Jes S. Pedersen

Evolution of supercolonies: The Argentine ants of southern Europe

Some ants have an extraordinary social organization, called unicoloniality, whereby individuals mix freely among physically separated nests. This type of social organization is not only a key attribute responsible for the ecological domination of these ants, but also an evolutionary paradox and a potential problem for kin selection theory because relatedness between nest mates is effectively zero. The introduction of the Argentine ant in Europe was apparently accompanied by a dramatic loss of inter-nest aggression and the formation of two immense supercolonies (which effectively are two unicolonial populations). Introduced populations experienced only limited loss of genetic diversity at neutral markers, indicating that the breakdown of recognition ability is unlikely to be merely due to a genetic bottleneck. Rather, we suggest that a “genetic cleansing” of recognition cues occurred after introduction. Indeed workers of the same supercolony are never aggressive to each other despite the large geographical distance and considerable genetic differentiation between sampling sites. By contrast, aggression is invariably extremely high between the two supercolonies, indicating that they have become fixed for different recognition alleles. The main supercolony, which ranges over 6,000 km from Italy to the Spanish Atlantic coast, effectively forms the largest cooperative unit ever recorded.

NATIVE SUPERCOLONIES OF UNRELATED INDIVIDUALS IN THE INVASIVE ARGENTINE ANT

Abstract Kinship among group members has long been recognized as a main factor promoting the evolution of sociality and reproductive altruism, yet some ants have an extraordinary social organization, called unicoloniality, whereby individuals mix freely among physically separated nests. This type of social organization is not only a key attribute responsible for the ecological dominance of these ants, but also an evolutionary paradox because relatedness between nestmates is effectively zero. Recently, it has been proposed that, in the Argentine ant, unicoloniality is a derived trait that evolved after its introduction into new habitats. Here we test this basic assumption by conducting a detailed genetic analysis of four native and six introduced populations with five to 15 microsatellite loci and one mitochondrial gene. In contrast to the assumption that native populations consist of family‐based colonies with related individuals who are aggressive toward members of other colonies, we found that native populations also form supercolonies, and are effectively unicolonial. Moreover, just as in introduced populations, the relatedness between nestmates is not distinguishable from zero in these native range supercolonies. Genetic differentiation between native supercolonies was very high for both nuclear and mitochondrial markers, indicating extremely limited gene flow between supercolonies. The only important difference between the native and introduced populations was that supercolonies were several orders of magnitude smaller in the native range (25‐500 m). This size difference has important consequences for our understanding of the evolution and stability of unicolonial structures because the relatively small size of supercolonies in the native range implies that competition can occur between supercolonies, which can act as a break on the spread of selfish mutants by eliminating supercolonies harboring them.

Relative roles of climatic suitability and anthropogenic influence in determining the pattern of spread in a global invader

Because invasive species threaten the integrity of natural ecosystems, a major goal in ecology is to develop predictive models to determine which species may become widespread and where they may invade. Indeed, considerable progress has been made in understanding the factors that influence the local pattern of spread for specific invaders and the factors that are correlated with the number of introduced species that have become established in a given region. However, few studies have examined the relative importance of multiple drivers of invasion success for widespread species at global scales. Here, we use a dataset of >5,000 presence/absence records to examine the interplay between climatic suitability, biotic resistance by native taxa, human-aided dispersal, and human modification of habitats, in shaping the distribution of one of the worlds most notorious invasive species, the Argentine ant (Linepithema humile). Climatic suitability and the extent of human modification of habitats are primarily responsible for the distribution of this global invader. However, we also found some evidence for biotic resistance by native communities. Somewhat surprisingly, and despite the often cited importance of propagule pressure as a crucial driver of invasions, metrics of the magnitude of international traded commodities among countries were not related to global distribution patterns. Together, our analyses on the global-scale distribution of this invasive species provide strong evidence for the interplay of biotic and abiotic determinants of spread and also highlight the challenges of limiting the spread and subsequent impact of highly invasive species.

Ant parasite queens revert to mating singly

Multiple mating (polyandry) is widespread among animal groups, particularly insects. But the factors that maintain it and underlie its evolution are hard to verify because benefits and costs are not easily quantified and they tend to be similar in related species. Here we compare the mating strategies of the leaf-cutting ant Acromyrmex echinatior and its recently derived social parasite Acromyrmex insinuator, which is also its closest relative (see Fig. 1). We find that although the host queens mate with up to a dozen different males, the social parasite mates only singly. This rapid and surprising reversion to single mating in a socially parasitic ant indicates that the costs of polyandry are probably specific to a free-living lifestyle.

The Evolution of Invasiveness in Garden Ants

It is unclear why some species become successful invaders whilst others fail, and whether invasive success depends on pre-adaptations already present in the native range or on characters evolving de-novo after introduction. Ants are among the worst invasive pests, with Lasius neglectus and its rapid spread through Europe and Asia as the most recent example of a pest ant that may become a global problem. Here, we present the first integrated study on behavior, morphology, population genetics, chemical recognition and parasite load of L. neglectus and its non-invasive sister species L. turcicus. We find that L. neglectus expresses the same supercolonial syndrome as other invasive ants, a social system that is characterized by mating without dispersal and large networks of cooperating nests rather than smaller mutually hostile colonies. We conclude that the invasive success of L. neglectus relies on a combination of parasite-release following introduction and pre-adaptations in mating system, body-size, queen number and recognition efficiency that evolved long before introduction. Our results challenge the notion that supercolonial organization is an inevitable consequence of low genetic variation for chemical recognition cues in small invasive founder populations. We infer that low variation and limited volatility in cuticular hydrocarbon profiles already existed in the native range in combination with low dispersal and a highly viscous population structure. Human transport to relatively disturbed urban areas thus became the decisive factor to induce parasite release, a well established general promoter of invasiveness in non-social animals and plants, but understudied in invasive social insects.

The introduction history of invasive garden ants in Europe: Integrating genetic, chemical and behavioural approaches

BackgroundThe invasive garden ant, Lasius neglectus, is the most recently detected pest ant and the first known invasive ant able to become established and thrive in the temperate regions of Eurasia. In this study, we aim to reconstruct the invasion history of this ant in Europe analysing 14 populations with three complementary approaches: genetic microsatellite analysis, chemical analysis of cuticular hydrocarbon profiles and behavioural observations of aggression behaviour. We evaluate the relative informative power of the three methodological approaches and estimate both the number of independent introduction events from a yet unknown native range somewhere in the Black Sea area, and the invasive potential of the existing introduced populations.ResultsThree clusters of genetically similar populations were detected, and all but one population had a similar chemical profile. Aggression between populations could be predicted from their genetic and chemical distance, and two major clusters of non-aggressive groups of populations were found. However, populations of L. neglectus did not separate into clear supercolonial associations, as is typical for other invasive ants.ConclusionThe three methodological approaches gave consistent and complementary results. All joint evidence supports the inference that the 14 introduced populations of L. neglectus in Europe likely arose from only very few independent introductions from the native range, and that new infestations were typically started through introductions from other invasive populations. This indicates that existing introduced populations have a very high invasive potential when the ants are inadvertently spread by human transport.

Extreme queen-mating frequency and colony fission in African army ants

Army ants have long been suspected to represent an independent origin of multiple queen‐mating in the social Hymenoptera. Using microsatellite markers, we show that queens of the African army ant Dorylus (Anomma) molestus have the highest absolute (17.3) and effective (17.5) queen‐mating frequencies reported so far for ants. This confirms that obligate multiple queen‐mating in social insects is associated with large colony size and advanced social organization, but also raises several novel questions. First, these high estimates place army ants in the range of mating frequencies of honeybees, which have so far been regarded as odd exceptions within the social Hymenoptera. Army ants and honeybees are fundamentally different in morphology and life history, but are the only social insects known that combine obligate multiple mating with reproduction by colony fission and extremely male‐biased sex ratios. This implies that the very high numbers of matings in both groups may be due partly to the relatively low costs of additional matings. Second, we were able to trace recent events of colony fission in four of the investigated colonies, where the genotypes of the two queens were only compatible with a mother–daughter relationship. A direct comparison of male production between colonies with offspring from one and two queens, respectively, suggested strongly that new queens do not produce a sexual brood until all workers of the old queen have died, which is consistent with kin selection theory.

Effect of habitat saturation on the number and turnover of queens in the polygynous ant, Myrmica sulcinodis

In polygynous social insects more than one queen reproduces in a colony. In such populations ecological factors affecting survival and reproduction of queens are likely to be of prime importance for social organization. In particular, habitat saturation leading to severe limitations in the availability of nest sites has been suggested to promote high queen number. In this study we examine the social and genetic structure of colonies in the polygynous ant Myrmica sulcinodis. We investigated a single breeding population in two adjacent habitats which differed markedly in the availability of nest sites. In the main habitat M. sulcinodis occupied almost all suitable nest sites, whereas in the other (marginal) habitat most sites were unoccupied by ants, due to a recent fire. In support of the habitat saturation hypothesis, the number of queens per colony which could explain the estimated relatedness among workers was almost five times higher for the main habitat than for the marginal habitat. This is the first demonstration that the kin structure of a social insect population is plastic and responds adaptively to short‐term changes in ecological constraints such as nest site availability. Based on combined genetic and demographic data we discuss queen reproductive strategies and suggest that a special class of queen ‘floaters’ only stays ephemerally in the colonies, thus causing a substantial turnover of reproducing queens across years.

Loss of Wolbachia infection during colonisation in the invasive Argentine ant Linepithema humile

Wolbachia are maternally inherited bacteria, which are very common in arthropods and nematodes. Wolbachia infection may affect host reproduction through feminisation, parthenogenesis, male-killing, cytoplasmic incompatibility and increased fecundity. Previous studies showing discrepancies between the phylogenies of Wolbachia and its arthropod hosts indicate that infection is frequently lost, but the causes of symbiont extinction have so far remained elusive. Here, we report data showing that colonisation of new habitats is a possible mechanism leading to the loss of infection. The presence and prevalence of Wolbachia were studied in three native and eight introduced populations of the Argentine ant Linepithema humile. The screening shows that the symbiont is common in the three native L. humile populations analysed. In contrast, Wolbachia was detected in only one of the introduced populations. The loss of infection associated with colonisation of new habitats may result from drift (founder effect) or altered selection pressures in the new habitat. Furthermore, a molecular phylogeny based on sequences of the Wolbachia wsp gene indicates that L. humile has been infected by a single strain. Horizontal transmission of the symbiont may be important in ants as suggested by the sequence similarity of strains in the three genera Linepithema, Acromyrmex, and Solenopsis native from South and Central America.

Multiple paternity in social Hymenoptera: estimating the effective mate number in single–double mating populations

Several hypotheses have been advanced to explain the widespread occurrence of multiple mating by queens in eusocial bees, wasps and ants. In order to test competing hypotheses, it is essential to obtain an accurate description of the distribution of mate number and the mates’ respective contributions to the brood in populations under study. In this study we examine current methods for estimating the effective mate number and other paternity frequency parameters in populations dominated by single and double mating of queens, based on genetical data from parent–offspring combinations. Estimation errors are due to limited sample size of offspring (nonsampling error) and limited variation of genetic markers (nondetection error). We demonstrate that limited sample size of offspring leads to an underestimation of the paternity contribution from the majority male of double‐mated queens (the paternity skew or sperm bias), thus overestimating the effectiveness of double matings and underestimating the population frequency of double‐mated queens. We propose a calculation procedure which avoids this bias. Furthermore, we propose a general method to correct simultaneously for errors from nondetection and nonsampling when estimating the population frequency of double‐mated queens. The calculation procedures presented are designed for male‐haplodiploid social Hymenoptera but some can be applied directly to studies of diplo‐diploid mating systems where single and double mating prevail. This has particular relevance to vertebrate studies where the number of offspring studied per mother is invariably low. The remaining calculation procedures are conceptually widely applicable, but details would have to be modified for other than haplodiploid mating systems.