Luc Passera

Size and fat content of gynes in relation to the mode of colony founding in ants (Hymenoptera; Formicidae)

SummaryIn ants, there are two main processes of colony founding, the independent and the dependent modes. In the first case young queens start colony founding without the help of workers, whereas in the second case they are accompanied by workers. To determine the relation between the mode of colony founding and the physiology of queens, we collected mature gynes of 24 ant species. Mature gynes of species utilizing independent colony founding had a far higher relative fat content than gynes of species employing dependent colony founding. These fat reserves are stored during the period of maturation, i.e. between the time of emergence and mating, and serve as fuel during the time of colony founding to nurture the queen and the brood. Gynes of species founding independently but non claustrally were found to have a relative fat content intermediate between the values found for gynes founding independently and those founding dependently. This suggests that such gynes rely partially on their fat reserves and partially on the energy provided by prey they collect to nurture themselves and the first brood during the time of colony founding. Study of the fat content of mature gynes of all species has shown that it gives a good indication of the mode of colony founding.

Incest avoidance, fluctuating asymmetry, and the consequences of inbreeding in Iridomyrmex humilis, an ant with multiple queen colonies

SummaryInbreeding may have important consequences for the genetic structure of social insects and thus for sex ratios and the evolution of sociality and multiple queen (polygynous) colonies. The influence of kinship on mating preferences was investigated in a polygynous ant species, Iridomyrmex humilis, which has within-nest mating. When females were presented simultaneously with a brother that had been reared in the same colony until the pupal stage and an unrelated male produced in another colony, females mated preferentially with the unrelated male. The role of environmental colony-derived cues was tested in a second experiment where females were presented with two unrelated males, one of which had been reared in the same colony until the pupal stage (i.e., as in the previous experiment), while the other had been produced in another colony. In this experiment there was no preferential mating with familiar or unfamiliar males, suggesting that colony-derived cues might not be important in mating preferences. Inbreeding was shown to have no strong effect on the reproductive output of queens as measured by the number of worker and sexual pupae produced. The level of fluctuating asymmetry of workers produced by inbreeding queens was not significantly higher than that of non-inbreeding queens. Finally, colonies headed by inbreeding queens did not produce adult diploid males. Based on the current hypotheses of sex-determination the most plausible explanations for the absence of diploid-male-producing colonies are that (i) workers recognized and eliminated these males early in their development, and/or (ii) there are multiple sex-determining loci in this species. It is suggested that even if inbreeding effects on colony productivity are absent or low, incest avoidance mechanisms may have evolved and been maintained if inbreeding queens produce a higher proportion of unviable offspring.

Queen execution in the Argentine ant, Iridomyrmex humilis

ABSTRACT. Field censuses and laboratory experiments show that in the Argentine ant, Iridomyrmex humilis (Mayr), c. 90% of the queens are executed by workers in May, at the beginning of the reproductive season. The reduction in the number of queens probably decreases the inhibition exerted by queens on the differentiation of sexuals and thus allows the production of new queens and males shortly thereafter. In the laboratory, there was no correlation between the percentage of queens executed and their weight or fecundity. At the time of execution of queens, nearly all queens were of the same age; less than 1 year. Therefore it is not likely that the age of queens plays any role in the choice that workers make in the queens they executed. Execution of these queens results in a heavy energetic cost for the colony which amounts c. 8% of the total biomass. This behaviour of workers executing nestmate queens is discussed with regard to possible evolutionary significance at the queen and worker level.

Influence of the number of queens on nestmate recognition and attractiveness of queens to workers in the Argentine ant, Iridomyrmex humilis (Mayr)

To investigate the influence of the number of queens per colony on nestmate recognition in Iridomyrmex humilis, comparative assays were performed to study the attraction of workers to queens. These assays demonstrated that a phenomenon of recognition is superimposed on the attraction of workers to queens. Workers could discriminate non-nestmate queens from their nestmate queen to which they were significantly more attracted. This discrimination is probably based on the learning by workers of queen and colony odour. The level of attraction of workers to non-nestmate queens was similar in monogynous and polygynous colonies, whereas the level of attraction of workers to nestmate queens was significantly lower in polygynous colonies. This difference in the level of attraction of workers to nestmate queens almost certainly resulted from a lower efficiency in nestmate recognition in polygynous colonies. It is hypothesized that the mixture of several pheromonal sources produced by less related individuals in polygynous colonies may result in a less distinct colony odour than in monogynous colonies. The results are discussed with regard to some implications of polygyny and particularly to the loss of intercolonial aggression in I. humilis as well as in other polygynous ant species.

Queen‐worker conflict over sex ratio: A comparison of primary and secondary sex ratios in the Argentine ant, Iridomyrmex humilis

We compare the primary sex ratio (proportion of haploid eggs laid by queens) and the secondary sex ratio (proportion of male pupae produced) in the Argentine ant Iridomyrmex humilis with the aim of investigating whether workers control the secondary sex ratio by selectively eliminating male brood. The proportion of haploid eggs produced by queens was close to 0.5 in late winter, decreased to less than 0.3 in spring and summer, and increased again to a value close to 0.5 in fall. Laboratory experiments indicate that temperture is a proximate factor influencing the primary sex ratio with a higher proportion of haploid eggs being laid at colder temperatures. Production of queen pupae ceased in mid‐June, about three weeks before that of male pupae. After this time only worker pupae were produced. During the period of production of sexuals, the proportion of male pupae ranged from 0.30 to 0.38. Outside this period no males were reared although haploid eggs were produced all the year round by queens. Workers thus exert a control on the secondary sex ratio by eliminating a proportion of the male brood during the period of sexual production and eliminating all the males during the remainder of the cycle. These data are consistent with workers preferring a more female‐biased sex ratio than queens. The evolutionary significance of the production of male eggs by queens all the year round is as yet unclear. It may be a mechanism allowing queen replacement in the case of the death of the queens in the colony.

Mating system, optimal number of matings, and sperm transfer in the Argentine ant Iridomyrmex humilis

SummaryIn ants, because males have a finite sperm supply and females mate only at the beginning of their reproductive lives, it is possible to infer which is the limiting sex from a few parameters: the amount of sperm produced by males, the amount of sperm stored by females, and the numerical sex ratio. In the Argentine ant Iridomyrmex humilis mating takes place in the nest. Laboratory experiments and field data showed that the numerical sex ratio is heavily male-biased (10.1:1) and that the maximum number of sperm a female can store is similar to the number of sperm a male possesses. Thus females are the limiting sex in this species. In a set of mating experiments, one queen was presented with 1–20 males. The highest proportion of successful matings occurred when females were presented with two males. There was a significant negative correlation between the amount of sperm queens stored and the number of males present in the mating arena. This relationship most likely resulted from male interference during the copulation process. When several males were present in the arena, the mating pair was frequently disturbed by other males trying to copulate. Newly mated queens collected from the field stored 172,000 ± 76,000 sperm, a quantity most similar to that measured in laboratory mating experiments with a ratio of 5 or 10 males per queen. Because the operational sex ratio in I. humilis is highly male-biased, male interference may also decrease the amount of sperm queens store in the field. In many ants, fewer sperm stored by queens should decrease their reproductive success because they would run out of sperm earlier in their reproductive lifetimes. However, comparison of the amount of sperm present in young and old I. humilis queens collected in the field suggests that most use only a small proportion of their sperm supply during their lifetimes. Males mate once and discharge all their sperm during a single mating. Females may mate with several males but dissection of these males indicated that in most cases only one of them had empty seminal vesicles thus suggesting that a single male is responsible for most of the sperm transfer. Thus caution should be exercised in inferring multiple inseminations, as is frequently done in eusocial insects, from the observation of multiple copulations.

Pheromonal and behavioral queen control over the production of gynes in the Argentine ant Iridomyrmex humilis (Mayr)

SummaryBoth field observations and laboratory experiments have suggested that queens of I. humilis inhibit the production of new queens (gynes). Using small colony fragments, laboratory experiments were conducted to determine the means by which this inhibition is achieved. The addition of queen corpses to queenless fragments effectively inhibited the production of gynes, suggesting that a queen inhibitory primer pheromone is involved. This inhibitory influence was removed when corpses were washed in pentane, lending further support to the pheromonal hypothesis. Adult gynes (winged virgin queens) were not inhibitory, whereas young dealated mated queens of the same age were, suggesting that only inseminated queens produce the pheromone. Daily addition of eggs to queenless units did not appear to have a strong inhibitory influence, indicating that the lower worker/larva ratios associated with the presence of an egg-laying queen in such colony fragments does not greatly influence the production of sexuals. Pheromonal inhibition of gyne development appears to be achieved mainly by preventing the sexualization of bipotent female larvae, probably by affecting the brood-rearing behavior of workers. In addition, queens may also cause the execution of female larvae after they have become sexualized. In nearly all cases, the addition of a living queen to previously queenless units containing gyne larvae caused workers to execute one or more of these larvae within 24 h. In some cases queens were also seen attacking gyne larvae. The addition of queen corpses resulted in the execution of gyne larvae, suggesting that a queen pheromone mediates, at least in part, this execution behavior of workers. These results show that I. humilis queens exert control over the production of gynes in two ways: (1) by preventing the sexualization of female larvae and (2) by killing female larvae after they have become sexualized. A queen primer pheromone appears to be involved in both processes. Queen behavior also plays a role, at least in the execution of gyne larvae. This queen control over the production of gynes, probably mostly pheromonal, appears to operate strongly in the field where gynes are produced only in spring just after a sharp drop in the inhibitory queen influence due to the massive execution of queens by the workers.

Primary and secondary sex ratios in monogyne colonies of the fire ant

Abstract Patterns of sex ratios and sex investment ratios play an instrumental role in theoretical and empirical considerations of the evolution and maintenance of insect sociality. An assumption of sex-ratio studies in the eusocial Hymenoptera is that workers, who reproduce indirectly by rearing the queens offspring, have the ability to distinguish the sex of larvae and direct preferential treatment towards developing females. To determine if workers of the monogyne (single queen per colony) form of the fire ant, Solenopsis invicta, have this ability and the extent to which they might use it to influence the sex ratio of the colonys reproductives, the primary sex ratio (ratio of male/female-determined eggs produced by the queen) and the secondary sex ratio (ratio of male/female reproductive adults or pupae) were compared, in mature colonies producing sexuals of almost exclusively one sex or the other, a common condition in monogyne colonies of this and other ant species. Queens of male-producing colonies laid about 19% haploid (male) eggs, whereas queens of female-producing colonies laid about 11% haploid eggs. In both cases, the proportion of haploid eggs laid was far higher than the proportion of adult males reared by the workers. These results suggest that workers strongly influence the colonys secondary sex ratio by selective elimination of male larvae, but the magnitude of this influence depends upon the primary sex ratio produced by the queen. Highly male-biased secondary sex ratios produced by workers in relation to more male-biased primary sex ratios may be caused by ergonomic constraints that could limit the ability of workers to skew the sex-investment ratio.

Loss of mating flight and shift in the pattern of carbohydrate storage in sexuals of ants (Hymenoptera; Formicidae)

SummaryIn ants, energy for flying is derived from carbohydrates (glycogen and free sugars). The amount of these substrates was compared in sexuals participating or not participating in mating flights. Results show that in participating females (Lasius niger, L. flavus, Myrmica scabrinodis, Formica rufa, F. polyctena, F. lugubris), the amount of carbohydrates, especially glycogen, was higher than in non-participating females (Cataglyphis cursor, Iridomyrmex humilis). Similarly, male C. cursor and I. humilis which fly, exhibit a much higher carbohydrate content than do the non-flying females of these species. Furthermore, the quantity of carbohydrates stored was generally higher in males than in females for each species. These results are discussed with regard to the loss of the nuptial flight by some species of ants.

Early sex discrimination and male brood elimination by workers of the Argentine ant

An implicit assumption of sex allocation theories in ants is that workers discriminate the sex of brood to manipulate the juvenile forms towards the adequate investment ratio. This study deals with this possibility by testing the capability of workers of the Argentine ant Linepithema Humile to recognize the sex of larvae. Our data demonstrate for the first time larval recognition followed by male brood elimination. Batches of eggs and larvae of unknown sex were removed at different stages from queenright societies in which males pupae never appear. This brood was transferred in queenless colony fragments and we checked the number of male and female pupae obtained, and thus the proportion of male brood still alive in queenright colonies at the time of transfer. The results showed that haploid eggs were not eliminated whereas about half of the male brood was destroyed just after hatching. The remaining male brood was cannibalized later before pupation, but male pupae were spared. Hence, the combined data indicate that workers are able to identify the sex of the brood and to selectively eliminate male larvae. This behaviour appears to fit with the values of the secondary sex ratio observed in this species. Early sex brood discrimination and elimination of male larvae are discussed in connection with ergonomic costs as well as with the life history of the Argentine ant.