Ants are some of the most abundant and familiar animals on Earth, and they play vital roles in most terrestrial ecosystems. Although all ants are eusocial, and display a variety of complex and fascinating behaviors, few genomic resources exist for them. Here, we report the draft genome sequence of a particularly widespread and well-studied species, the invasive Argentine ant ( Linepithema humile ), which was accomplished using a combination of 454 (Roche) and Illumina sequencing and community-based funding rather than federal grant support. Manual annotation of >1,000 genes from a variety of different gene families and functional classes reveals unique features of the Argentine ant's biology, as well as similarities to Apis mellifera and Nasonia vitripennis . Distinctive features of the Argentine ant genome include remarkable expansions of gustatory (116 genes) and odorant receptors (367 genes), an abundance of cytochrome P450 genes (>110), lineage-specific expansions of yellow/major royal jelly proteins and desaturases, and complete CpG DNA methylation and RNAi toolkits. The Argentine ant genome contains fewer immune genes than Drosophila and Tribolium , which may reflect the prominent role played by behavioral and chemical suppression of pathogens. Analysis of the ratio of observed to expected CpG nucleotides for genes in the reproductive development and apoptosis pathways suggests higher levels of methylation than in the genome overall. The resources provided by this genome sequence will offer an abundance of tools for researchers seeking to illuminate the fascinating biology of this emerging model organism.
SUMMARY 1. Adaptive maternal programming occurs when mothers alter their offspring's phenotype in response to environmental information such that it improves offspring fitness. When a mother's environment is predictive of the conditions her offspring are likely to encounter, such transgenerational plasticity enables offspring to be better-prepared for this particular environment. However, maternal effects can also have deleterious effects on fitness. 2. Here, we test whether female threespined stickleback fish exposed to predation risk adaptively prepare their offspring to cope with predators. We either exposed gravid females to a model predator or not, and compared their offspring's antipredator behaviour and survival when alone with a live predator. Importantly, we measured offspring behaviour and survival in the face of the same type of predator that threatened their mothers (Northern pike). 3. We did not find evidence for adaptive maternal programming; offspring of predator-exposed mothers were less likely to orient to the predator than offspring from unexposed mothers. In our predation assay, orienting to the predator was an effective antipredator behaviour and those that oriented, survived for longer. 4. In addition, offspring from predator-exposed mothers were caught more quickly by the predator on average than offspring from unexposed mothers. The difference in antipredator behaviour between the maternal predator-exposure treatments offers a potential behavioural mechanism contributing to the difference in survival between maternal treatments. 5. However, the strength and direction of the maternal effect on offspring survival depended on offspring size. Specifically, the larger the offspring from predator-exposed mothers, the more vulnerable they were to predation compared to offspring from unexposed mothers. 6. Our results suggest that the predation risk perceived by mothers can have long-term behavioural and fitness consequences for offspring in response to the same predator. These stress-mediated maternal effects can have nonadaptive consequences for offspring when they find themselves alone with a predator. In addition, complex interactions between such maternal effects and offspring traits such as size can influence our conclusions about the adaptive nature of maternal effects.
Aim The Argentine ant, Linepithema humile, has been spreading via human activities from its native range in South America across much of the globe for more than a century. This invasive ant was first detected in Japan in 1993. Its successful world‐wide expansion is attributed to a social structure, namely supercoloniality, whereby individuals from separate nests cooperate. Here, we examined the genetic structure of L. humile populations to understand its invasion history. Location Japan. Methods We analysed mitochondrial DNA of Linepithema humile workers from native and other introduced populations and then integrated previously registered sequences. Results Sequencing revealed six haplotypes distributed across its introduced ranges, of which five were present in Japan. The first haplotype was shared by the dominant Japanese, European, North American, Australian and New Zealand supercolonies; the second by the Kobe C supercolony and a Florida population; and the third by the Kobe B and secondary Californian supercolonies and North Carolina colonies. The remaining three haplotypes were each restricted to the Kobe A, Tokyo and Catalonian supercolonies, respectively. Each of the five mutually antagonistic supercolonies was fixed for one of the five haplotypes, and multiple supercolonies were found within a small area. Main conclusions The large number of haplotypes found in Japan likely reflects the strong propagule pressure of L. humile resulting from the fact that the country is one of the top five importers of trade commodities world‐wide. The short invasion history of L. humile in Japan could explain the maintenance of genetic diversity of each independent introduction. In addition, our sampling mostly occurred at major international shipping ports that are likely to be primary sites of introduction. The several recently established L. humile populations within a small area in Japan provide an opportunity to identify the sources of introduction and the local patterns of spread.
The success of invasive ants is frequently attributed to genetic and behavioural shifts in colony structure during or after introduction. The Argentine ant (Linepithema humile), a global invader, differs in colony genetic structure and behaviour between native populations in South America and introduced populations in Europe, Japan, New Zealand and North America. However, little is known about its colony structure in Australia. We investigated the genetic structure and behaviour of L. humile across Melbourne, Victoria by quantifying variation at four microsatellite loci and assaying intraspecific aggression at neighbourhood (30-200 m), fine (1-3.3 km) and regional (5-82 km) spatial scales. Hierarchical analyses across these scales revealed that most genetic variation occurred among workers within nests (~98%). However, although low genetic differentiation occurred among workers between nests at the fine and regional scales (~2%), negligible differentiation was detected among workers from neighbouring nests. Spatial genetic autocorrelation analysis confirmed that neighbouring nests were genetically more similar to each other. Lack of aggression within and across these scales supported the view that L. humile is unicolonial and forms a large supercolony across Melbourne. Comparisons of genetic structure of L. humile among single nests sampled from Adelaide, Brisbane, Hobart and Perth with Melbourne showed no greater levels of genetic differentiation or dissimilar spatial structure, suggesting an Australia-wide supercolony.
Biological invasions have significant ecological, evolutionary and economic consequences. Ants are exemplary invaders and their invasion success is frequently attributed to a shift in social structure between native and introduced populations. Here, we use a multidisciplinary approach to determine the social structure, origin and expansion of the invasive Argentine ant, Linepithema humile, in Australia by linking behavioural and genetic studies with indicators of dispersal pathways and propagule pressure. Behavioural assays revealed a complete absence of aggression within and between three cities – Melbourne, Adelaide and Perth – spanning 2700 km across Australia. Microsatellite analyses showed intracity genetic homogeneity and limited but significant intercity genetic differentiation. Exceptions were two Perth nests that likely represent independent translocations from Adelaide. These patterns suggest efficient local gene flow with more limited jump dispersal via transport corridors between cities. Microsatellite analyses of L. humile from potential source regions, combined with data from port interceptions, trade pathways and the timeline of spread within Australia, implicate the main European supercolony as the source of L. humile in Melbourne. Such an introduction probably then redistributed across Australia and spread to New Zealand to form an expansive Australasian supercolony.
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