Ant–scale mutualism increases scale infestation,decreases folivory,and disrupts biological control in restored tropical forests

Ant–hemipteran mutualisms can have positive and negative effects on host plants depending on the level of hemipteran infestation and plant protection conferred by ants against folivory. Differential effects of such mutualisms on plant survival are well documented in undisturbed and ant-invaded systems, but few have explored how anthropogenic disturbance affects interactions between hemipterans and native ant species and what the consequences may be for recovering ecosystems. Within a fragmented landscape in Costa Rica, restored tropical forests harbor a mutualism between the native ant Wasmannia auropunctata and the scale insect Alecanochiton marquesi on the abundant, early-successional tree Conostegia xalapensis. I added A. marquesi scales to C. xalapensis seedlings and either allowed or excluded W. auropunctata to investigate if this mutualism leads to increased scale infestation, decreased scale mortality, and decreased folivory. I also examined whether these effects are mediated by the percentage of remnant forest cover in the landscape. I found that seedlings with ants excluded had fewer scale insects and higher herbivory than plants with ants present. I also found evidence that scale mortality due to fungal attack and parasitism was higher on ant-excluded versus ant-allowed seedlings but only at sites with high surrounding landscape forest cover. Together, these results suggest that mutualisms between scale insects and native ants can promote scale infestation, reduce folivory on native plant species, and potentially disrupt biological control of scale insects in recovering tropical forests. Further, my experiment underscores the importance of remnant tropical forests as sources of biological control in anthropogenically disturbed landscapes. Abstract in Spanish is available with online material.     

Rapid evolution by sexual selection in a wild,invasive mammal

Sexual selection theory provides a framework for investigating the evolution of traits involved in attracting and competing for mates. Given the sexual function of such traits, studies generally focus on individual interactions (i.e., displays and contests) in explaining trait origin and persistence. We show that ecological factors can strongly influence the adaptive value of these traits, and changes to these factors can lead to rapid evolutionary change. We compared sexually selected traits in the small Indian mongoose (Urva auropunctata) between their sparsely populated native range and four tropical islands to which they were introduced within the last 150 years and where, due to a lack of interspecific competition and predation, they have become invasive and densely populated. Because of a likely increase in encounter rate, we predicted that selection on long-distance chemical advertisement by males would relax in the introduced range. Accordingly, male, but not female, anal pads (used in scent marking) decreased in size in relation to both time since introduction and population density, and their relationship to body size and condition weakened. Concurrently, as predicted by intensified sperm competition, testis size increased following introduction. The small Indian mongoose thus experienced an inversion in the relative contributions to fitness of two sexual traits, followed by their rapid evolution in line with ecological changes.     

Sex and clonality in the little fire ant

Reproduction systems are controlling the creation of new genetic variants as well as how natural selection can operate on these variants. Therefore, they had historically been one of the main foci of evolutionary biology studies. The little fire ant, Wasmannia auropunctata, has been found to display an extraordinary reproduction system, in which both males and female queens are produced clonally. So far, native sexual populations of W. auropunctata have not been identified. Our goals were to identify such sexual populations and investigate the origins of female parthenogenesis and male clonality. Using mitochondrial DNA and microsatellite markers in 17 native populations, we found that traditional sexual populations occurred in W. auropunctata and are likely the recent source of neighboring clonal populations. Queen parthenogenesis has probably evolved several times through mutational events. Male clonality is tightly linked to queen parthenogenesis and thus appears to be female controlled. Its origin could be accounted for by 2 mutually exclusive hypotheses: either by the expected coevolution of the 2 sexes (i.e., a variant of the maternal genome elimination hypothesis) or by a shared mechanistic origin (i.e., by the production of anucleate ovules by parthenogenetic queens). Our results also show that W. auropunctata males and females do not form separate evolutionary units and are unlikely to be engaged in an all-out battle of sexes. This work opens up new perspectives for studies on the adaptive significance and evolutionary stability of mixed sexual and clonal reproduction systems in living organisms.     

Unadapted behaviour of native,dominant ant species during the colonization of an aggressive,invasive ant

Among the factors driving the invasive success of non-indigenous species, the “escape opportunity” or “enemy release” hypothesis argues that an invader’s success may result partly from less resistance from the new competitors found in its introduced range. In this study, we examined competitive interactions between the little fire ant Wasmannia auropunctata (Roger) and ant species of the genus Pheidole in places where both are native (French Guiana) and in places where only species of Pheidole are native (New Caledonia). The experimental introduction of W. auropunctata at food resources monopolized by the Pheidole species induced the recruitment of major workers only for the Guianian Pheidole species, which were very effective at killing Wasmannia competitors. In contrast, an overall decrease in the number of Pheidole workers and no recruitment of major workers were observed for the New Caledonian species, although the latter were the only ones able to kill the Wasmannia workers. These results emphasize the inappropriate response of native dominant New Caledonian species to W. auropunctata and, thus, the importance of enemy recognition and specification in the organization of ant communities. This factor could explain how invasive animal species, particularly ants, may be able to successfully invade species-rich communities.     

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.     

Where do adaptive shifts occur during invasion? A multidisciplinary approach to unravelling cold adaptation in a tropical ant species invading the Mediterranean area

Evolution may improve the invasiveness of populations, but it often remains unclear whether key adaptation events occur after introduction into the recipient habitat (i.e. post‐introduction adaptation scenario), or before introduction within the native range (i.e. prior‐adaptation scenario) or at a primary site of invasion (i.e. bridgehead scenario). We used a multidisciplinary approach to determine which of these three scenarios underlies the invasion of the tropical ant Wasmannia auropunctata in a Mediterranean region (i.e. Israel). Species distribution models (SDM), phylogeographical analyses at a broad geographical scale and laboratory experiments on appropriate native and invasive populations indicated that Israeli populations followed an invasion scenario in which adaptation to cold occurred at the southern limit of the native range before dispersal to Israel. We discuss the usefulness of combining SDM, genetic and experimental approaches for unambiguous determination of eco‐evolutionary invasion scenarios.     

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.     

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.     

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.