The economics of anti-parasite defences in animal societies

RESUME : De nombreuses espèces animales vivent en groupe. Du simple grégarisme aux colonies hautement intégrées de fourmis, la vie sociale a atteint des degrés divers de complexité. Les nombreuses interactions entre membres d'une société favorisent la transmission de parasites. Cela représente un coût potentiel de la vie sociale. Cette thèse s'intéresse aux défenses permettant de réduire le coût du parasitisme dans les colonies de fourmis ainsi qu'à la manière dont le parasitisme a pu façonner certains aspects de ces sociétés. Les colonies de fourmis des bois (Forimica paralugubris) contiennent de grandes quantités de résine de conifères. Cette résine réduit la densité microbienne dans le nid et augmente la survie des ouvrières lors d'infections parasitaires. Dans cette thèse, nous montrons, d'une part, que les ouvrières collectent activement la résine et que ce comportement est plutôt préventif que curatif et, d'autre part, que la résine permet aux ouvrières une utilisation moindre de leurs défenses immunitaires. Ces résultats permettent de conclure que ce comportement réduit l'exposition au parasitisme et qu'il a une fonction adaptative. L'émergence d'un tel comportement de médication chez une espèce d'insectes sociaux illustre le fait que la socialité, bien yue provoquant une exposition accrue au parasitisme, permet également l'émergence de mécanismes sociaux de défense. II a été suggéré que la présence de plusieurs reines au sein d'un même nid (polygynie) améliore la résistance aux parasites en augmentant la diversité génétique au sein de la colonie. En accord avec cette hypothèse, nous montrons qu'une augmentation de la diversité génétique au sein de groupes expérimentaux de Formica selysi améliore leur survie lors d'une infection parasitaire. Cependant, nous suggérons également que sur le terrain, d'autres facteurs corrélés à la polygynie ont des effets antagoniques sur la résistance. Nous montrons par exemple que les ouvrières polygynes semblent avoir une capacité moindre à monter une réponse immunitaire. Certains aspects de la reproduction des fourmis ont pu également être façonnés par le parasitisme. L'accouplement n'a lieu que lors d'une courte période au début de la vie adulte, généralement à l'extérieur de la colonie. Les reines stockent ensuite le sperme et l'utilisent parcimonieusement au cours de leur vie alors que les males meurent rapidement. Nous montrons que les défenses immunitaires des reines de fourmis des bois (F. paralugubris) sont fortement affectées par l'accouplement. Ces modulations immunitaires sont probablement liées à une augmentation de l'exposition au parasitisme lors de l'accouplement ainsi qu'à des blessures copulatoires. I1 semble donc que l'accouplement soit accompagné de coûts immunitaires pour les reines. Dans son ensemble, cette thèse illustre la diversité des mécanismes de défenses contre les parasites dans les sociétés de fourmis. La vie sociale, en offrant un nouveau niveau d'interaction, permet en effet l'émergence d'adaptations originales. Cela explique probablement le grand succès écologique des espèces sociales. SUMMARY : Sociality is widespread among animals and has reached variable degrees of complexity, from loose social Groups to highly integrated ant colonies. The many interactions between members of a social group promote the spread of parasites, but social life also permits the evolution of original defence mechanisms. This thesis sheds light on how ant colonies defend themselves against parasites, and on how parasitism shapes certain aspects of these societies. Wood ants nests (Formica paralugubris) contain large amounts of conifer resin which reduces the microbial density in ant nests and enhances the survival of ants challenged by some pathogens. We show that resin is actively collected by workers and that resin collection is rather a prophylactic than a curative behaviour. Moreover, we suggest that resin reduces the use of the immune defences of workers. Altogether, these results indicate that the use of resin is a collective adaptation to prevent the spread of parasites. The emergence of medication in a social insect species illustrates that sociality does not only increase the exposure to parasites but also allows the emergence of social mechanisms to counter this threat. The number of reproducing queens per colony is a variable trait in ants. It has been suggested that polygyny (the occurrence of multiple queens within a colony), by increasing the colonial genetic diversity, improves disease resistance. In line with this hypothesis, we show that in a socially polymorphic ant (Formica selysi), an experimental increase of colony genetic diversity enhances disease resistance. However, we also suggest that factors covarying with queen number variation in the field have antagonistic effects on parasite resistance. We show for instance that polygyne workers seem to have lower immune defences. Parasites may also shape some aspects of ant queen reproductive biology. Ant queens mate at the beginning of their adult life, usually outside of the colony, and store sperm for several years to fertilize eggs. Males die shortly after mating and queens never remate later in life, which drastically reduces sexual conflicts. Moreover, mating and nest founding occur away from the collective defence mechanisms of the natal colony and might be associated with an increased risk of parasitism. We show that mating affects the immune defences of wood ant queens (F. paralugubris) in multiple ways that are consistent with mating wounds and increased risk of parasitism. We suggest that mating is associated with immunity costs in ants, despite the reduced level of sexual conflicts. Altogether, my thesis illustrates the diversity of anti-parasite mechanisms in ant societies. This sheds light on how sociality, by offering a new level of interactions, allows the evolution of original adaptations, which may explain the wide ecological success of social species.

A double role of sperm in scorpions: the mating plug of Euscorpius italicus (Scorpiones: Euscorpiidae) consists of sperm.

Mating plugs occluding the female gonopore after mating are a widespread phenomenon. In scorpions, two main types of mating plugs are found: sclerotized mating plugs being parts of the spermatophore that break off during mating, and gel-like mating plugs being gelatinous fluids that harden in the female genital tract. In this study, the gel-like mating plug of Euscorpius italicus was investigated with respect to its composition, fine structure, and changes over time. Sperm forms the major component of the mating plug, a phenomenon previously unknown in arachnids. Three parts of the mating plug can be distinguished. The part facing the outside of the female (outer part) contains sperm packages containing inactive spermatozoa. In this state, sperm is transferred. In the median part, the sperm packages get uncoiled to single spermatozoa. In the inner part, free sperm is embedded in a large amount of secretions. Fresh mating plugs are soft gelatinous, later they harden from outside toward inside. This process is completed after 3-5 days. Sperm from artificially triggered spermatophores could be activated by immersion in insect Ringer's solution indicating that the fluid condition in the females' genital tract or females' secretions causes sperm activation. Because of the male origin of the mating plug, it has likely evolved under sperm competition or sexual conflict. As females refused to remate irrespective of the presence or absence of a mating plug, females may have changed their mating behavior in the course of evolution from polyandry to monandry.

Postmating-prezygotic isolation between two allopatric populations of Drosophila montana: fertilisation success differs under sperm competition

Postmating but prezygotic (PMPZ) interactions are increasingly recognized as a potentially important early-stage barrier in the evolution of reproductive isolation. A recent study described a potential example between populations of the same species: single matings between Drosophila montana populations resulted in differential fertilisation success because of the inability of sperm from one population (Vancouver) to penetrate the eggs of the other population (Colorado). As the natural mating system of D. montana is polyandrous (females remate rapidly), we set up double matings of all possible crosses between the same populations to test whether competitive effects between ejaculates influence this PMPZ isolation. We measured premating isolation in no-choice tests, female fecundity, fertility and egg-to-adult viability after single and double matings as well as second-male paternity success (P-2). Surprisingly, we found no PMPZ reproductive isolation between the two populations under a competitive setting, indicating no difficulty of sperm from Vancouver males to fertilize Colorado eggs after double matings. While there were subtle differences in how P-2 changed over time, suggesting that Vancouver males' sperm are somewhat less competitive in a first-male role within Colorado females, these effects did not translate into differences in overall P-2. Fertilisation success can thus differ dramatically between competitive and noncompetitive conditions, perhaps because the males that mate second produce higher quality ejaculates in response to sperm competition. We suggest that unlike in more divergent species comparisons, where sperm competition typically increases reproductive isolation, ejaculate tailoring can reduce the potential for PMPZ isolation when recently diverged populations interbreed.