Rare sexual reproduction events in the clonal reproduction system of introduced populations of the little fire ant

A unique reproductive system has previously been described in Wasmannia auropunctata, a widespread invasive ant species, where males are produced clonally, female queens are parthenogens, and female workers are produced sexually. However, these findings were mostly based on samples originating from only a limited part of the native range of the species in South America. We used microsatellite markers to uncover the reproductive modes displayed by a large number of nests collected in various invasive W. auropunctata populations introduced 40 years ago into New Caledonia, where the species now forms a single 450-km-long supercolony. Although the main reproduction system in New Caledonia remained clonality for both male and female reproductives, we found evidence of rare sexual reproduction events that led to the production of both new queen and male clonal lineages. All clonal lineages observed in New Caledonia potentially derived from sexual reproduction, recombination, and mutation events from a single female and a single male genotype. Hence, the male and female gene pools are not strictly separated in New Caledonia and the two sexes do not follow independent evolutionary trajectories. Our results also suggest genetic determination for both parthenogenesis and caste. We discuss the evolutionary implications of the emergence of sex in the clonal reproduction system of introduced populations of W. auropunctata.     

Reproductive system,social organization,human disturbance and ecological dominance in native populations of the little fire ant,Wasmannia auropunctata

The invasive ant species Wasmannia auropunctata displays both ecologically dominant and non‐dominant populations within its native range. Three factors could theoretically explain the ecological dominance of some native populations of W. auropunctata: (i) its clonal reproductive system, through demographic and/or adaptive advantages; (ii) its unicolonial social organization, through lower intraspecific and efficient interspecific competition; (iii) the human disturbance of its native range, through the modification of biotic and abiotic environmental conditions. We used microsatellite markers and behavioural tests to uncover the reproductive modes and social organization of dominant and non‐dominant native populations in natural and human‐modified habitats. Microsatellite and mtDNA data indicated that dominant and non‐dominant native populations (supercolonies as determined by aggression tests) of W. auropunctata did not belong to different evolutionary units. We found that the reproductive system and the social organization are neither necessary nor sufficient to explain W. auropunctata ecological dominance. Dominance rather seems to be set off by unknown ecological factors altered by human activities, as all dominant populations were recorded in human‐modified habitats. The clonal reproductive system found in some populations of W. auropunctata may however indirectly contribute to its ecological dominance by allowing the species to expand its environmental niche, through the fixation over time of specific combinations of divergent male and female genotypes. Unicoloniality may rather promote the range expansion of already dominant populations than actually trigger ecological dominance. The W. auropunctata model illustrates the strong impact of human disturbance on species’ ecological features and the adaptive potential of clonal reproductive systems.     

Clonal reproduction by males of the ant Vollenhovia emeryi (Wheeler)

In colonies of the queen‐polymorphic ant Vollenhovia emeryi, some colonies produce only long‐winged (L) queens, while others produce only short‐winged (S) queens. At four nuclear microsatellite loci, males in the S colony had alleles that were different from those of their queen. This suggests that the nuclear genome of males is not inherited from their colony queen, as has also been described for Wasmannia auropunctata (Roger). In V. emeryi the possibility of male transfer from other colonies has not been ruled out because previous studies of this species have obtained only nuclear gene information. We analyzed both mitochondrial and nuclear genes for S queens, S males and L queens to clarify the origins of males. Sequence analyses showed that although S queens and S males shared the same mtDNA haplotype, they had a different genotype at a nuclear gene (long‐wavelength opsin) locus. Neighbor‐joining analysis based on the four microsatellite loci also suggested gene pool separation between S queens and S males. These results are consistent with predictions of clonal reproduction by males. While L queens share opsin genotypes with S males, they have very different mtDNA sequences. Hybridization in the near past between S queens and L males or gene transmission from S males to L queen populations in the present would explain these differences.     

Habitat association and coexistence of endemic and introduced ant species in the Galápagos Islands

1. We investigated ant communities in all main vegetation zones of the model island of Santa Cruz in the Galápagos archipelago (155 collection points, spread over 21 sites; 28 ant species collected), and evaluated the distribution, coexistence, and effect of environmental factors in a community composed of endemic, probably endemic, and introduced ants of the New World and exotic origin. 2. Introduced species were the most frequent, occurring in 98% of the samples, yet endemic and probably endemic species still occurred in 54% of the samples, and constituted one of three most common species. The present study revealed that the habitat type along with altitude and the tree cover are the primary factors shaping ant community composition. Little evidence was found for a competitively structured assemblage of ant species. 3. The present study confirmed the predominance of two dominant invasive species, Solenopsis geminata Fabricius and Wasmannia auropunctata Roger, whose abundances are negatively correlated. The abundance of S. geminata is positively correlated with the overall species richness, and with the proportion of other introduced species. The presence of both invasive ants is associated with a low evenness of ant communities. 4. The present study (i) stresses the dominance of introduced species and the relative resistance of endemic species, (ii) highlights the on‐going processes of species introductions and (iii) points out the need for adequate monitoring and conservation of the pristine and threatened environments that constitute the Galápagos Islands.     

Ecologically heterogeneous populations of the invasive ant Wasmannia auropunctata within its native and introduced ranges

Abstract 1. The biology of most invasive species in their native geographical areas remains largely unknown. Such studies are, however, crucial in shedding light on the ecological and evolutionary processes underlying biological invasions. 2. The present study focuses on the little fire ant Wasmannia auropunctata, a species native to Central and South America that has been widely introduced and which has become invasive throughout the tropics. We characterise and compare several ecological traits of native populations in French Guiana with those in one of its introduced ranges, New Caledonia. 3. We found ecologically heterogeneous populations of W. auropunctata coexisting in the species’ native geographical area. First, we found populations restricted to naturally perturbed areas (particularly floodplains) within the primary forest, and absent from the surrounding forest areas. These populations were characterised by low nest and worker densities. Second, we found dominant populations in recent anthropogenic areas (e.g. secondary forest or forest edge along road) characterised by high nest and worker densities, and associated with low ant species richness. The local dominance of W. auropunctata in such areas can be due to the displacement of other species (cause) or the filling‐up of empty habitats unsuitable to other ants (effect). With respect to their demographic features and ant species richness, the populations of native anthropogenic habitats were to a large extent similar to the invasive populations introduced into remote areas. 4. The results point to the need for greater research efforts to better understand the ecological and demographic features of invasive species within their native ranges.     

Immediate impacts of invasion by Wasmannia auropunctata (Hymenoptera: Formicidae) on native litter ant fauna in a New Caledonian rainforest

Abstract For the last 30 years, Wasmannia auropunctata (the little fire ant) has spread throughout the Pacific and represents a severe threat to fragile island habitats. This invader has often been described as a disturbance specialist. Here we present data on its spread in a dense native rainforest in New Caledonia. We monitored by pitfall trapping the litter ant fauna along an invasive gradient from the edge to the inner forest in July 1999 and March 2000. When W. auropunctata was present, the abundance and richness of native ants drops dramatically. In invaded plots, W. auropunctata represented more than 92% of all trapped ant fauna. Among the 23 native species described, only four cryptic species survived. Wasmannia auropunctata appears to be a highly competitive ant that dominates the litter by eliminating native ants. Mechanisms involved in this invasive success may include predation as well as competitive interactions (exploitation and interference). The invasive success of W. auropunctata is similar to that of other tramp ants and reinforces the idea of common evolutionary traits leading to higher competitiveness in a new environment.     

Absence of individual sterility in thelytokous colonies of the ant <Emphasis Type="Italic">Cerapachys biroi</Emphasis> Forel (Formicidae,Cerapachyinae)

Summary The reproductive partitioning generates a persistent conflict within insects societies and a sustained theoretical and empirical attention is devoted to understand its resolution. In that context, thelytokous parthenogenesis by workers is an intriguing phenomenon where each individual is virtually reproducing. This reproductive strategy, scarce among Formicidae, was studied in C. biroi, an obligatory thelytokous cerapachyine ant. Particularly, we searched for a reproductive division of labour in colonies assumed to be clonal. The results revealed that no sterile caste was present in the colonies. However, reproduction was linked both to a temporal polyethism, in which older workers ceased to lay as they became foragers, and to a morphological polyethism, illustrated by two morphological types of individuals displaying different task allocations and ovary capacities. Evolutionary implication of this uncommon social structure, seemingly free of traditional conflict and characterised by a reproduction evenly distributed among nestmates, is discussed from comparisons to other ant species with extreme kin structure.Received 18 June 2003; revised 6 August 2003; accepted 7 August 2003.     

Impact of an invasive alien ant,Wasmannia auropunctata Roger., on a specialised plant–ant mutualism,Barteria fistulosa Mast. and Tetraponera aethiops F. Smith., in a Gabon forest

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Habitat disturbance modifies dominance,coexistence, and competitive interactions in tropical ant communities

1. Interspecific competition is a major structuring principle in ecological communities. Despite their prevalence, the outcome of competitive interactions is hard to predict, highly context-dependent, and multiple factors can modulate such interactions. 2. We tested predictions concerning how competitive interactions are modified by anthropogenic habitat disturbance in ground-foraging ant assemblages inhabiting fragmented Inter-Andean tropical dry forests in southwestern Colombia, and investigated ant assemblages recruiting to baits in 10 forest fragments exposed to varying level of human disturbance. 3. Specifically, we evaluated how different components of competitive interactions (patterns of species co-occurrence, resource partitioning, numerical dominance, and interspecific trade-offs between discovery and dominance competition) varied with level of habitat disturbance in a human-dominated ecosystem. 4. Multiple lines of evidence suggest that the role of competitive interactions in structuring ground-foraging ant communities at baits varied with respect to habitat disturbance. As disturbance increased, community structure was more likely to exhibit random co-occurrence patterns, higher levels of monopolization of food resources by dominant ants, and disproportionate dominance of a single species, the little fire ant (Wasmannia auropunctata). At a regional scale, we found evidence for a trade-off between dominance and discovery abilities of the 15 most common species at baits. 5. Together, these results suggest that human disturbance modifies the outcome of competitive interactions in ground-foraging ant assemblages and may promote dominant species that reduce diversity and coexistence in tropical ecosystems.     

Host-Specific Myrmecophily and Myrmecophagy in the Tropical Coccinellid Diomus thoracicus in French Guiana

A variety of arthropods, particularly insects, have developed myrmecophilous interactions with ants to gain access to resources and/or for protection. Among these myrmecophiles, only a few examples have been documented in the Coccinellidae, most of them involving species able to feed on ant-tended Hemiptera. We report here a new case of obligate myrmecophily in the coccinellid Diomus thoracicus. Larvae are invariably and exclusively found in the nests of the ant Wasmannia auropunctata and seem to rely on ant brood as their only food source. Not only do ant workers show no aggressiveness toward the D. thoracicus larvae in their behavioral interactions at the colonial level, but also at the species level; while coccinellid adults are always attacked. The integration of the larvae inside of the ant nests is based on their chemical mimicry of the host's cuticular cues. Therefore, given the presence of the D. thoracicus larvae inside of the ant's nest, their predation on Wasmannia brood and their chemical mimicry, this species can be considered a specific parasite of W. auropunctata. Overall, this new case of myrmecophily not only specifically involves a highly invasive ant species, but also provides insights into the evolution of myrmecophily and myrmecophagy in coccinellids.     

Effect of propagule pressure on the establishment and spread of the little fire ant Wasmannia auropunctata in a Gabonese oilfield

We studied the effect of propagule pressure on the establishment and subsequent spread of the invasive little fire ant Wasmannia auropunctata in a Gabonese oilfield in lowland rain forest. Oil well drilling, the major anthropogenic disturbance over the past 21 years in the area, was used as an indirect measure of propagule pressure. An analysis of 82 potential introductions at oil production platforms revealed that the probability of successful establishment significantly increased with the number of drilling events. Specifically, the shape of the dose–response establishment curve could be closely approximated by a Poisson process with a 34% chance of infestation per well drilled. Consistent with our knowledge of largely clonal reproduction by W. auropunctata , the shape of the establishment curve suggested that the ants were not substantially affected by Allee effects, probably greatly contributing to this species' success as an invader. By contrast, the extent to which W. auropunctata spread beyond the point of initial introduction, and thus the extent of its damage to diversity of other ant species, was independent of propagule pressure. These results suggest that while establishment success depends on propagule pressure, other ecological or genetic factors may limit the extent of further spread. Knowledge of the shape of the dose–response establishment curve should prove useful in modelling the future spread of W. auropunctata and perhaps the spread of other clonal organisms.     

The assembly and importance of a novel ecosystem: The ant community of coffee farms in Puerto Rico

Agricultural ecosystems are by their very nature novel and by definition the more general biodiversity associated with them must likewise constitute a novel community. Here, we examine the community of arboreally foraging ants in the coffee agroecosystem of Puerto Rico. We surveyed 20 coffee plants in 25 farms three times in a period of one year. We also conducted a more spatially explicit sampling in two of the farms and conducted a species interaction study between the two most abundant species, Wasmannia auropunctata and Solenopsis invicta, in the laboratory. We find that the majority of the most common species are well‐known invasive ants and that there is a highly variable pattern of dominance that varies considerably over the main coffee producing region of Puerto Rico, suggesting an unusual modality of community structure. The distribution pattern of the two most common species, W. auropunctata and S. invicta, suggests strong competitive exclusion. However, they also have opposite relationships with the percent of shade cover, with W. auropunctata showing a positive relationship with shade, while S. invicta has a negative relationship. The spatial distribution of these two dominant species in the two more intensively studied farms suggests that young colonies of S. invicta can displace W. auropunctata. Laboratory experiments confirm this. In addition to the elaboration of the nature and extent of this novel ant community, we speculate on the possibilities of its active inclusion as part of a biological control system dealing with several coffee pests, including one of the ants itself, W. auropunctata.     

Sex investment ratios in monogyne and polygyne populations of the fire ant Solenopsis invicta

Both monogyne (single queen per colony) and polygyne (multiple queens per colony) populations of the fire ant Solenopsis invicta are good subjects for tests of kin selection theory because their genetic and reproductive attributes are well-characterized, permitting quantitative predictions about the degree to which sex investment ratios should be female-biased if workers and not queens control reproductive allocation. In the study populations, an investment ratio of 3 females: 1 male is predicted (a proportional investment in females of 0.75) in the monogyne form, whereas a proportional investment in females between 0.637 and 0.740 is expected in the polygyne form. To test these predictions, colonies from a single population of each social form were collected and censused during three different seasons. Consistent with their alternative modes of colony founding, monogyne colonies invested more in reproduction (sexual production) and less in growth/maintenance (worker production) than did the polygyne colonies. Overall, the sex investment ratios were female-biased in both forms, although there was considerable seasonal variation. After adjusting for sex-specific energetic costs, the proportional investment in females was 0.607 in the monogyne population, a value in between those expected under complete control by either the queen or the workers. However, when combined with data from four other previously studied monogyne populations in the U.S.A., the mean investment ratio did not differ significantly from the value predicted if workers have exclusive control. In the polygyne population, the proportional investment in females of 0.616 was consistent with the level of female bias expected under partial to complete worker control, although the potential influence of two confounding factors — possible contact with monogyne colonies and the preponderance of sterile diploid males — weakens this conclusion somewhat. Taken as a whole, the sex investment ratios of monogyne and polygyne populations of S. invicta are consistent with at least partial worker control. Of several ultimate and proximate explanations that have been proposed to explain inter-colonial variation in the sex investment ratio, only the effect of the primary sex ratio (female-determined eggs: male-determined eggs) laid by the queen appears to account for the observed variation among monogyne colonies. In the polygyne population, there is limited support for the hypothesis that greater resource abundance favors investment in females.     

Sex is not a solution for reproduction: the libertine bubble theory

Here, I propose a new hypothesis: sex originated from an archaic gene transfer process among prebiotic bubbles without the prerequisite for reproduction. This de‐coupling from reproduction might make the thorny problem of accounting for the evolution of sex, despite the apparent advantages of parthenogenicity, more tractable.     

Sex determination and evolution of unisexuality in the Conchostraca

Field collected or laboratory-reared samples of 60 species of conchostracans (representing all extant genera) indicate that males and females are equally common in most species. Deviations from this pattern occur in four lineages.Cyzicus andLeptestheria each include at least one unisexual species; many species of Limnadiinae are either unisexual or characterized by female-biased sex ratios; and Cyclestheriidae are either unisexual or express males in the later generations of their life cycles. Laboratory studies indicate that species with sex ratios near unity are gonochoric (obligately sexual), whereas females in species with female-biased sex ratios are capable of both outcrossing and selfing modes of reproduction. Phylogenetic analysis of patterns of reproduction suggest that sexual reproduction is the primitive condition. Genetic analysis of sexual species indicate that gender is determined by one or a few genetic factors and that the male-determining allele is recessive. The inheritance of gender in androdioecious species (where females are capable of self-fertilization) is similar to that in sexual species. Androdioecy is likely to be the intermediate stage between obligately sexual reproduction and unisexuality in the Limnadiinae. The phylogenetic distribution of sex ratio variation suggests that unisexuality in Cyzicidae, Leptestheriidae, and Cyclestheriidae has arisen independently of that in the Limnadiinae and that these cases have evolved by different evolutionary pathways.     

Androgenesis is a maternal trait in the invasive ant Wasmannia auropunctata

Androgenesis is the production of an offspring containing exclusively the nuclear genome of the fathering male via the maternal eggs. This unusual mating system is generally considered a male trait, giving to androgenetic males a substantial fitness advantage over their sexually reproducing relatives. We here provide the first empirical study of the evolutionary outcomes of androgenesis in a haplo-diploid organism: the invasive ant Wasmannia auropunctata. Some of the populations of this species have a classical haplo-diploid sexual mating system. In other populations, females and males are produced through parthenogenesis and androgenesis, respectively, whereas workers are produced sexually. We conducted laboratory reciprocal-cross experiments with reproductive individuals from both types of populations and analysed their progenies with genetic markers, to determine the respective contribution of males and females to the production of androgenetic males. We found that androgenesis was a parthenogenetic female trait. A population genetic study conducted in natura confirmed the parthenogenetic female origin of androgenesis, with the identification of introgression events of sexual male genotypes into androgenetic/parthenogenetic lineages. We argue that by producing males via androgenesis, parthenogenetic queen lineages may increase and/or maintain their adaptive potential, while maintaining the integrity of their own genome, by occasionally acquiring new male genetic material and avoiding inbreeding depression within the sexually produced worker cast.     

Effects of ploidy and sex-locus genotype on gene expression patterns in the fire ant Solenopsis invicta

Males in many animal species differ greatly from females in morphology, physiology and behaviour. Ants, bees and wasps have a haplodiploid mechanism of sex determination whereby unfertilized eggs become males while fertilized eggs become females. However, many species also have a low frequency of diploid males, which are thought to develop from diploid eggs when individuals are homozygous at one or more sex determination loci. Diploid males are morphologically similar to haploids, though often larger and typically sterile. To determine how ploidy level and sex-locus genotype affect gene expression during development, we compared expression patterns between diploid males, haploid males and females (queens) at three developmental timepoints in Solenopsis invicta. In pupae, gene expression profiles of diploid males were very different from those of haploid males but nearly identical to those of queens. An unexpected shift in expression patterns emerged soon after adult eclosion, with diploid male patterns diverging from those of queens to resemble those of haploid males, a pattern retained in older adults. The finding that ploidy level effects on early gene expression override sex effects (including genes implicated in sperm production and pheromone production/perception) may explain diploid male sterility and lack of worker discrimination against them during development.     

Sperm length and quality in sperm-dependent parthenogens

Is the male function of parthenogenetic hermaphrodites a historic remnant or an adaptive investment? In the first case, one would expect the male function to be ‘degraded’ and, in the second case, fully functional, despite being reduced. To answer this question, we investigated sperm morphology and quality in the hermaphroditic planarian Schmidtea polychroa. Parthenogenetic forms of this species are sperm‐dependent and require allosperm to trigger embryogenesis. Although there is generally no genetic paternal contribution, occasional fertilization of parthenogenetic eggs has been reported, leading to genetic changes in an otherwise apomictic lineage (‘occasional sex’). Comparing two locations, one with pure clonality and one with occasional sexuality, revealed substantial differences in both sperm length and fertility: Occasional sex appears to be coupled with longer sperm and higher sperm quality. We discuss the implications of these results for the maintenance of the male function in sperm‐dependent parthenogens. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 93 , 81–87.     

Associations of ant species to land cover types and human disturbance in south‐west Gabon

We recorded ground‐foraging ant species in forest and savannah habitats along a 52‐km‐long road planned for upgrade in the buffer zone of the Moukalaba‐Doudou National Park in south‐west Gabon. Sixty stations were established with three sampling points on each side of the future road and baited with peanut butter to record the presence of invasive Wasmannia auropunctata (Roger, 1863). We documented 46 ant species including one genus and eight species not previously reported in Gabon, but no evidence of the presence of W. auropunctata. We also found species known to have an opportunistic behaviour such as Cardiocondyla emeryi (Forel, 1881), Tetramorium simillimum (Smith, 1851) and Trichomyrmex destructor (Jerdon, 1851). Species richness in forested stations was significantly higher than in savannah. Among the most common ant species in the area, we identified 13 associated with forests, eight associated with savannahs and one generalist. Four species were highly tolerant to human disturbance. Our study, even if biased towards stress‐tolerant species, provides new insights about ant species associations with habitats and contributes to the establishment of a reference system to classify African ant species that could be used to monitor the success of restoration of areas impacted by human activities.     

Sex at the margins: parthenogenesis vs. facultative and obligate sex in a Neotropical ant

Geographic parthenogenesis is a distribution pattern, in which parthenogenetic populations tend to live in marginal habitats, at higher latitudes and altitudes and island‐like habitats compared with the sexual forms. The facultatively parthenogenetic ant Platythyrea punctata is thought to exhibit this general pattern throughout its wide range in Central America and the Caribbean Islands. Workers of P. punctata from the Caribbean produce diploid female offspring from unfertilized eggs by thelytokous parthenogenesis, and mated females and males are rare. In contrast, workers in one colony from Costa Rica were incapable of thelytoky; instead mated workers produced all female offspring. Because sample sizes were very low in former studies, we here use microsatellite markers and explicit tests of thelytoky to examine the population genetic structure of ancestral and derived populations of P. punctata throughout the Caribbean and Central America. Populations from the Caribbean islands were fully capable of parthenogenesis, and population genetic signatures indicate that this is the predominant mode of reproduction, although males are occasionally produced. In contrast, the northernmost population on the mainland (Texas) showed signatures of sexual reproduction, and individuals were incapable of reproduction by thelytoky. Contrary to expectations from a geographic parthenogenesis distribution pattern, most parts of the mainland populations were found to be facultatively thelytokous, with population genetic signatures of both sexual and parthenogenetic reproduction.