Population genetic structure and male-biased dispersal in the queenless ant Diacamma cyaneiventre

In this study we investigated the population genetic structure of the queenless ant Diacamma cyaneiventre. This species, lacking winged queens, is likely to have a restricted female dispersal. We used both mitochondrial and microsatellite markers to assess the consequence of such restricted female dispersal at three geographical scales: within a given locality (< 1 km), between localities within a given region (< 10 km) and between regions (> 36 km). Within a locality, a strong population structure was observed for mitochondrial DNA (mtDNA) whereas weak or nonexistent population genetic structure was observed for the microsatellites (around 5% of the value for mtDNA). Male gene flow was estimated to be about 20-30 times higher than female gene flow at this scale. At a larger spatial scale, very strong genetic differentiation for both markers was observed between localities - even within a single region. Female dispersal is nonexistent at these scales and male dispersal is very restricted, especially between regions. The phylogeographical structure of the mtDNA haplotypes as well as the very low genetic diversity of mtDNA within localities indicate that new sites are colonized by a single migration event from adjacent localities, followed by successive colony fissions. These patterns of genetic variability and differentiation agree with what is theoretically expected when colonization events are kin-structured and when, following colonization, dispersion is mainly performed by males.     

Influence of colony associated factors on nest selection in an Indian queenless ant

1. Organisms face the difficult task of selecting an optimal new nest from the available options during relocation. Studies on honeybees and ants in their natural habitat indicate that scouts encounter multiple options that vary in their physical and biotic characteristics. 2. Architectural features, location, odour, and the presence of nest mates impact their choice of nest site selection. In order to examine the influence of diverse parameters on final nest site selection we conducted choice experiments on ants in the context of relocation. 3. After controlling for any influence by physical characteristics, we found that the presence of brood, adults, and colony odour acted as attractants with more colonies relocating into these new nests than expected by chance alone. In contrast, the presence of a reproductive female, or familiarity of location had no influence on the choice. New nests containing dead ants evoked cleaning responses from scouts, which may interfere with relocation into these nests. 4. Even although colonies consist of hundreds of adults and brood, colony integrity was maintained in 98.7% of colonies. Furthermore, we found that none of the eight studied colonies relocated when faced with minor flooding in their natural habitat, indicating that the cost of relocation is non‐trivial and that this species is capable of minor damage repairs. 5. These observations highlight the complexity of relocation in general, allow the characterisation of desirable nest attributes in this species, and highlight the need for similar exploration in other social insects.     

Identification of polymorphic microsatellite loci in the queenless,ponerine ant Diacamma ceylonense

Diacamma ceylonense is a queenless, ponerine ant whose colonies are headed by a single, mated, egg‐laying worker referred to as the gamergate. Thus, new colonies are a result of dispersal by wingless gamergates. This is expected to influence patterns of colony dispersal and spatial distribution of genetic variablity. In order to facilitate the study of population genetic structure we have identified six unique, polymorphic, microsatellite loci. We have used fluorescence tagged primers to detect polymorphism at these loci.     

Coupled adult-brood transport augments relocation in the Indian queenless ant Diacamma indicum

Colony relocation is an important aspect in the lives of social insects. In ants, the process of relocation is further complicated as brood, in addition to adults, have to be transported to the new nest. Here, we have investigated brood transport in the Indian ponerine ant Diacamma indicum, which uses tandem running—a primitive mode of recruitment—for the entire colony to relocate. We have found that there were no brood transport specialists and most of the brood was transported in the mandibles of followers that were being tandem run. Therefore, in a single tandem run, one adult and one brood item was effectively transported by tandem leaders augmenting the relocation process.     

Estimating the rate of gamergate turnover in the queenless ant Diacamma cyaneiventre using a maximum likelihood model

In monogynous ants, the death of the queen generally implies the death of the colony. However, queen replacement by either unrelated or related queen has been described in few species. In queenless ants from the genus Diacamma, the single reproductive worker (gamergate) is replaced by one of her daughters (or occasionally by a sister). From a long-term genetic survey of nests of D. cyaneiventre, we estimated the rate of gamergate turnover as well as the lifespan of workers and gamergate tenure using a maximum likelihood model developed for this purpose. We specifically compared the genotypes of two cohorts of workers sampled at 2 and 16 months interval from the same nests, using five microsatellite markers. To improve the accuracy of the estimates, we also used in the model the nests from the same population sampled only once and analysed by André et al. (2001). The model indicates that the possibility of the same nest not sheltering the same colony at two different sampling dates (colony turnover) was not significantly different from zero in our sample. The likelihood of the model was maximal for a probability of gamergate change p_γ = 0.005 per day (i.e. a gamergate tenure of 200 days) and a worker lifespan w=60 days, indicating that the gamergate ‘s tenure is about 3 times longer than workers’ expected lifespan in the population studied. Moreover, the genetic analysis of the gamergate and brood in three colonies excavated completely, reveals that colony fission can occur just after a gamergate replacement with the sister of the new gamergate reproducing in the new propagule. Received 12 October 2005; revised 7 December 2005; accepted 5 January 2006.     

Shift in the behaviours regulating monogyny is associated with highgenetic differentiation in the queenless ant Diacamma ceylonense

Summary In the queenless ant genus Diacamma, one mated worker (called gamergate) maintains reproductive mono-poly in a colony by mutilating newly emerged workers. However, in several populations from south India, referred to as nilgiri, gamergates do not mutilate their nestmates but monopolize reproduction using dominance interactions . Various lines of evidence indicate that nilgiri populations are closely related to the neighboring species D. ceylonense. To determine whether this important behavioural difference between nilgiri and D. ceylonense is associated with signi-ficant genetic differentiation, we have used microsatellite and mitochondrial markers to examine genetic variation within and between nilgiri and D. ceylonense. We found a very high genetic differentiation between the two forms, which suggests a lack of gene flow. There was an unexpected pattern of mitochondrial variation, because all nilgiri populations show identical or very closely related COII sequences except one population with a very different haplotype. This divergent haplotype is genetically much more distant from the other nilgiri haplotypes than are D. ceylonense haplotypes. This pattern is not observed at the nuclear level, which suggests that introgression of mitochondrial DNA probably occurred in some nilgiri populations.     

Differentiation of the reproductive tract between dominant and subordinate workers in the Japanese queenless ant Diacamma sp.

In queenless ants, gamergates (mated egg‐laying workers) fulfil the reproductive task normally reserved for the queen. Every worker is a potential gamergate, thus we expect pronounced conflicts over sexual reproduction within their colonies. In the queenless ant genus Diacamma, gamergates inhibit nest mates from mating by aggressively removing (‘mutilating’) a pair of small appendages on the thorax, termed gemmae, shortly after eclosion. Dissection and serial sectioning of the reproductive tracts of both mutilated and unmutilated individuals of Diacamma sp. from Japan at different ages revealed that mutilation inhibits the development of the bursa copulatrix and the spermatheca, two structures fundamental for sexual reproduction. The precursor of the bursa copulatrix develops into a fully functional structure in unmutilated individuals, whereas it degenerates irreversibly in mutilated callows. Experimental manipulations showed that the removal of the gemmae is not the sole factor regulating this development. The spermathecal epithelium and accessory spermathecal gland of unmutilated individuals are thicker than that of mutilated individuals, indicating a higher degree of activity in the former. Mutilated females are therefore left incapable of copulating and less competent for long‐time sperm storage.     

Molecular genetic diversity in populations of the stingless bee Plebeia remota: A case study

Genetic diversity is a major component of the biological diversity of an ecosystem. The survival of a population may be seriously threatened if its genetic diversity values are low. In this work, we measured the genetic diversity of the stingless bee Plebeia remota based on molecular data obtained by analyzing 15 microsatellite loci and sequencing two mitochondrial genes. Population structure and genetic diversity differed depending on the molecular marker analyzed: microsatellites showed low population structure and moderate to high genetic diversity, while mitochondrial DNA (mtDNA) showed high population structure and low diversity in three populations. Queen philopatry and male dispersal behavior are discussed as the main reasons for these findings.     

Nestmate discrimination in the queenless ponerine ant Diacamma sp. from Japan

We examined the nestmate discrimination ability of Diacamma sp., an ant that reproduces by colony budding. We also tested for a relationship between internest distance and hostility. Hostility toward non‐nestmates was significantly stronger than that toward nestmates, suggesting that Diacamma sp. discriminates between nestmates and non‐nestmates. There was no significant correlation between internest hostility and internest distance, which indicates the absence of a “dear enemy” phenomenon in this species.     

Obligatory female philopatry affects genetic population structure in the ant Proformica longiseta

Evolution of sociality has instigated many changes in the biology of social insects. Particularly, evolution towards complex social systems in ants affects how individuals move in space, usually by making females philopatric. Proformica longisetais well-suited for studying the effects of female philopatry, because female sexuals are wingless and do not actively disperse. We studied genetic population structure in P. longiseta in local scale both as genetic viscosity within one subpopulation, and as differentiation between closely (0.1–1.5 km) located subpopulations, by using nuclear (microsatellites) and mitochondrial (SSCP) markers. Dependent colony founding by splitting old nests is the only known nest founding strategy in P. longiseta. However, no genetic viscosity was detected at the nuclear markers within the subpopulation studied, possibly due to the dynamic nature of P. longiseta populations. The extreme female philopatry showed as strong structure between closely located subpopulations in the mitochondrial genome, but there was no isolation by distance showing that the differentiation pattern was random. Genetic structure in the nuclear genome was much weaker, and there was an indication of isolation by distance. This suggests that male dispersal is strong but not totally free across the area. Finally, non-dispersing P. longiseta females necessarily mate locally raising the possibility of inbreeding, but inbreeding coefficients showed that mating is random. Received 10 January 2006; revised 13 April 2006; accepted 20 April 2006.     

Hierarchical analysis of population genetic structure in the monogynous ant Cataglyphis cursor using microsatellite and mitochondrial DNA markers

Despite having winged queens, female dispersal in the monogynous ant Cataglyphis cursor is likely to be restricted because colonies reproduce by fission. We investigated the pattern of population genetic structure of this species using eight microsatellite markers and a mitochondrial DNA (mtDNA) sequence, in order to examine the extent of female and nuclear gene flow in two types of habitat. Sampling was carried out at a large spatial scale (16 sites from 2.5 to 120 km apart) as well as at a fine spatial scale (two 4.5-km transects, one in each habitat type). The strong spatial clustering of mtDNA observed at the fine spatial scale strongly supported a restricted effective female dispersal. In agreement, patterns of the mtDNA haplotypes observed at large and fine spatial scales suggested that new sites are colonized by nearby sites. Isolation by distance and significant nuclear genetic structure have been detected at all the spatial scales investigated. The level of local genetic differentiation for mitochondrial marker was 15 times higher than for the nuclear markers, suggesting differences in dispersal pattern between the two sexes. However, male gene flow was not sufficient to prevent significant nuclear genetic differentiation even at short distances (500 m). Isolation-by-distance patterns differed between the two habitat types, with a linear decrease of genetic similarities with distance observed only in the more continuous of the two habitats. Finally, despite these low dispersal capacities and the potential use of parthenogenesis to produce new queens, no signs of reduction of nuclear genetic diversity was detected in C. cursor populations.     

Dominance hierarchy and reproductive conflicts among subordinates in a monogynous queenless ant

In insect societies lacking morphologically specialized breedersand helpers, reproduction is often restricted to behaviorallydominant individuals. Such societies occur in about 100 speciesof ants that have secondarily lost the queen caste. All females,who are morphologically workers, can potentially mate and layeggs but only a few do so, and we demonstrate in Dinoponeraquadriceps that this is regulated by a dominance hierarchy.Six types of agonistic interactions allowed the ranking of 5-10workers in the hierarchy (n = 15 colonies). In particular, alphaand beta had characteristic behavioral profiles and were easily recognized.Only alpha mated, and workers ranking beta to delta sometimes producedunfertilized, male-destined eggs. Natural replacements (n = 19)and experimental removals (n = 15) of alpha demonstrated that betawas the individual most likely to replace alpha, although gammaand more rarely delta sometimes did, and we discuss the conflictthat occurs among high-ranking individuals over who should replacealpha. After such replacements, the new alpha behaved more aggressivelythan the overthrown alpha. Newly emerged workers tended to reachhigh ranks and displaced older high-ranking individuals downthe hierarchy. Low-ranking subordinates often prevented high-rankingindividuals from replacing alpha by biting and holding theirappendages (worker policing), which is consistent with the patternof relatedness associated with monogyny and monandry in D. quadriceps. Weinvestigated the relative importance of chemical communicationand dominance interactions to regulate reproduction. Alpha,beta, and sterile workers have different signatures of cuticularhydrocarbons, and these may provide honest information whichunderpins worker policing by low-ranking individuals.     

Reproductive monopoly enforced by sterile police workers in a queenless ant

In societies of totipotent insects, dyadic dominance interactionsgenerate a hierarchy that often underlies an extreme reproductiveskew. Subordinates remain infertile but can maximize their indirectfitness benefits through collective power (worker policing):interference with challenging high-rankers can prevent an untimelyreplacement of the reproductive. However, police workers onlybenefit if they favor individuals with high fertility. In themonogynous queenless ant Streblognathus peetersi, we used behavioral,physiological, and chemical methods to show that police workershave the primary role in the selection of the reproductive,and that they probably use reliable information about fertilityencoded in the cuticular hydrocarbons to make their decision.We successfully decreased an alpha's fertility by using a hormonaltreatment (Pyriproxyfen, a juvenile hormone analogue), and shewas always removed from the hierarchy by police workers. Inthe preceding days, one of the high-rankers became aggressive,although her interactions were not directed at the treated alpha.All treated alphas (n = 10) remained aggressive but ended upimmobilized by low-ranking workers after a median time of 11.5days. By then, the challenging high ranker exhibited dominancebehaviors typical of the alpha rank. In parallel, the cuticularprofile of the treated alpha exhibited predictable and oppositemodifications to that of the challenger's. This is the firststudy that uncouples dominance and fertility in a social insect:it gives a better understanding of the crucial role of sterilehelpers in the control of reproductive skew in animal societies.     

Higher genetic diversity on mountain tops: the role of historical and contemporary processes in shaping genetic variation in the bank vole

Glacial phases during the Pleistocene caused remarkable changes in species range distributions, with inevitable genetic consequences. Specifically, during interglacial phases, when the ice melted and new habitats became suitable again, species could recolonize regions that were previously covered by ice, such as high latitudes and elevations. Based on theoretical models and empirical data, a decrease in genetic variation is predicted along recolonization routes as a result of the consecutive founder effects that characterize the recolonization process. In the present study, we assessed the relative importance of historical and contemporary processes in shaping genetic diversity and differentiation of bank vole (Myodes glareolus) populations at different elevations in the Swiss Alps. By contrast to expectations, we found that genetic variation increased with elevation. Estimates of recent migration rates and a contrasting pattern of genetic differentiation observed at the mitochondrial cytochrome b gene and nuclear microsatellites support the hypothesis that higher genetic diversity at high elevation results from contemporary gene flow. Although historical recolonization processes can have marked effects on the genetic structure of populations, the present study provides an example where contemporary processes along an environmental gradient can reverse predicted patterns of genetic variation.     

Extremely low effective population sizes, genetic structuring and reduced genetic diversity in a threatened bumblebee species, Bombus sylvarum (Hymenoptera: Apidae)

Habitat fragmentation may severely affect survival of social insect populations as the number of nests per population, not the number of individuals, represents population size, hence they may be particularly prone to loss of genetic diversity. Erosion of genetic diversity may be particularly significant among social Hymenoptera such as bumblebees (Bombus spp.), as this group may be susceptible to diploid male production, a suggested direct cost of inbreeding. Here, for the first time, we assess genetic diversity and population structuring of a threatened bumblebee species (Bombus sylvarum) which exists in highly fragmented habitat (rather than oceanic) islands. Effective population sizes, estimated from identified sisterhoods, were very low (range 21-72) suggesting that isolated populations will be vulnerable to loss of genetic variation through drift. Evidence of significant genetic structuring between populations (theta = 0.084) was found, but evidence of a bottleneck was detected in only one population. Comparison across highly fragmented UK populations and a continental population (where this species is more widespread) revealed significant differences in allelic richness attributable to a high degree of genetic diversity in the continental population. While not directly related to population size, this is perhaps explained by the high degree of isolation between UK populations relative to continental populations. We suggest that populations now existing on isolated habitat islands were probably linked by stepping-stone populations prior to recent habitat loss.     

Phylogeography and population genetic structure of the European roe deer in Switzerland following recent recolonization

In the early 1800s, the European roe deer (Capreolus capreolus) was probably extirpated from Switzerland, due to overhunting and deforestation. After a federal law was enacted in 1875 to protect lactating females and young, and limiting the hunting season, the roe deer successfully recovered and recolonized Switzerland. In this study, we use mitochondrial DNA and nuclear DNA markers to investigate the recolonization and assess contemporary genetic structure in relation to broad topographic features, in order to understand underlying ecological processes, inform future roe deer management strategies, and explore the opportunity for development of forensic traceability tools. The results concerning the recolonization origin support natural, multidirectional immigration from neighboring countries. We further demonstrate that there is evidence of weak genetic differentiation within Switzerland among topographic regions. Finally, we conclude that the genetic data support the recognition of a single roe deer management unit within Switzerland, within which there is a potential for broad‐scale geographic origin assignment using nuclear markers to support law enforcement.     

Reduced genetic diversity and low effective size in peripheral northern European catfish Silurus glanis populations

Using 10 polymorphic microsatellites and 1251 individual samples (some dating back to the early 1980s), genetic structure and effective population size in all native and introduced Swedish populations of the European wels catfish or Silurus glanis were studied. Levels of genetic variability and phylogeographic relationships were compared with data from a previous study of populations in other parts of Europe. The genetically distinct Swedish populations displayed comparably low levels of genetic variability and according to one-sample estimates based on linkage disequilibrium and sib ship-reconstruction, current local effective population sizes were lower than minimum levels recommended for short-term genetic conservation. In line with a previous suggestion of postglacial colonisation from a single refugium, all Swedish populations were assembled on a common branch in a star-shaped dendrogram together with other European populations. Two distinct subpopulations were detected in upper and lower habitats of River Emån, indicating that even minor dispersal barriers may restrict gene flow for wels in running waters. Genetic assignment of specimens encountered in the brackish Baltic Sea and in lakes where the species does not occur naturally indicated presence of long-distance sea dispersal and confirmed unauthorised translocations, respectively.     

Genetic analysis of a documented population bottleneck: introduced Bennett's wallabies (Macropus rufogriseus rufogriseus) in New Zealand

Few bottlenecks of wild populations are sufficiently well-documented to constitute models for testing theories about the impact of bottlenecks on genetic variation, and subsequent population persistence. Relevant details of the Bennett's wallaby (Macropus rufogriseus rufogriseus) introduction into New Zealand were recorded (founder number, source and approximate bottleneck duration) and suggest this may provide a rare opportunity to examine the efficacy of tests designed to detect recent bottlenecks in wild populations. We first assessed the accuracy of historic accounts of the introduction using genetic diversity detected in mitochondrial DNA (mtDNA) and at five microsatellite loci. Phylogenetic analyses of mtDNA D-loop sequence haplotypes were consistent with the reported origin of the founders as Tasmania, rather than one of the Bass Strait islands in which Bennett's wallabies are also found. Microsatellite allele frequencies from the Tasmanian source population were then used to seed bottleneck simulations encompassing varying sizes and numbers of generations, in order to assess the severity of bottleneck consistent with diversity observed in the New Zealand population. The results suggested that the founder number was unlikely to have been as small as the three animals suggested by the account of the introduction. Nonetheless, the bottleneck was probably severe; in the range of three to five pairs of wallabies for one to three generations. It resulted in significantly reduced levels of allelic diversity and heterozygosity relative to the source population. This bottleneck is only detectable under the infinite allele model (IAM) and not under the stepwise mutation model (SMM) or the two-phase model (TPM), and possible explanations for this are discussed.     

Age polyethism,idiosyncrasy and behavioural flexibility in the queenless ponerine ant,Diacamma sp.

Age-related behavioural change of individually marked and known-age workers of a colony ofDiacamma sp. was observed through entire ant lives in the laboratory for more than a year. Although typical age polyethism was observed, activity of inside and outside tasks, life span, or time schedule of behavioural change varied considerably among workers. Idiosyncrasies in age-related behavioural change was detected among workers that eclosed on the same day. Cluster analyses revealed that individual patterns of behavioural change tended to be different when eclosion dates were far apart. This suggests that most workers change their behaviour flexibly. Thus, there is little effect of idiosyncrasy on colony response to changes in colony condition.