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Unexpected absence of a multiple-queen supergene haplotype from supercolonial populations of Formica ants
Abstract
Ants exhibit many complex social organization strategies. One particularly elaborate strategy is supercoloniality, in which a colony consists of many interconnected nests (= polydomy) with many queens (= polygyny). In many species of Formica ants, an ancient queen number supergene determines whether a colony is monogyne (= headed by single queen) or polygyne. The presence of the rearranged P haplotype typically leads colonies to be polygyne. However, the presence and function of this supergene polymorphism have not been examined in supercolonial populations. Here, we use genomic data from species in the Formica rufa group to determine whether the P haplotype leads to supercoloniality. In a Formica paralugubris population, we find that nests are polygyne despite the absence of the P haplotype in workers. We find spatial genetic ancestry patterns in nests consistent with supercolonial organization. Additionally, we find that the P haplotype is also absent in workers from supercolonial Formica aquilonia and Formica aquilonia × polyctena hybrid populations but is present in some Formica polyctena workers. We conclude that the P haplotype is not necessary for supercoloniality in the Formica rufa group, despite its long-standing association with non-supercolonial polygyny across the Formica genus.
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Social organization, dispersal and fecundity coevolve, but whether they are genetically linked remains little known. Supergenes are prime candidates for coupling adaptive traits and mediating sex-specific trade-offs. Here, we test whether a supergene that controls social structure in Formica selysi also influences dispersal-related traits and fecundity within each sex. In this ant species, single-queen colonies contain only the ancestral supergene haplotype M and produce MM queens and M males, while multi-queen colonies contain the derived haplotype P and produce MP queens, PP queens and P males. By combining multiple experiments, we show that the M haplotype induces phenotypes with higher dispersal potential and higher fecundity in both sexes. Specifically, MM queens, MP queens and M males are more aerodynamic and more fecund than PP queens and P males, respectively. Differences between MP and PP queens from the same colonies reveal a direct genetic effect of the supergene on dispersal-related traits and fecundity. The derived haplotype P, associated with multi-queen colonies, produces queens and males with reduced dispersal abilities and lower fecundity. More broadly, similarities between the Formica and Solenopsis systems reveal that supergenes play a major role in linking behavioural, morphological and physiological traits associated with intraspecific social polymorphisms.
Antagonistic selection has long been considered a major driver of the formation and expansion of sex chromosomes. For example, sexually antagonistic variation on an autosome can select for suppressed recombination between that autosome and the sex chromosome, leading to a neo-sex chromosome. Autosomal supergenes, chromosomal regions containing tightly linked variants affecting the same complex trait, share similarities with sex chromosomes, raising the possibility that sex chromosome evolution models can explain the evolution of genome structure and recombination in other contexts. We tested this premise in a Formica ant species, wherein we identified four supergene haplotypes on chromosome 3 underlying colony social organization and sex ratio. We discovered a novel rearranged supergene variant (9r) on chromosome 9 underlying queen miniaturization. The 9r is in strong linkage disequilibrium with one chromosome 3 haplotype (P 2 ) found in multi-queen (polygyne) colonies. We suggest that queen miniaturization is strongly disfavored in the single-queen (monogyne) background and is thus socially antagonistic. As such, divergent selection experienced by ants living in alternative social ‘‘environments’’ (monogyne and polygyne) may have contributed to the emergence of a genetic polymorphism on chromosome 9 and associated queen-size dimorphism. Consequently, an ancestral polygyne-associated haplotype may have expanded to include the polymorphism on chromosome 9, resulting in a larger region of suppressed recombination spanning two chromosomes. This process is analogous to the formation of neo-sex chromosomes and consistent with models of expanding regions of suppressed recombination. We propose that miniaturized queens, 16%–20% smaller than queens without 9r, could be incipient intraspecific social parasites.
Hybridization is frequent in the wild but it is unclear when admixture events lead to predictable outcomes and if so, at what timescale. We show that selection led to correlated sorting of genetic variation rapidly after admixture in 3 hybrid Formica aquilonia × F. polyctena ant populations. Removal of ancestry from the species with the lowest effective population size happened in all populations, consistent with purging of deleterious load. This process was modulated by recombination rate variation and the density of functional sites. Moreover, haplotypes with signatures of positive selection in either species were more likely to fix in hybrids. These mechanisms led to mosaic genomes with comparable ancestry proportions. Our work demonstrates predictable evolution over short timescales after admixture in nature.
Social parasites exploit the brood care behavior of their hosts to raise their own offspring. Social parasites are common among eusocial Hymenoptera and exhibit a wide range of distinct life history traits in ants, bees, and wasps. In ants, obligate inquiline social parasites are workerless (or nearly-so) species that engage in lifelong interactions with their hosts, taking advantage of the existing host worker forces to reproduce and exploit host colonies’ resources. Inquiline social parasites are phylogenetically diverse with approximately 100 known species that evolved at least 40 times independently in ants. Importantly, ant inquilines tend to be closely related to their hosts, an observation referred to as ‘Emery’s Rule’. Polygyny, the presence of multiple egg-laying queens, was repeatedly suggested to be associated with the origin of inquiline social parasitism, either by providing the opportunity for reproductive cheating, thereby facilitating the origin of social parasite species, and/or by making polygynous species more vulnerable to social parasitism via the acceptance of additional egg-laying queens in their colonies. Although the association between host polygyny and the evolution of social parasitism has been repeatedly discussed in the literature, it has not been statistically tested in a phylogenetic framework across the ants. Here, we conduct a meta-analysis of ant social structure and social parasitism, testing for an association between polygyny and inquiline social parasitism with a phylogenetic correction for independent evolutionary events. We find an imperfect but significant over-representation of polygynous species among hosts of inquiline social parasites, suggesting that while polygyny is not required for the maintenance of inquiline social parasitism, it (or factors associated with it) may favor the origin of socially parasitic behavior. Our results are consistent with an intra-specific origin model for the evolution of inquiline social parasites by sympatric speciation but cannot exclude the alternative, inter-specific allopatric speciation model. The diversity of social parasite behaviors and host colony structures further supports the notion that inquiline social parasites evolved in parallel across unrelated ant genera in the formicoid clade via independent evolutionary pathways.
Most supergenes discovered so far are young, occurring in one species or a few closely related species. An ancient supergene in the ant genus Formica presents an unusual opportunity to compare supergene‐associated phenotypes and the factors that influence the persistence of polymorphism in different species. We investigate the genetic architecture of social organization in Formica francoeuri, an ant species native to low‐ and mid‐elevation semiarid regions of southern California, and describe an efficient technique for estimating mode of social organization using population genomic data. Using this technique, we show that F. francoeuri exhibits polymorphism in colony social organization and that the phenotypic polymorphism is strongly associated with genotypes within the Formica social supergene region. The distribution of supergene haplotypes in F. francoeuri differs from that of related species Formica selysi in that colonies with multiple queens contain almost exclusively workers that are heterozygous for alternative supergene haplotypes. Moreover, heterozygous workers exhibit allele‐specific expression of the polygyne‐associated haplotype at the candidate gene Knockout, which is thought to influence social organization. We also report geographic population structure and variation in worker size across a large fraction of the species range. Our results suggest that, although the Formica supergene is conserved within the genus, the mechanisms that maintain the supergene and its associated polymorphisms differ among species. An ancient supergene underlies queen number polymorphism in the California native ant Formica francoeuri, but this species has a novel genotype distribution. This article examines population structure, the supergene and phenotypic variation in this little‐known species. @EeobUcr @UCRentomology.
Species commonly exhibit alternative morphs, with individual fate being determined during development by either genetic factors, environmental cues or a combination thereof. Ants offer an interesting case study because many species are polymorphic in their social structure. Some colonies contain one queen while others contain many queens. This variation in queen number is generally associated with a suite of phenotypic and life-history traits, including mode of colony founding, queen lifespan, queen–worker dimorphism and colony size. The basis of this social polymorphism has been studied in five ant lineages, and remarkably social morph seems to be determined by a supergene in all cases. These ‘social supergenes’ tend to be large, having formed through serial inversions, and to comprise hundreds of linked genes. They have persisted over long evolutionary timescales, in multiple lineages following speciation events, and have spread between closely related species via introgression. Their evolutionary dynamics are unusually complex, combining recessive lethality, spatially variable selection, selfish genetic elements and non-random mating. Here, we synthesize the five cases of supergene-based social polymorphism in ants, highlighting interesting commonalities, idiosyncrasies and implications for the evolution of polymorphisms in general.
This article is part of the theme issue ‘Genomic architecture of supergenes: causes and evolutionary consequences’.
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, e.g., 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 (ca. 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.
Formica red wood ants are a keystone species of boreal forest ecosystems and an emerging model system in the study of speciation and hybridization. Here we performed a standard DNA extraction from a single, field-collected Formica aquilonia × Formica polyctena haploid male and assembled its genome using ~60× of PacBio long reads. After polishing and contaminant removal, the final assembly was 272 Mb (4,687 contigs, N50 = 1.16 Mb). Our reference genome contains 98.5% of the core Hymenopteran BUSCOs and was pseudo-scaffolded using the assembly of a related species, F. selysi (28 scaffolds, N50 = 8.49 Mb). Around one third of the genome consists of repeats, and 17,426 gene models were annotated using both protein and RNAseq data (97.4% BUSCO completeness). This resource is of comparable quality to the few other single individual insect genomes assembled to date and paves the way to genomic studies of admixture in natural populations and comparative genomic approaches in Formica wood ants.
Significance
Some social insects exhibit split sex ratios, wherein a subset of colonies produce future queens and others produce males. This phenomenon spawned many influential theoretical studies and empirical tests, both of which have advanced our understanding of parent–offspring conflicts and the maintenance of cooperative breeding. However, previous studies assumed that split sex ratio was not under genetic control. Here, we show that split sex ratio is associated with a large genomic region in two ant species. The discovery that sex allocation can have a genetic basis provides an additional perspective on this well-studied trait of social insects.
Significance
Identifying the conditions associated with a life history transition from cooperative colony life to exploitative social parasitism is important for understanding how changes in behavior contribute to speciation. To explore the evolutionary origins of social parasitism, we reconstructed the evolutionary history of Formica ants because half of all species are social parasites and all socially parasitic life history syndromes known from eusocial insects are represented in this genus. We demonstrate that social parasites evolved from an ancestor that lost the ability to establish new colonies independently and that highly specialized parasites can evolve from less complex social parasite syndromes. Our findings emphasize that social parasite syndromes readily originate in socially polymorphic organisms and evolved convergently across the ant phylogeny.
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. We study behavior and genetic structure in a dense supercolony‐like aggregation of more than 1,300 ant nests. Aggression bioassays reveal some aggression within the assumed supercolony, but there are no clear colony borders. The occurrence of aggression increases with distance from the focal nest, in accordance with the genetically viscous population structure we observe by using 10 microsatellite markers.
Supergenes are clusters of linked genetic loci that jointly affect the expression of complex phenotypes, such as social organization. Little is known about the origin and evolution of these intriguing genomic elements. Here we analyse whole-genome sequences of males from native populations of six fire ant species and show that variation in social organization is under the control of a novel supergene haplotype (termed Sb), which evolved by sequential incorporation of three inversions spanning half of a ‘social chromosome’. Two of the inversions interrupt protein-coding genes, resulting in the increased expression of one gene and modest truncation in the primary protein structure of another. All six socially polymorphic species studied harbour the same three inversions, with the single origin of the supergene in their common ancestor inferred by phylogenomic analyses to have occurred half a million years ago. The persistence of Sb along with the ancestral SB haplotype through multiple speciation events provides a striking example of a functionally important trans-species social polymorphism presumably maintained by balancing selection. We found that while recombination between the Sb and SB haplotypes is severely restricted in all species, a low level of gene flux between the haplotypes has occurred following the appearance of the inversions, potentially mitigating the evolutionary degeneration expected at genomic regions that cannot freely recombine. These results provide a detailed picture of the structural genomic innovations involved in the formation of a supergene controlling a complex social phenotype. A supergene controlling social behaviour arose in the common ancestor of six ant species by the sequential incorporation of three inversions.
The extreme diversity of dispersal strategies in ants is unique among terrestrial animals. The nature of ant colonies as social, perennial, and sessile superorganisms is the basis for understanding this diversity, together with the inclusive fitness framework for social evolution. We review ant dispersal strategies, with the aim of identifying future research directions on ant dispersal and its evolution. We list ultimate and proximate determinants of dispersal traits and the ecological and evolutionary consequences of dispersal for population structures and dynamics, as well as species communities.
We outline the eco-evolutionary feedbacks between the multitude of traits affecting dispersal evolution and the likely evolutionary routes and ecological drivers in transitions among the diverse ant dispersal strategies. We conclude by presenting a research framework to fill the gaps in current knowledge, including comparative studies of colony life histories and population structures and theoretical models of the eco-evolutionary dynamics affecting dispersal, in an inclusive-fitness framework.
The >15 000 ant species are all highly social and show great variation in colony organization, complexity and behavior. The mechanisms by which such sociality evolved, as well as those underpinning the elaboration of ant societies since their ∼140 million year old common ancestor, have long been pondered. Here, we review recent insights generated using various genomic approaches. This includes understanding the molecular mechanisms underlying caste differentiation and the diversity of social structures, studying the impact of eusociality on genomic evolutionary rates, and investigating gene expression changes associated with differences in lifespan between castes. Furthermore, functional studies involving RNAi and CRISPR have recently been successfully applied to ants, opening the door to exciting research that promises to revolutionize the understanding of the evolution and diversification of social living.
Dispersal determines gene flow among groups in a population and so plays a major role in many ecological and evolutionary processes. As gene flow shapes kin structure, dispersal is important to the evolution of social behaviours that influence reproduction within groups. Conversely, dispersal depends on kin structure and social behaviour. Dispersal and social behaviour therefore co-evolve, but the nature and consequences of this interplay are not well understood. Here, we show that it readily leads to the emergence of two social morphs: a sessile, benevolent morph expressed by individuals who tend to increase the reproduction of others within their group relative to their own; and a dispersive, self-serving morph expressed by individuals who tend to increase their own reproduction. This social polymorphism arises due to a positive linkage between the loci responsible for dispersal and social behaviour, leading to benevolent individuals preferentially interacting with relatives and self-serving individuals with non-relatives. We find that this linkage is favoured under a large spectrum of conditions, suggesting that associations between dispersal and other social traits should be common in nature. In line with this prediction, dispersers across a wide range of organisms have been reported to differ in their social tendencies from non-dispersers.
Semi-natural linear habitats such as field and meadow margins are often crucial in maintaining insect diversity and species distributions in agricultural landscapes. While many ant species are capable of forming large colonies (supercolonies) that can have considerable effects on the ecosystem within which they are embedded, it is not known how colony development, persistence, and spatial structure in agricultural areas may be affected by these boundary habitats. We used historical orthophotographs, extensive mapping of ant nests, and spatial statistics to study how the structure of fine-scale traditional agricultural land-use mosaic in the western Carpathians of Central Europe (Slovakia) influenced one of the largest supercolonies of Formica exsecta documented in Europe—the second largest supercolony in terms of the number of nests (~1500 nests) and significant in its spatial extent (~5 ha) and estimated population abundance (~50 million of workers). The spatial analysis indicated that a distinct linear arrangement of the majority of nests along unmanaged property boundaries contributed to the remarkable size of the colony. Further, the structure of the supercolony appeared to be variable in space and dynamic over time; while some areas appeared to be saturated by larger older nests (hot spots), other areas were characterized by clusters of smaller younger nests (cold spots) potentially suggesting colony expansion over time. Field and grassland boundaries are important components of traditional fine-scale land organization in Central Europe and elsewhere, and they appeared to provide suitable and stable nesting habitat that facilitated the growth of the second largest European supercolony of F. exsecta, while the areas further away from the boundaries were affected negatively by land management. Our results demonstrate that F. exsecta supercolonies may persist in a broader range of agricultural disturbance regimes, including intensive grassland management (e.g., mowing), when an appropriate network of habitat refugia is included into land organization (e.g., unmanaged margins).
A Lepisiota (Hymenoptera: Formicidae: Formicinae) species in Ethiopia has been observed forming supercolonies spanning up to 38 km. L. canescens occurs at very high densities where there is sufficient moisture or herbaceous cover and dominates the local ant community, traits reminiscent of an invasive species. The supercolonies are genetically diverse, however, indicating they have not gone through the population bottleneck usually characteristic of species invasions. We conclude that the species is native to this region, though expanding its range locally into areas of human disturbance, where it is exploding in numbers. The lack of aggression across a genetically diverse population suggests that mitochondrial genetic variation is decoupled from variation relating to colony recognition cues like cuticular hydrocarbons. All in all, L. canescens could have the makings of an invasive species at an international scale and may represent a novel system to study the evolution and spread of supercolonies in ants.
A supercolonial mound-building wood ant was intentionally introduced from the Italian Alps to Quebec, Canada, in 1971. This species was believed so far to represent Formica lugubris ZETTERSTEDT, 1838. Yet, recent investigations on the distributions of F. lugubris and the closely related species F. paralugubris SEIFERT, 1996 in the Italian Alps showed presence of both species and also that the supercolonial social type is represented here mainly by the latter species. This raised doubts on the species identity of the Canadian ants and prompted a taxonomic re-investigation. Advanced exploratory and hypothesis-driven data analyses of worker phenotype of 152 nest samples of both species from the Alps and of two samples collected from the supercolony in Quebec convincingly confirmed the Canadian introduction to represent F. paralugubris. The Quebec samples were safely allocated to the F. paralugubris cluster in both Nest Centroid (NC)-Ward and NC-K-Means clustering, a nest-centroid based principal component analysis (PCA), and a linear discriminant analysis. The error of exploratory data analyses over all 154 samples varied between 0.6% (NC-KMeans) and 1.9% (NC-Ward, PCA). A new method calculating the size of nest populations of polygynous Formica rufa group ants is introduced, according to which the growth of the Valcartier introduction was estimated from about one million workers in 1971 to 19 million workers in 2005. Data on mating biology, strategy and speed of dispersal, colony structure, and ecological requirements indicate that active spreading of this ant to areas remote from the Valcartier beachhead is unlikely. There is also a low probability of passive dispersal by unintentional anthropogenic transfer of colony fragments. Although supercolonial, F. paralugubris lacks some of the essential properties of invasive tramp ants - its species-specific preadaptations are not comparable with the situation in the imported European Fire Ant Myrmica rubra (LINNAEUS, 1758). A prediction of the role of F. paralugubris in the Nearctic forest ecosystems is presented. The concluded low risk of it becoming a dangerous invasive species does not refute the importance of keeping the situation in Quebec under careful observation.
Identifying homology between sex chromosomes of different species is essential to understanding the evolution of sex determination. Here, we show that the identity of a homomorphic sex chromosome pair can be established using a linkage map, without information on offspring sex. By comparing sex-specific maps of the European tree frog Hyla arborea, we find that the sex chromosome (linkage group 1) shows a threefold difference in marker number between the male and female maps. In contrast, the number of markers on each autosome is similar between the two maps. We also find strongly conserved synteny between H. arborea and Xenopus tropicalis across 200 million years of evolution, suggesting that the rate of chromosomal rearrangement in anurans is low. Finally, we show that recombination in males is greatly reduced at the centers of large chromosomes, consistent with previous cytogenetic findings. Our research shows the importance of high-density linkage maps for studies of recombination, chromosomal rearrangement and the genetic architecture of ecologically or economically
important traits.
In this study, conducted in French Guiana, a part of the native range of the fire ant Solenopsis saevissima, we compared the cuticular hydrocarbon profiles of media workers with previous results based on intraspecific aggressiveness tests. We noted a strong congruence between the two studies permitting us to delimit two supercolonies extending over large distances (up to 54 km), a phenomenon known as unicoloniality. Solenopsis geminata workers, taken as an out-group for cluster analyses, have a very different cuticular hydrocarbon profile. Because S. saevissima has been reported outside its native range, our conclusion is that this species has the potential to become invasive because unicoloniality (i.e., the main attribute for ants to become invasive) was shown at least for the Guianese population. This article is protected by copyright. All rights reserved.
This article is protected by copyright. All rights reserved.
Complex adaptive polymorphisms are common in nature, but what mechanisms maintain the underlying favorable allelic combinations [1-4]? The convergent evolution of polymorphic social organization in two independent ant species provides a great opportunity to investigate how genomes evolved under parallel selection. Here, we demonstrate that a large, nonrecombining ''social chromosome'' is associated with social organization in the Alpine silver ant, Formica selysi. This social chromosome shares architectural characteristics with that of the fire ant Solenopsis invicta [2], but the two show no detectable similarity in gene content. The discovery of convergence at two levels - the phenotype and the genetic architecture associated with alternative social forms - points at general genetic mechanisms underlying transitions in social organization. More broadly, our findings are consistent with recent theoretical studies suggesting that suppression of recombination plays a key role in facilitating coordinated shifts in coadapted traits [5, 6].
The Illumina paired-end sequencing technology can generate reads from both ends of target DNA fragments, which can subsequently be merged to increase the overall read length. There already exist tools for merging these paired-end reads when the target fragments are equally long. However, when fragment lengths vary and, in particular, when either the fragment size is shorter than a single-end read, or longer than twice the size of a single-end read, most state-of-the-art mergers fail to generate reliable results. Therefore, a robust tool is needed to merge paired-end reads that exhibit varying overlap lengths because of varying target fragment lengths.
We present the PEAR software for merging raw Illumina paired-end reads from target fragments of varying length. The program evaluates all possible paired-end read overlaps and does not require the target fragment size as input. It also implements a statistical test for minimizing false-positive results. Tests on simulated and empirical data show that PEAR consistently generates highly accurate merged paired-end reads. A highly optimized implementation allows for merging millions of paired-end reads within a few minutes on a standard desktop computer. On multi-core architectures, the parallel version of PEAR shows linear speedups compared to the sequential version of PEAR.
PEAR is implemented in C and uses POSIX threads. It is freely available at http://www.exelixis-lab.org/pear.
Tomas.Flouri@h-its.org.
Massively parallel short-read sequencing technologies, coupled with powerful software platforms, are enabling investigators to analyse tens of thousands of genetic markers. This wealth of data is rapidly expanding and allowing biological questions to be addressed with unprecedented scope and precision. The sizes of the data sets are now posing significant data processing and analysis challenges. Here we describe an extension of the Stacks software package to efficiently use genotype-by-sequencing data for studies of populations of organisms. Stacks now produces core population genomic summary statistics and SNP-by-SNP statistical tests. These statistics can be analysed across a reference genome using a smoothed sliding window. Stacks also now provides several output formats for several commonly used downstream analysis packages. The expanded population genomics functions in Stacks will make it a useful tool to harness the newest generation of massively parallel genotyping data for ecological and evolutionary genetics.
The correct identification of colony boundaries is an essential prerequisite for empirical studies of ant behaviour and evolution. Ant colonies function at various organizational levels, and these boundaries may be difficult to assess. Moreover, new complexity can be generated through the presence of spatially discrete subgroups within a more or less genetically homogeneous colony, a situation called polydomy. A colony is polydomous only if individuals (workers and brood) of its constituent nests function as a social and cooperative unit and are regularly interchanged among nests. This condition was previously called polycalic, and the term polydomy was used in a broader sense for a group of daughter nests of the same mother colony (implying limited female dispersal), without regard to whether these different nests continued to exchange individuals. We think that this distinction between ‘polycaly’ and ‘polydomy’ concerns two disparate concepts. We thus prefer the narrower definition of polydomy, which groups individuals that interact socially. Does this new level of organization affect the way in which natural selection acts on social traits? Here, after examining the history of terms, we review all ant species that have been described as expressing polydomous structures. We show that there is no particular syndrome of traits predictably associated with polydomy. We detail the existing theoretical predictions and empirical results on the ecology of polydomy, and the impact of polydomy on social evolution and investment strategies, while carefully distinguishing monogynous from polygynous species. Finally, we propose a methodology for future studies and offer ideas about what remains to be done. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 90, 319–348.
Ants are among the most damaging invasive species, and their success frequently arises from the widespread cooperation displayed by introduced populations, often across hundreds of kilometers. Previous studies of the invasive Argentine ant (Linepithema humile) have shown that introduced populations on different continents each contain a single, vast supercolony and, occasionally, smaller secondary colonies. Here, we perform inter-continental behavioral analyses among supercolonies in North America, Europe, Asia, Hawaii, New Zealand and Australia and show that these far-flung supercolonies also recognize and accept each other as if members of a single, globally distributed supercolony. Furthermore, populations also possess similar genetic and chemical profiles. However, these ants do show aggression toward ants from South Africa and the smaller secondary colonies that occur in Hawaii and California. Thus, the largest and most dominant introduced populations are likely descended from the same ancestral colony and, despite having been established more than 100 years ago, have diverged very little. This apparent evolutionary stasis is surprising because, in other species, some of the most rapid rates of evolutionary change have occurred in introduced populations. Given the spatial extent of the Argentine ant society we report here, there can be little doubt that this intercontinental supercolony represents the most populous known animal society.
Many invasive ants, including the Argentine ant Linepithema humile, form expansive supercolonies, within which intraspecific aggression is absent. The behavioral relationships among introduced
Argentine ant populations at within-country or within-continent scales have been studied previously, but the behavioral relationships
among intercontinental populations have not been examined. The present study investigated the levels of aggression among intercontinental
Argentine ant populations by transporting live ants from Europe and California to Japan and conducting aggression tests against
Japanese populations. Workers from the dominant supercolonies of Europe and California did not show aggressive behavior toward
workers from the dominant supercolony of Japan, whereas they fought vigorously against workers from minor supercolonies. The
three massive supercolonies, together with Argentine ants from Macaronesia, may be the largest non-aggressive unit formed
by a social insect species in which intraspecific aggression exists. Absence or low levels of aggression at transcontinental
scale, which may have derived from low genetic variation, may help introduced Argentine ants maintain expansive supercolonies.
The lack of aggression implies possible frequent exchanges of individuals among the intercontinental populations mediated
by human activities.
Ant colonies may have a single or several reproductive queens (monogyny and polygyny, respectively). In polygynous colonies, colony reproduction may occur by budding, forming multinest, polydomous colonies. In most cases, budding leads to strong genetic structuring within populations, and positive relatedness among nestmates. However, in a few cases, polydomous populations may be unicolonial, with no structuring and intra-nest relatedness approaching zero. We investigated the spatial organisation and genetic structure of a polygynous, polydomous population of Formica truncorum in Finland. F. truncorum shifts nest sites between hibernation and the reproductive season, which raises the following question: are colonies maintained as genetic entities throughout the seasons, or is the population unicolonial throughout the season? Using nest-specific marking and five microsatellite loci, we found a high degree of mixing between individuals of the population, and no evidence for a biologically significant genetic structuring. The nestmate relatedness was also indistinguishable from zero. Taken together, the results show that the population is unicolonial. In addition, we found that the population has undergone a recent bottleneck, suggesting that the entire population may have been founded by a very limited number of females. The precise causes for unicoloniality in this species remain open, but we discuss the potential influence of intra-specific competition, disintegration of recognition cues and the particular hibernation habits of this species.
We document the variation in number of queens occurring naturally in founding, immature and mature nests of the ant Formica podzolica, and compare development of colonies and survivorship of queens in experimental nests started with 1–16 foundresses. Number of queens per nest was associated with stage of colony development. Most nests were monogynous, but 20% of immature nests (n = 66) and 25% of mature nests (n = 92) were oligogynous or polygynous. Colonies were usually established by single queens (i.e., haplometrosis), but colony establishment by multiple queens (i.e., pleometrotis) was also common, occurring in 27% of founding nests (n = 492). Foundress groups in the field were small ( = 1.47 0.04 queens/nest), and large groups experienced high mortality and low productivity in artificial nests. Therefore, the many queens (up to 140) in some immature and mature colonies were probably secondarily pleometrotic. Experimental nests started with 1–4 queens were more successful than those initiated by 8 or 16 queens. Small groups (2–4 queens) produced more pupae before the first nests reared workers than single foundresses or larger groups (8 or 16 queens). Although single foundresses were less productive than queens in small groups, they experienced greater survivorship and less weight loss than queens in pleometrotic associations. Besides low productivity, queen mortality and weight loss were greatest in large groups.
Some of the most striking examples of phenotypic variation within species are controlled by supergenes. However, most research on supergenes has focused on their emergence and long-term maintenance, leaving the later stages of their life cycle largely unexplored. Specifically, what happens to a derived supergene haplotype when the trait it controls reaches fixation? Here we answer this question using the ancient supergene system of Formica ants, where (monogynous) single-queen colonies carry only the ancestral haplotype M while the derived haplotype P is exclusive to (polygynous) colonies with multiple queens. Through comparative genomics of all seven European wood ant species, we found that the P haplotype was present in only one of the three obligate polygynous species ( F. polyctena ). In the two others ( F. aquilonia and F. paralugubris ) the P haplotype was completely missing except for duplicated P-specific paralogs of two genes, Zasp52 and TTLL2 , with Zasp52 being directly involved in wing muscle development. We hypothesize that these genes play a direct role in polygyny and contribute to differences in body size and/or dispersal behaviour between monogynous and polygynous queens. A complete lack of P/P genotypes among the 136 workers suggest strong selection against such genotypes. While our analyses did not reveal evidence of increased mutation load on the P, it is possible that this skew in genotype distributions is driven by a few loci with strong fitness effects. We propose that selection to escape P-associated fitness costs underlies the loss of this haplotype in obligate polygynous wood ants.
Supergenes are clusters of tightly linked genes that jointly produce complex phenotypes. Although widespread in nature, how such genomic elements are formed and how they spread are in most cases unclear. In the fire ant Solenopsis invicta and closely related species, a “social supergene controls whether a colony maintains one or multiple queens. Here, we show that the three inversions constituting the Social b ( Sb ) supergene emerged sequentially during the separation of the ancestral lineages of S. invicta and Solenopsis richteri . The two first inversions arose in the ancestral population of both species, while the third one arose in the S. richteri lineage. Once completely assembled in the S. richteri lineage, the supergene first introgressed into S. invicta , and from there into the other species of the socially polymorphic group of South American fire ant species. Surprisingly, the introgression of this large and important genomic element occurred despite recent hybridization being uncommon between several of the species. These results highlight how supergenes can readily move across species boundaries, possibly because of fitness benefits they provide and/or expression of selfish properties favoring their transmission.
Background
Supergenes are chromosomal regions with tightly linked clusters of alleles that control compound phenotypic traits. Supergenes have been demonstrated to contribute to the maintenance of polymorphisms within populations in traits as diverse as mimetic wing coloration in butterflies, mating strategies in birds, and malarial susceptibility in mosquitoes. A large supergene also underlies variation in social organization in Formica ants. Alternative supergene haplotypes are associated with the presence of either a single queen (monogyny) or multiple queens (polygyny) within colonies. Here, we assess the social structure and supergene status of the North American species Formica neoclara .
Results
We sequenced a subset of the genome in 280 individuals sampled in populations from California to northern British Columbia using ddRADseq. We determined that F. neoclara is socially polymorphic in queen number, and we show that the social polymorphism is associated with alternative haplotypes at the social supergene. Intriguingly, polygyne colonies can harbor workers that are homozygous for both haplotypes as well as heterozygotes.
Conclusions
This colony genetic composition contrasts with other Formica species, in which almost all individuals in polygyne colonies have the polygyne-associated haplotype. The social polymorphism is present in widely distributed and genetically subdivided populations of F. neoclara. In studying this system in F. neoclara , we expand our understanding of the functional evolution of supergene haplotypes as they diverge in different lineages.
Supergenes, regions of the genome with suppressed recombination between sets of functional mutations, contribute to the evolution of complex phenotypes in diverse systems. Excluding sex chromosomes, most supergenes discovered so far appear to be young, being found in one species or a few closely related species. Here, we investigate how a chromosome harboring an ancient supergene has evolved over about 30 Ma. The Formica supergene underlies variation in colony queen number in at least five species. We expand previous analyses of sequence divergence on this chromosome to encompass about 90 species spanning the Formica phylogeny. Within the non‐recombining region, the gene knockout contains 22 single nucleotide polymorphisms (SNPs) that are consistently differentiated between two alternative supergene haplotypes in divergent European Formica species, and we show that these same SNPs are present in most Formica clades. In these clades, including an early diverging Nearctic Formica clade, individuals with alternative genotypes at knockout also have higher differentiation in other portions of this chromosome. We identify hotspots of SNPs along this chromosome that are present in multiple Formica clades to detect genes that may have contributed to the emergence and maintenance of the genetic polymorphism. Finally, we infer three gene duplications on one haplotype, based on apparent heterozygosity within these genes in the genomes of haploid males. This study strengthens the evidence that this supergene originated early in the evolution of Formica and that just a few loci in this large region of suppressed recombination retain strongly differentiated alleles across contemporary Formica lineages.
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.
Although social behavior can have a strong genetic component, it can also result in selection on genome structure and function, thereby influencing the evolution of the genome itself. Here we explore the bidirectional links between social behavior and genome architecture by considering variation in social and/or mating behavior among populations (social polymorphisms) and across closely related species. We propose that social behavior can influence genome architecture via associated demographic changes due to social living. We establish guidelines to exploit emerging whole-genome sequences using analytical approaches that examine genome structure and function at different levels (regulatory vs structural variation) from the perspective of both molecular biology and population genetics in an ecological context.
We used microsatellites to study the fine-scale genetic structure of a highly polygynous and largely unicolonial population of the ant Formica paralugubris. Genetic data indicate that long-distance gene flow between established nests is limited and new queens are primarily recruited from within their natal nest. Most matings occur between nestmates and are random at this level. In the center of the study area, budding and permanent connections between nests result in strong population viscosity, with close nests being more similar genetically than distant nests. In contrast, nests located outside of this supercolony show no isolation by distance, suggesting that they have been initiated by queens that participated in mating flights rather than by budding from nearby nests in our sample population. Recruitment of nestmates as new reproductive individuals and population viscosity in the supercolony increase genetic differentiation between nests. This in turn inflates relatedness estimates among worker nestmates (r = 0.17) above what is due to close pedigree links. Local spatial genetic differentiation may favor the maintenance of altruism when workers raise queens that will disperse on foot and compete with less related queens from neighboring nests or disperse on the wing and compete with unrelated queens.
This new edition to the classic book by ggplot2 creator Hadley Wickham highlights compatibility with knitr and RStudio. ggplot2 is a data visualization package for R that helps users create data graphics, including those that are multi-layered, with ease. With ggplot2, it's easy to:
• produce handsome, publication-quality plots with automatic legends created from the plot specification
• superimpose multiple layers (points, lines, maps, tiles, box plots) from different data sources with automatically adjusted common scales
• add customizable smoothers that use powerful modeling capabilities of R, such as loess, linear models, generalized additive models, and robust regression
• save any ggplot2 plot (or part thereof) for later modification or reuse
• create custom themes that capture in-house or journal style requirements and that can easily be applied to multiple plots
• approach a graph from a visual perspective, thinking about how each component of the data is represented on the final plot
This book will be useful to everyone who has struggled with displaying data in an informative and attractive way. Some basic knowledge of R is necessary (e.g., importing data into R). ggplot2 is a mini-language specifically tailored for producing graphics, and you'll learn everything you need in the book. After reading this book you'll be able to produce graphics customized precisely for your problems, and you'll find it easy to get graphics out of your head and on to the screen or page. New to this edition:<
• Brings the book up-to-date with ggplot2 1.0, including major updates to the theme system
• New scales, stats and geoms added throughout
• Additional practice exercises
• A revised introduction that focuses on ggplot() instead of qplot()
• Updated chapters on data and modeling using tidyr, dplyr and broom
In unicolonial populations of ants, individuals can mix freely within large networks of nests that contain many queens. It has been proposed that the absence of aggression in unicolonial populations stems from a loss of nest mate recognition, but few studies have tested this hypothesis. We investigated patterns of aggression and nest mate recognition in the unicolonial wood ant, Formica paralugubris. Little aggression occurred, even between workers from nests separated by up to 5 km. However, when aggression took place, it was directed toward non–nest mates rather than nest mates. Trophallaxis (exchange of liquid food) occurred very frequently, and surprisingly, workers performed significantly more trophallaxis with non–nest mates than with nest mates (bias 2.4:1). Hence, workers are able to discriminate nest mates from non–nest mates. Higher rates of trophallaxis between non–nest mates may serve to homogenize the colony odor or may be an appeasement mechanism. Trophallaxis rate and aggression level were not correlated with geographical distance and did not differ within and between two populations separated by several kilometers. Hence, these populations do not represent differentiated supercolonies with clear-cut behavioral boundaries. Overall, the data demonstrate that unicoloniality can evolve despite well-developed nest mate recognition. Reduced levels of aggression might have been favored by the low rate of interactions with foreign workers, high cost of erroneously rejecting nest mates, and low cost of accepting foreign workers. Key words: aggression, discrimination, kin recognition, unicoloniality. [Behav Ecol]
Recently considerable research has focused on the causes of evolution of multiple-queen (polygynous) colonies. In order to better understand the factors which may have led to these polygynous associations it is vital to compare the reproductive success of queens in monogynous (one queen per colony) and polygynous colonies as well as the relative fitness of queens in polygynous colonies. This paper addresses the difficulties arising from such comparisons and their implications with regard to the methods commonly used to assess reproductive success in queens. The relative reproductive success of queens in monogynous and polygynous colonies is commonly assessed by comparing the relative number of reproductives they produce during a single reproductive season. However, shift in queen number seems to be only one aspect of a profound shift in social structure and reproductive strategy that constitutes, in effect, a "polygyny syndrome'. For example, female reproductives produced in polygynous colonies frequently use a different mode of colony founding, which in turn affects the probability of their survival. Furthermore, queens from monogynous and polygynous colonies frequently differ in their life-span and the number of sexual broods they produce. As a result, the reproductive success of queens in monogynous and polygynous colonies may not be directly related to the relative number of sexuals they produce during a single reproductive season. -Author
Ant supercolonies (large networks of interconnected nests) represent the most extreme form of multi-queen breeding (polygyny) and have been found across ant lineages, usually in specific long-term stable populations. Many studies on the genetic population structure and demography of ant supercolonies have been done in recent decades, but they have lacked multicolonial control patches with separated colonies headed by a single or few queens so the origin of the supercolonial trait syndrome has remained enigmatic. Here, we set out to compare sympatric supercolonial and multicolonial patches in two natural Danish populations of the common red ant Myrmica rubra. We used DNA microsatellites to reconstruct genetic colony/population structure and obtained morphological and density measurements to estimate life history and ecology covariates. We found that supercolonies in both populations completely dominated their patches whereas colonies in multicolonial patches coexisted with other ant species. Supercolony patches had very low genetic differentiation between nests, negligible relatedness within nests, and lower inbreeding than multicolonial patches, but there were no significant morphological differences. One population also had nests that approached true outbred monogyny with larger workers and males but smaller queens than in the two other social nest types. Our results suggest that once smaller colonies start to adopt additional queens, they also gain the potential to ultimately become supercolonial when the habitat allows rapid expansion through nest budding. This is relevant for understanding obligate polygyny in ants and for appreciating how and why introduced North American populations of M. rubra have recently become invasive.
Adaptation is commonly a multidimensional problem, with changes in multiple traits required to match a complex environment. This is epitomized by balanced polymorphisms in which multiple phenotypes co-exist and are maintained in a population by a balance of selective forces. Consideration of such polymorphisms led to the concept of the supergene, where alternative phenotypes in a balanced polymorphism segregate as if controlled by a single genetic locus, resulting from tight genetic linkage between multiple functional loci. Recently, the molecular basis for several supergenes has been resolved. Thus, major chromosomal inversions have been shown to be associated with polymorphisms in butterflies, ants and birds, offering a mechanism for localised reduction in recombination. In several examples of plant self-incompatibility, the functional role of multiple elements within the supergene architecture has been demonstrated, conclusively showing that balanced polymorphism can be maintained at multiple coadapted and tightly linked elements. Despite recent criticism, we argue that the supergene concept remains relevant and is more testable than ever with modern molecular methods.Heredity advance online publication, 19 March 2014; doi:10.1038/hdy.2014.20.
Human impact on boreal forests has been extensive during a fairly short evolutionary time scale. Character species of boreal forests, such as Formica ants, may face loss of genetic diversity, increasing inbreeding, and decreasing gene flow among extant habitat fragments owing to habitat loss and fragmentation. Here we review the genetic data on old-world boreal species of the genus Formica. In Formica ants colonies can have one or several queens (mono- and polygyny respectively) and this trait is often assumed to be linked with dispersal propensity, such that monogyne species disperse well and polygyne species disperse less well. Our analysis of the available data reveals three important aspects of the social and dispersal biology of Formica. First, the traditional division in mono- and polygyne species is too simple and we propose a population-based division into highly polygyne, weakly or moderately polygyne, and monogyne populations. Second, there is indeed an association between colony kin structure and dispersal in the predicted direction, i.e. restricted dispersal in polygyne species. However, this only holds for between-population differentiation, not within population genetic viscosity. When genetic viscosity within populations was examined most species nevertheless showed a negative relationship between F1s and relatedness, indicating that low relatedness (many queens) is associated with reduced dispersal also locally. Only one species (F. exsecta) showed a significant positive relationship. Finally, we predict that sex-biased dispersal may be a common trait in Formica species, although data on more species are needed to confirm this.
Significance
Genome scans often find that the loci involved in local adaptation tend to cluster together on chromosomes. A leading explanation suggests that clusters evolve because the probability of a new mutation establishing is higher when occurring near another locally adapted mutation, because such architectures are seldom disrupted by recombination. I show that this theory is unlikely to explain empirically observed clusters. Instead, simulations show that clusters are more likely to form through genomic rearrangements that bring coadapted loci close together. This suggests that ecological selection may play an important role in shaping genome architecture, in contrast to many nonadaptive explanations.
According to the inclusive fitness theory, some degree of positive relatedness is required for the evolution and maintenance of altruism. However, ant colonies are sometimes large interconnected networks of nests, which are genetically homogenous entities, causing a putative problem for the theory. We studied spatial structure and genetic relatedness in two supercolonies of the ant Formica exsecta, using nuclear and mitochondrial markers. We show that there may be multiple pathways to supercolonial social organization leading to different spatial genetic structures. One supercolony formed a genetically homogenous population dominated by a single mtDNA haplotype, as expected if founded by a small number of colonizers, followed by nest propagation by budding and domination of the habitat patch. The other supercolony had several haplotypes, and the spatial genetic structure was a mosaic of nuclear and mitochondrial clusters. Genetic diversity probably originated from long-range dispersal, and the mosaic population structure is likely a result of stochastic short-range dispersal of individuals. Such a mosaic spatial structure is apparently discordant with the current knowledge about the integrity of ant colonies. Relatedness was low in both populations when estimated among nestmates, but increased significantly when estimated among individuals sharing the same genetic cluster or haplogroup. The latter association indicates the important historical role of queen dispersal in the determination of the spatial genetic structure.
Genetic organization of colonies and populations of the ant Formica aquilonia were studied at the edge of the urban area of the city of Helsinki within an area of about 400 km 2 . Over six thousand old queens and workers were sampled from a total of 288 nest mounds from 14 populations (patches of forest) for an allozyme study, and workers from 13–15 nests in each of three populations were also characterized by microsatel-lite genotyping. Genetic relatedness among nest mates within populations was close to zero for both queens (estimates ranging from 0.02 to 0.13) and workers (from 0.01 to 0.22), with some of the estimates being significantly greater than zero. These results supported the view of a high level of polygyny within the nests. The populations showed significant genetic differences both at the allozyme loci (overall F ST = 0.17) and at the microsatellites (F ST = 0.24). The estimates of F ST between pairs of popula-tions varied from 0.01 to 0.61, the largest values being associated to reduced genetic variation and an apparent bottleneck within one population. The results showed that the local populations of this highly polygynous (multiple queens in a nest) and polydo-mous (multiple nests in a colony) ant can be differentiated genetically within potential dispersal distances, suggesting restricted dispersal and possible bottlenecks when colo-nizing new patches of forest.
The pervasive social and ecological differences between ant colonies that have a single queen and those that have multiple queens are defined. The evolutionary tendencies which lead to polygyny and the adaptive significance of multiple queens are examined. The discussion of the ecological consequences of polygyny and monogyny leads to a deeper understanding of territoriality, spacing and species packing in ants.