high sororal relatedness, helpers would need to direct help toward sisters, and this would bias the population sex ratio. Under a 1:3 males:females sex ratio, the inclusive fitness valuation a female places on her sister, brother, and an own offspring are equal—apparently removing the benefit of helping over independent reproduction. Based on this argumentation, haplodiploidy hypothesis has been considered a red herring. However, here we show that when population sex ratio, cost of altruism, and population growth rate are considered together, haplodiploidy does promote female helping even with female‐biased sex ratio, due the lowered cost of altruism in such populations. Our analysis highlights the need to re‐evaluate the role of haplodiploidy in the evolution of helping, and the importance of fully exploring the model assumptions when comparing interactions of population sex ratios and social behaviors.

Social insects provide systems for studying epigenetic regulation of phenotypes, particularly with respect to differentiation of reproductive and worker castes, which typically arise from a common genetic background. The role of gene expression in caste specialization has been extensively studied, but the role of DNA methylation remains controversial. Here, we perform well replicated, integrated analyses of DNA methylation and gene expression in brains of an ant (Formica exsecta) with distinct female castes using traditional approaches (tests of differential methylation) combined with a novel approach (analysis of co‐expression and co‐methylation networks). We found differences in expression and methylation profiles between workers and queens at different life stages, as well as some overlap between DNA methylation and expression at the functional level. Large portions of the transcriptome and methylome are organized into “modules” of genes, some significantly associated with phenotypic traits of castes and developmental stages. Several gene co‐expression modules are preserved in co‐methylation networks, consistent with possible regulation of caste‐specific gene expression by DNA methylation. Surprisingly, brain co‐expression modules were highly preserved when compared with a previous study that examined whole‐body co‐expression patterns in 16 ant species, suggesting that these modules are evolutionarily conserved and for specific functions in various tissues. Altogether, these results suggest that DNA methylation participates in regulation of caste specialization and age‐related physiological changes in social insects.

Temporary social parasite ant queens initiate new colonies by entering colonies of host species, where they begin laying eggs. As the resident queen can be killed during this process, host colonies may lose their entire future reproductive output. Selection thus favours the evolution of defence mechanisms, before and after parasite intrusion. Most studies on social parasites focus on host worker discrimination of parasite queens and their offspring. However, ant larvae can also influence brood composition by consuming eggs. This raises the question whether host larvae can aid in preventing colony takeover by consuming eggs laid by parasite queens. To test whether larvae could play a role in anti-parasite defence, we compared the rates at which larvae of a common host species, Formica fusca, consumed eggs laid by social parasite, non-parasite, nest-mate, or conspecific non-nest-mate queens. Larvae consumed social parasite eggs more than eggs laid by a heterospecific non-parasite queen, irrespective of the chemical distance between the egg cuticular profiles. Also, larvae consumed eggs laid by conspecific non-nest-mate queens more than those laid by nest-mate queens. Our study suggests that larvae may act as players in colony defence against social parasitism, and that social parasitism is a key factor shaping discrimination behaviour in ants.

Queen pheromones are chemical signals that mediate reproductive division of labor in eusocial animals. Remarkably, queen pheromones are composed of identical or chemically similar compounds in some ants, wasps and bees, even though these taxa diverged >150MYA and evolved queens and workers independently. Here, we measure the transcriptomic consequences of experimental exposure to queen pheromones in workers from two ant and two bee species (genera: Lasius, Apis, Bombus), and test whether they are similar across species. Queen pheromone exposure affected transcription and splicing at many loci. Many genes responded consistently in multiple species, and the set of pheromone-sensitive genes was enriched for functions relating to lipid biosynthesis and transport, olfaction, production of cuticle, oogenesis, and histone (de)acetylation. Pheromone-sensitive genes tend to be evolutionarily ancient, positively selected, peripheral in the gene coexpression network, hypomethylated, and caste-specific in their expression. Our results reveal how queen pheromones achieve their effects, and suggest that ants and bees use similar genetic modules to achieve reproductive division of labor.

Coptoformica Müller, 1923 is a subgenus of Formica Linnaeus, 1758 that consists of c. a dozen species of ants that typically inhabit open grassy habitats and build small nest mounds. The most recent addition to the group is Formica fennica Seifert, 2000. The description was based on morphological characters, but the species status has not been confirmed by molecular methods. In this study, we use thirteen DNA microsatellite markers and a partial mitochondrial COI gene sequence to assess the species status of F. fennica, by comparing the genetic variation among samples identified as F. fennica and six other boreal Formica (Coptoformica) species. Most of the species studied form separate, discontinuous clusters in phylogenetic and spatial analyses with only little intraspecific genetic variation. However, both nuclear and mitochondrial markers fail to separate the species pair F. exsecta Nylander, 1846 and F. fennica despite established morphological differences. The genetic variation within the F. exsecta/fennica group is extensive, but reflects spatial rather than morphological differences. Finnish F. fennica populations studied so far should not be considered a separate species, but merely a morph of F. exsecta.