The evolutionary fate of parthenogenetic ants' societies

Parthenogenetic eusocial insects (among ants and bees) combine two lingering and exciting issues: the evolution of sex on the one hand, and the evolution of social behaviour on the other hand, undoubtedly the "Royal Couple" for evolutionists! Important insights may arise from the comparative study of these few species displaying different and sometimes extraordinary social structure. Notably, new and original factors contributing to the paradoxical maintenance of sex can be identified. Relying on recent major discovers in ants, I here venture the hypothesis that evolution towards parthenogenesis may be constrained by aspects of social organisation. These proximate mechanisms would act for the maintenance of sex, regardless of the theoretically advantageous genetic variance then provided at the colony level. Indeed, the social structure of eusocial hymenoptera is the locus of permanent kin conflicts and hinges on task partitioning between a sexual and a worker caste. These characteristics may represent important social constraints preventing the loss of sexuals and would then appear as specific and novel ways to save biparental reproduction. Introduction: The ubiquity of bisexual reproduction (amphimixy) in pluricellular organisms has long been considered “the queen of problems in evolutionary biology” . It indeed seems difficult to explain the success of this strategy in view of its weak efficiency to promote genes, when compared to parthenogenesis and its theoretical two-fold advantage of coping without males (Fig. 1). Numerous hypotheses have been developed to shed light on this crucial issue . Stressing a genetic viewpoint, some hypotheses focus on the efficient purge of the mutation load arising from recombination and amphimixy. Others advocate, in an ecological perspective, the constant shuffling of allelic combinations as a major advantage for sustaining varying selective pressures. Moreover, given that species incapable of retaining bisexual reproduction are likely to disappear after invasion by evolutionary dead-end parthenogens, an alternative standpoint may regard persistent amphimictic species as those that encounter constraints on parthenogenetic development . This underlines the need to determine specific biological barriers that may influence the evolution of parthenogenesis in order to understand its current distribution. In this context, some promising new insights may come from eusocial Hymenoptera (ants and social bees) that developed parthenogenetic reproduction. The behaviour of these insects, thus, reflects two lingering and exciting issues: the evolution of sex on the one hand, and the evolution of social behaviour on the other hand, undoubtedly the "Royal Couple" for evolutionists! Basing on recent serendipitous discoveries 4, , I here venture the hypothesis that evolution towards parthenogenesis may be constrained by some aspects of social organisation that would act as proximate mechanisms for the maintenance of sex . 1) Some extraordinary ants: Original genetic systems were recently reported in two ant species. Queens of Cataglyphis cursor and Wasmannia auropunctata were found to reproduce alternatively by amphimixy and parthenogenesis to produce genetically diverse worker offspring and clonal gynes, respectively 4, . One can wonder why C. cursor and W. auropunctata have not discarded amphimixy by queens despite its persistent cost. Alternating between both modes of reproduction may represent the optimal strategy for an ant species, as it leads to a more efficient promotion of genes through clonal gynes while a highly heterogeneous worker caste may provide the colony with some of the benefits usually advocated for genetic diversity. Decreased relatedness between workers might help to enhance colony homeostasis and division of labour, and ensure an invaluable lead in the arms race against pathogens. Nevertheless, though theoretically stimulating, these putative short-term advantages suffer weak empirical demonstration and it is not clear whether they could resist clonal reproduction by selfish individuals. 2) Worker policing as a possible social constraint upon parthenogenesis In insect societies, selfish reproduction can be prevented by collective behaviours, such as mutual policing . Nestmates (queens and/or workers) may harass reproductive workers or selectively destroy worker-laid eggs. Theory predicts that worker policing will be selected when their selfish reproduction leads to a fall in colony efficiency and/or when the colony kin structure induces a decreased mean relatedness among workers . A decreased relatedness may, indeed, enhance social cohesion by lessening potential kin conflicts over reproduction. This last point is crucial and may prove to mortgage the raising of a fully parthenogenetic reproduction in C. cursor, and by extension, the evolutionary fate of parthenogenetic societies in social hymenoptera (Fig. 2). Genetical analyses were conducted on 38 colonies of C. cursor using four highly polymorphic microsatellite loci (Table 1). They showed that queens had mated with an average of 5.6 ± 1.3 males (range 4 to 8) . Then, the social structure of C. cursor clearly offers an opportunity for worker policing to emerge. Thus, amphimixy coupled with polyandry allows the queen to save her head and remain the unique reproducer within the colony, for the paradoxical greater genetic advantage of every nestmate, with males excluded as they gain no fitness any more. Consequently, the occurrence of social constraints in C. cursor signs away the further spread of parthenogenesis. 3) Caste determinism as another possible social constraint upon parthenogenesis Nevertheless, the hypothesis of a constraint imposed by kin conflicts, as advocated here for the maintenance of amphimixy in eusocial hymenoptera, cannot apply straightaway to the late case of parthenogenesis just demonstrated in ants 4 (Table 2). This should stimulate the search for alternative specific constraints on parthenogenesis. For instance, though caste determination in social hymenoptera is usually assumed to be environmentally induced, genetically determined caste differentiation was also recently demonstrated in two other ant species . Here, the level of heterozygosity at a single locus governs the developmental fate of larvae towards the queen or worker caste (Fig. 3). A similar genetic process may also be at work in W. auropunctata (Table 2). It could explain, indeed, why workers agree to rear clonal gynes that are less related to them than sexually produced sisters. Given the partitioning between the male and female gene pools, workers that usually develop from fertilized eggs are likely to be heterozygous at the putative "caste" locus. On the contrary, parthenogenetic gynes are more prone to homozygosity. Since a colony composed of only gynes has no chance of survival, the absolute necessity of a worker caste, again regardless of the genetic diversity among individuals, would then be a pressing social constraint upon the loss of males. This hypothesis, of course, may also apply to C. cursor with the restriction that polyandry would then be unnecessary (see above). 4) Conclusion and perspectives: The social structure of eusocial hymenoptera provides a locus of permanent kin conflicts and hinges on task partitioning between a sexual and a worker caste. Thus, social constraints preventingthe loss of the sexual caste appear to be a specific and original way to maintain amphimixy in theseinsects. In order to test some of the proposed hypothesis, several experiments can be easilyconducted. First, it appears important to check whether virgin queens can really lay thelytokouseggs. If not, that is if sperm is necessary to induce embryonic development, this would be a muchmore pressing constraint upon parthenogenesis than the proposed social constraint. Secondly,analysing the social structure of other populations belonging to both species but displaying classicalsexual reproduction would help understanding the proximate factors involved there in themaintenance of sex. Finally, additional cases of parthenogenesis in ants, and the study of their socialstructure, will bring a robust test of the social constraint hypothesis. In that context, my project onthe myrmecofauna of Okinawa (Japon Ryukyus), especially the study of several species ofMonomorium sp. (Figure 3) that were recently demonstrated also parthenogenetic (unpublisheddata), is likely to bring important insights. Behavioural observations and micrasatellite analyses arethe main experiments planned for this project. References1. Bell, G. The masterpiece of nature (University of California Press, San Francisco, 1982).2. Kondrashov, A. S. Classification of hypotheses on the advantage of amphimixis. Journal of Heredity 84, 372-387 (1993).3. Gouyon, P.-H. Sex: a pluralist approach includes species selection. (One step beyond and it's good.). Journal ofEvolutionary Biology 12, 1029-1030 (1999).4. Fournier, D. et al. Clonal reproduction by males and females in the little fire ant. Nature 435, 1230-1234(2005).5. Pearcy, M., Aron, S., Doums, C. & Keller, L. Conditional use of sex and parthenogenesis for worker andqueen production in ants. Science 306, 1780-1783 (2004).6. Ravary, F. Sex and sociality: the Royal Couple of evolutionary biology. Submitted.7 Frank, S.A. Mutual policing and repression of competition in the evolution of cooperative groups. Nature 377,520-522 (1995).8 Hammond, R. L., Keller, L. Conflict over male parentage in social insects. PLoS Biology 2 (2004).9. Helms Cahan, S. & Keller, L. Complex hybrid origin of genetic caste determination in harvester ants. Nature424, 306-309 (2003).AcknowledgmentsThe author wishes to thank the Japanese Society for the Promotion of Science (JSPS) for providing financial support.