Thèse de doctorat
| Résumé : | A key feature of social Hymenoptera is the division of labor in reproduction between one or a few fertile individuals – the queen(s) – and many sterile nestmates that function as helpers – the workers. The reproductive altruism of workers has long been considered as one of the most important paradox of Evolution. Today, kin selection (Hamilton 1964a,b) is recognized as a prime selective force for the evolution reproductive altruism in Hymenoptera. Hamilton’s kin selection theory states that workers may benefit helping relatives reproduce as long as the relatives they aid share a higher than average proportion of their genes with the workers and effectively pass on copies of the workers' genes to the next generation. Relatedness between colony members is therefore pivotal in kin selection theory, because it directly influences the benefits from indirect fitness. In social Hymenoptera, within-colony relatedness is usually high, because of the haplodiploid sex determinism system. However, several factors of the breeding system are known to affect the colony genetic structure and, hence, the workers’ indirect inclusive fitness: the number of breeders, their genetic relationships and their relative contribution to the reproduction. On the other hand, dispersal strategies influence the population genetic structure, which in turn may result in different interaction patterns between members from neighboring colonies. Despite its central role in the evolution of cooperation and reproductive altruism in animals, kin selection also predicts conflicts between colony members. Because the individuals from a colony are not genetically identical, their reproductive interests may be different (Trivers 1974). These conflicts are diversified, both regarding their actors and their causes (Trivers & Hare 1976; Bourke & Franks 1995; Keller 1995; Chapuisat & Keller 1999b; Keller & Reeve 1999; Sundström & Boomsma 2001). The first part of this work deals with the population genetic structure, mating system and dispersal strategies of two Pheidole ants, the Mediterranean ant Pheidole pallidula and the Mojave Desert ant Pheidole tucsonica. Chapter 1 investigates the population genetic structure, the breeding system, the colony kin composition and the colony genetic structure of the Mediterranean ant P. pallidula. This study was performed by using highly polymorphic DNA microsatellite marker loci. The results show that a single, unrelated male inseminates each queen. Colonies are monogynous (i.e. headed by one reproductive queen) or polygynous (i.e. headed by 2 to 4 functional queens). Moreover, they are genetically differentiated and form a population exhibiting significant isolation-by-distance, suggesting that some colonies originate through budding. Chapter 2 reports cross-species amplifications of microsatellite markers developed for the ant P. pallidula on 13 ant species belonging to the sub-family Myrmicinae. Moreover, levels of genetic diversity within a colony, as well as relationship among colonies are studied for the black ant Pheidole tucsonica. Chapter 3 characterizes the level of inter-nest aggression, the spatial distribution and the genetic structure of a P. tucsonica population. The results show that inter-colony aggression varies from none to “all out” fights and that it is largely non-transitive. No effect of geographical distance or genetic structure on inter-nest aggression levels is detected. Moreover, genetic data reveal high rates of polygyny and/or polyandry. Overall, these results do not support the idea of a simple mechanism of nestmate recognition through queen or worker-produced pheromones or environmental cues. The second part of this work is devoted to the queen-queen conflict over reproduction, and the queen-workers conflict over sex allocation in P. pallidula. Chapter 4 is a detailed analysis on the partitioning of reproduction among queens in polygynous colonies of the species. Our results show a significant departure from equal contribution of queens to reproductive female, male and worker production. Reproductive skew is greater for male production than for queen and worker production. There is no relationship between the magnitude of the reproductive skew and (i) the number of reproductive queens per colony, (ii) their relatedness and (iii) the overall colony productivity, some of the factors predicted to influence the extent of reproductive skew. Finally, this study reveals a trade-off in the relative contribution of nestmate queens to reproductive female and worker production. The queens contributing more to reproductive female production contribute significantly less to worker production. To our knowledge, such a trade-off is shown for the first time in the Formicidae. Chapter 5 focuses on queen-workers conflict over sex allocation. Colonies of the Mediterranean ant P. pallidula show a strong split sex ratio, with 85% colonies producing more than 80% sexuals of one sex. Genetic analyses reveal that this species has an unusual breeding system, with colonies being headed by a single or a few unrelated queens. As expected in such a breeding system, our results show no variation in relatedness asymmetry between monogynous (single queen per colony) and polygynous colonies. Nevertheless, sex allocation is tightly associated with the breeding structure, with monogynous colonies producing a male-biased brood and polygynous colonies almost only females. In addition, sex allocation is closely correlated with colony total sexual productivity. Overall, our data show that when colonies become more productive (and presumably larger) they shift from monogyny to polygyny and from male production to female production, a pattern that has never been reported in social insects so far. A new explanation based on the concept of the “tragedy of the commons” is proposed to explain the strong sex ratio specialization observed in P. pallidula and in other species characterized by facultative polygyny. Chapter 6 investigates the relationship between the breeding system (monogynous vs. polygynous colonies) and the biosynthesis rate of juvenile hormone. Previous works in P. pallidula showed (i) that maternal effects induced by hormones and/or other compounds transferred to the eggs could influence the caste fate of female eggs and (ii) that sex specialization is tightly associated with the breeding structure (monogynous colonies produce a male-biased brood and polygynous colonies almost only females - Chapter 5). This study reveals a strong relationship between the biosynthetic rate of juvenile hormone (JH) production and the breeding system. Because in this species the breeding structure is closely associated with colony sex ratio, we propose that the rate of JH in queens could be a critical parameter in colony sex ratio determination. Queens of P. pallidula would exert partial control over sex ratio by laying different proportions of worker-destined eggs and queen-destined eggs according to the structure monogynous or polygynous of their colony. To conclude, some perspectives for future research on the different topics presented in this work are suggested. |
