Julien Le Breton

Clonal reproduction by males and females in the little fire ant

Sexual reproduction can lead to major conflicts between sexes and within genomes. Here we report an extreme case of such conflicts in the little fire ant Wasmannia auropunctata. We found that sterile workers are produced by normal sexual reproduction, whereas daughter queens are invariably clonally produced. Because males usually develop from unfertilized maternal eggs in ants and other haplodiploid species, they normally achieve direct fitness only through diploid female offspring. Hence, although the clonal production of queens increases the queens relatedness to reproductive daughters, it potentially reduces male reproductive success to zero. In an apparent response to this conflict between sexes, genetic analyses reveal that males reproduce clonally, most likely by eliminating the maternal half of the genome in diploid eggs. As a result, all sons have nuclear genomes identical to those of their father. The obligate clonal production of males and queens from individuals of the same sex effectively results in a complete separation of the male and female gene pools. These findings show that the haplodiploid sex-determination system provides grounds for the evolution of extraordinary genetic systems and new types of sexual conflict.

Niche opportunity and ant invasion: the case of Wasmannia auropunctata in a New Caledonian rain forest

Due to the unbalanced distribution of their fauna and flora, which leads to the creation of a niche opportunities, it is generally accepted that island communities offer weak biotic resistance to biological invasion. In order to empirically test this statement, we compared resource use by ants in the understorey of an undisturbed New Caledonian rain forest recently invaded by the little fire ant, Wasmannia auropunctata. We tested the exploitation of: (1) food sources by placing baits on all trees with trunks greater than 5 cm in diameter; and (2) nesting sites on two tree species likely to shelter ant colonies. In non-invaded areas, the native ants occupied only 44.6% of the baits after 2 h of exposure, while in invaded areas all the baits were occupied by numerous W. auropunctata workers. Similarly, in non-invaded areas only 48.9% of Meryta coriacea (Araliaceae) trees and 64.5% of Basselinia pancheri (Arecaceae) sheltered ants, while in invaded areas W. auropunctata nested in 92.6-98.3% of these trees. Also, workers attended native Margarodidae (Hemiptera) for which they promoted the development of populations significantly larger than those attended by native ants. Thus native ants appear unable to efficiently exploit and defend several of the available food sources and nesting sites, providing a niche opportunity for an invader like W. auropunctata.

Experimental Evidence of Large-Scale Unicoloniality in the Tramp Ant Wasmannia auropunctata (Roger)

We examined intraspecific colonial aggressiveness in Wasmannia auropunctata (Roger), a tramp species originating from the neotropics. By observing the results of one-on-one confrontations, we compared the behavioral responses of workers originating from six New Caledonian locations (introduced range) and four Brazilian cocoa plantations (original range). We recorded interindividual “aggressive” behavior on four levels ranging from physical contact, with no aggressive response, to prolonged aggressiveness, including stinging by one or both ants. In Brazil, we often observed high intraspecific aggressiveness between populations originating from distant locations, indicating that W. auropunctata may behave as a multicolonial species in its native range. In New Caledonia, paired encounters resulted in low agonistic behavior, as shown by the absence of “full attacks” (which include stinging by one or both opponents). Our results suggest that W. auropunctata behaves as a single supercolony throughout New Caledonia and that the scale of its unicoloniality (widespread colonies with interconnected nests without aggressiveness between workers originating from distant areas) is different in introduced and native populations. According to the present study, it seems likely that differences in intraspecific aggressiveness between native and introduced populations of W. auropunctata contribute to its invasive success.

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.

RARE SEXUAL REPRODUCTION EVENTS IN THE CLONAL REPRODUCTION SYSTEM OF INTRODUCED POPULATIONS OF THE LITTLE FIRE ANT

Abstract 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.

Influence of interspecific competition on the recruitment behavior and liquid food transport in the tramp ant species Pheidole megacephala

This study was conducted on the reactions of Pheidole megacephala scouts when finding liquid food sources situated on territories marked by competing dominant ant species or on unmarked, control areas to see if the number of recruited nestmates is affected and if soldiers behave in ways adapted to the situation. We show that scouts recruit more nestmates, particularly soldiers, on marked rather than on unmarked areas. This recruitment allows P. megacephala to organize the defence and rapid depletion of these food sources prior to any contact with competitors. Soldiers can carry liquid foods both (1) in their crops like other Myrmicinae and (2), in a new finding concerning myrmicine ants, under their heads and thoraxes like certain poneromorph genera because the droplets adhere through surface tension strengths. Later, the liquids stored in the crop are distributed to nestmates through regurgitations during trophallaxis and the external droplets are distributed through “social buckets”, or the mode of liquid food transfer common in poneromorphs. Their flexibility to use or not use the latter technique, based on the situation, corroborates other reports that Pheidole soldiers have a relatively large behavioral repertoire.

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.

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.