Serge Aron

Self-Organization in Social Insects

Self-organization was introduced originally in the context of physics and chemistry to describe how microscopic processes give rise to macroscopic stuctures in out-of-equilibrium systems, Recent research that extends this concept to ethology suggests that it provides a concise description of a wide range of collective phenomena in animals, especially in social insects. This description does not rely on individual complexity to account for complex spatiotemporal features that emerge at the colony level, but rather assumes that intractions among simple individuals can produce highly structured collective behaviours.

Conditional use of sex and parthenogenesis for worker and queen production in ants

The near-ubiquity of sexual reproduction in animal species has long been considered a paradox because sexually reproducing individuals transmit only half of their genome to their progeny. Here, we show that the ant Cataglyphis cursor circumvents this cost by using alternative modes of reproduction for the production of reproductive and nonreproductive offspring. New queens are almost exclusively produced by parthenogenesis, whereas workers are produced by normal sexual reproduction. By selectively using sex for somatic growth and parthenogenesis for germline production, C. cursor has taken advantage of the ant caste system to benefit from the advantages of both sexual and asexual reproduction.

Thelytokous parthenogenesis and its consequences on inbreeding in an ant.

Thelytokous parthenogenesis, that is, the production of diploid daughters from unfertilized eggs, may involve various cytological mechanisms, each having a different impact on the genetic structure of populations. Here, we determined the cytological mechanism of thelytokous parthenogenesis and its impact on inbreeding in the ant Cataglyphis cursor, a species where queens use both sexual and asexual reproduction to produce, respectively, workers and new queens. It has been suggested that thelytokous parthenogenesis in C. cursor might have been selected for to face high queen mortality and, originally, to allow workers to replace the queen when she passes away. We first determined the mode of thelytokous parthenogenesis by comparing the rate of transition to homozygosity at four highly polymorphic loci to expectations under the different modes of parthenogenesis. Our data show that thelytoky is achieved through automictic parthenogenesis with central fusion. We then estimated the proportion of colonies headed by worker-produced queens in a natural population. We designed a model linking the observed homozygosity in queens to the proportion of queens produced by workers, based on the assumption that (i) parthenogenesis is automictic with central fusion and (ii) queen lineage is asexually produced, resulting in an increase of the inbreeding over generations, whereas workers are sexually produced and therefore not inbred. Our results indicate that more than 60% of the colonies should be headed by a worker-produced queen, suggesting that queens lifespan is low in this 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.

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.

Sex determination and inbreeding depression in an ant with regular sib-mating

Haplodiploidy is one of the most widespread mechanisms of sex determination in animals. In many Hymenoptera, including all hitherto investigated social species, diploid individuals, which are heterozygous at the sex locus, develop as females, whereas haploid, hemizygous individuals develop as males (single-locus complementary sex determination, sl-CSD). Inbreeding leads to homozygosity at the sex locus, resulting in the production of diploid males, which are usually sterile and constitute a considerable fitness cost. Nevertheless, regular inbreeding without diploid male production is known from several solitary wasps, suggesting that in these species sex is not determined by sl-CSD but alternative mechanisms. Here, we examine sex determination in an ant with regular inbreeding, Cardiocondyla obscurior. The almost complete absence of diploid males after 10 generations of brother–sister mating in the laboratory documents for the first time the absence of sl-CSD and CSD with two or a few unlinked sex loci in a species of social Hymenoptera. Queens, which mated with a brother, appeared to decrease the number of males in their brood, as expected from the relatedness relationships under inbreeding. In contrast, some colonies began to show signs of an inbreeding depression after several generations of sib-mating, such as shortened queen life span, higher brood mortality, and a shift to more male-biased sex ratios in some colonies, presumably due to lower insemination capability of sperm.

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.

Prudent sperm use by leaf-cutter ant queens

In many species, females store sperm between copulation and egg fertilization, but the consequences of sperm storage and patterns of sperm use for female life history and reproductive success have not been investigated in great detail. In hymenopteran insect societies (ants, bees, wasps), reproduction is usually monopolized by one or relatively few queens, who mate only during a brief period early in life and store sperm for later use. The queens of some ants are particularly long-lived and have the potential to produce millions of offspring during their life. To do so, queens store many sperm cells, and this sperm must remain viable throughout the years of storage. Queens should also be under strong selection to use stored sperm prudently when fertilizing eggs. We used the leaf-cutter ant Atta colombica to investigate the dynamics of sperm use during egg fertilization. We show that queens are able to fertilize close to 100 per cent of the eggs and that the average sperm use per egg is very low, but increases with queen age. The robustness of stored sperm was found to decrease with years of storage, signifying that senescence affects sperm either directly or indirectly via the declining glandular secretions or deteriorating sperm-storage organs. We evaluate our findings with a heuristic model, which suggests that the average queen has sperm for almost 9 years of normal colony development. We discuss the extent to which leaf-cutter ant queens have been able to optimize their sperm expenditure and infer that our observed averages of sperm number, sperm robustness and sperm use are consistent with sperm depletion being a significant cause of mortality of mature colonies of Atta leaf-cutter ants.

Social Hybridogenesis in the Clonal Ant Cataglyphis hispanica

With a few rare exceptions, the vast majority of animals reproduce sexually. Some species have, however, evolved alternative modes of reproduction by shifting from classical bisexuality to unorthodox reproductive systems, like parthenogenesis, gynogenesis, or hybridogenesis. Under hybridogenesis, both the maternal and paternal genomes are expressed in somatic tissues, whereas the germline is purely maternal. Recently, a form of hybridogenesis at the level of the society has been reported in some ants, where purebred females develop into reproductive queens and interlineage hybrids into sterile workers. Here, we report a unique case of social hybridogenesis in the desert ant Cataglyphis hispanica. Workers are produced exclusively from interbreeding between two distinct genetic lineages, whereas male and female sexuals are produced by asexual reproduction through parthenogenesis. As a consequence, all workers are pure hybridogens, and only maternal genes are perpetuated from one generation to the next. Thus, queens of C. hispanica use sexual reproduction for colony growth, whereas they reproduce asexually through parthenogenesis for germline production.

Dual mechanism of queen influence over sex ratio in the ant Pheidole pallidula

Social Hymenoptera are general models for the study of parent-offspring conflict over sex ratio, because queens and workers frequently have different reproductive optima. The ant Pheidole pallidula shows a split distribution of sex ratios with most of the colonies producing reproductives of a single sex. Sex ratio specialization is tightly associated with the breeding system, with single-queen (monogynous) colonies producing male-biased brood and multiple-queen (polygynous) colonies female-biased brood. Here, we show that this sex specialization is primarily determined by the queen’s influence over colony sex ratio. Queens from monogynous colonies produce a significantly more male-biased primary sex ratio than queens from polygynous colonies. Moreover, queens from monogynous colonies produce a significantly lower proportion of diploid eggs that develop into queens and this is associated with lower rate of juvenile hormone (JH) production compared to queens from polygynous colonies. These results indicate that queens regulate colony sex ratio in two complementary ways: by determining the proportion of female eggs laid and by hormonally biasing the development of female eggs into either a worker or reproductive form. This is the first time that such a dual system of queen influence over colony sex ratio is identified in an ant.