Extended family structure in the ant Formica paralugubris: the role of the breeding system

In populations of various ant species, many queens reproduce in the same nest (polygyny), and colony boundaries appear to be absent with individuals able to move fi eely between nests (unicoloniality). Such societies depart strongly from a simple family structure and pose a potential challenge to kin selection theory, because high queen number coupled with unrestricted gene flow among nests should result in levels of relatedness among nestmates close to zero. This study investigated the breeding system and genetic structure of a highly polygynous and largely unicolonial population of the wood ant Formica paralugubris. A microsatellite analysis revealed that nestmate workers, reproductive queens and reproductive males (the queens' mates) are all equally related to each other, with relatedness estimates centring around 0.14. This suggests that most of the queens and males reproducing in the study population had mated within or close to their natal nest, and that the queens did not disperse far after mating. We developed a theoretical model to investigate how the breeding system affects the relatedness structure of polygynous colonies. By combining the model and our empirical data, it was estimated that about 99.8% of the reproducing queens and males originated from within the nest, or from a nearby nest. This high rate of local mating and the rarity of long-distance dispersal maintain significant relatedness among nestmates, and contrast with the common view that unicoloniality is coupled with unrestricted gene flow among nests.

Local Competition, Inbreeding, and the Evolution of Sex-Biased Dispersal.

Using game theory, we developed a kin-selection model to investigate the consequences of local competition and inbreeding depression on the evolution of natal dispersal. Mating systems have the potential to favor strong sex biases in dispersal because sex differences in potential reproductive success affect the balance between local resource competition and local mate competition. No bias is expected when local competition equally affects males and females, as happens in monogamous systems and also in polygynous or promiscuous ones as long as female fitness is limited by extrinsic factors (breeding resources). In contrast, a male-biased dispersal is predicted when local mate competition exceeds local resource competition, as happens under polygyny/promiscuity when female fitness is limited by intrinsic factors (maximal rate of processing resources rather than resources themselves). This bias is reinforced by among-sex interactions: female philopatry enhances breeding opportunities for related males, while male dispersal decreases the chances that related females will inbreed. These results meet empirical patterns in mammals: polygynous/promiscuous species usually display a male-biased dispersal, while both sexes disperse in monogamous species. A parallel is drawn with sex-ratio theory, which also predicts biases toward the sex that suffers less from local competition. Optimal sex ratios and optimal sex-specific dispersal show mutual dependence, which argues for the development of coevolution models.

Effects of the social environment on the survival and fungal resistance of ant brood

The phenotype of social animals can be influenced by genetic, maternal and environmental effects, which include social interactions during development. In social insects, the social environment and genetic origin of brood can each influence a whole suite of traits, from individual size to caste differentiation. Here, we investigate to which degree the social environment during development affects the survival and fungal resistance of ant brood of known maternal origin. We manipulated one component of the social environment, the worker/brood ratio, of brood originating from single queens of Formica selysi. We monitored the survival of brood and measured the head size and ability to resist the entomopathogenic fungus Beauveria bassiana of the resulting callow workers. The worker/brood ratio and origin of eggs affected the survival and maturation time of the brood and the size of the resulting callow workers. The survival of the callow workers varied greatly according to their origin, both in controls and when challenged with B. bassiana. However, there was no interaction between the fungal challenge and either the worker/brood ratio or origin of eggs, suggesting that these factors did not affect parasite resistance in the conditions tested. Overall, the social conditions during brood rearing and the origin of eggs had a strong impact on brood traits that are important for fitness. We detected a surprisingly large amount of variation among queens in the survival of their brood reared in standard queenless conditions, which calls for further studies on genetic, maternal and social effects influencing brood development in the social insects.

Selective inhibition of CTL activation by a dipalmitoyl-phospholipid that prevents the recruitment of signaling molecules to lipid rafts.

Antigen-specific T-cell activation implicates a redistribution of plasma membrane-bound molecules in lipid rafts, such as the coreceptors CD8 and CD4, the Src kinases Lek and Fyn, and the linker for activation of T cells (LAT), that results in the formation of signaling complexes. These molecules partition in lipid rafts because of palmitoylation of cytoplasmic, membrane proximal cysteines, which is essential for their functional integrity in T-cell activation. Here, we show that exogenous dipalmitoyl-phosphatidylethanolamine (DPPE), but not the related unsaturated dioleoyl-phosphatidylethanolamine (DOPE), partitions in lipid rafts. DPPE inhibits activation of CD8(+) T lymphocytes by sensitized syngeneic antigen-presenting cells or specific major histocompatibility complex (MHC) peptide tetramers, as indicated by esterase release and intracellular calcium mobilization. Cytotoxic, T lymphocyte (CTL)-target cell conjugate formation is not affected by DPPE, indicating that engagement of the T-cell receptor by its cognate ligand is intact in lipid-treated cells. In contrast to other agents known to block raft-dependent signaling, DPPE efficiently inhibits the MHC peptide-induced recruitment of palmitoylated signaling molecules to lipid rafts and CTL activation without affecting cell viability or lipid raft integrity.

Massive nest-box supplementation boosts fecundity, survival and even immigration without altering mating and reproductive behaviour in a rapidly recovered bird population.

Habitat restoration measures may result in artificially high breeding density, for instance when nest-boxes saturate the environment, which can negatively impact species' demography. Potential risks include changes in mating and reproductive behaviour such as increased extra-pair paternity, conspecific brood parasitism, and polygyny. Under particular cicumstances, these mechanisms may disrupt reproduction, with populations dragged into an extinction vortex. With the use of nuclear microsatellite markers, we investigated the occurrence of these potentially negative effects in a recovered population of a rare secondary cavity-nesting farmland bird of Central Europe, the hoopoe (Upupa epops). High intensity farming in the study area has resulted in a total eradication of cavity trees, depriving hoopoes from breeding sites. An intensive nest-box campaign rectified this problem, resulting in a spectacular population recovery within a few years only. There was some concern, however, that the new, high artificially-induced breeding density might alter hoopoe mating and reproductive behaviour. As the species underwent a serious demographic bottleneck in the 1970-1990s, we also used the microsatellite markers to reconstitute the demo-genetic history of the population, looking in particular for signs of genetic erosion. We found i) a low occurrence of extra-pair paternity, polygyny and conspecific brood parasitism, ii) a high level of neutral genetic diversity (mean number of alleles and expected heterozygosity per locus: 13.8 and 83%, respectively) and, iii) evidence for genetic connectivity through recent immigration of individuals from well differentiated populations. The recent increase in breeding density did thus not induce so far any noticeable detrimental changes in mating and reproductive behaviour. The demographic bottleneck undergone by the population in the 1970s-1990s was furthermore not accompanied by any significant drop in neutral genetic diversity. Finally, genetic data converged with a concomitant demographic study to evidence that immigration strongly contributed to local population recovery.

Genetic differentiation of disjunct populations of the ants Formicaaquilonia and Formica lugubris in Europe.

The species Formica aquilonia and F. lugubris of the mound-building red wood ants have a disjunct boreoalpine distribution in Europe. The populations of F. aquilonia in Finland, Switzerland and the British Isles show little genetic differentiation, whereas the populations of F. lugubris show considerable differentiation. The Central European populations morphologically identified as F. lugubris can be genetically divided into two groups (here called types A and B). Type B is found in the Alps and the Jura mountains, and is genetically inseparable from F. aquilonia. Type A lives sympatrically with type B in the Jura mountains and is also found in the British Isles. Sympatry of the two types in the Jura shows that these are separate species. It remains open whether type B is morphologically atypical F. aquilonia or whether it is a separate species, perhaps with a past history of introgression between F. aquilonia and F. lugubris. The gene frequencies in the Finnish populations of F. lugubris differ from those of both types A and B. Genetic differences within F. lugubris indicate that the populations have evolved separately for a long time. The social structure of F. lugubris colonies also shows geographic variation. The nests in Finland and the British Isles seem to be mainly monogynous and monodomous, whereas the nests in Central Europe are polygynous and form polydomous colonies. F. aquilonia has polygynous and polydomous colonies in all populations studied.

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

Impact of social structure variation on population genetics, social conflicts and life histories in ants

Summary The evolution of social structures and breeding systems in animals is a complex process that combines ecological, genetical and social factors. This thesis sheds light on important changes in population genetics, life-history and social behavior that are associated with variation in social structure in ants. The socially polymorphic ant Formica selysi was chosen as the model organism because single- and multiple-queen colonies occur in close proximity within a single large population. The shift from single- to multiple-queen colonies is generally associated with profound changes in dispersal behavior and mode of colony founding. In chapter 1, we examine the genetic consequences of variation in social structure at both the colony and population levels. A detailed microsatellite analysis reveals that both colony types have similar mating systems, with few or no queen turnover. Furthermore, the complete lack of genetic differentiation observed between single- and multiple-queen colonies provides no support to the hypothesis that change in queen number leads to restricted gene flow between social forms. Besides changes in the genetic composition of the colony, the variation in the number of queens per colony is associated with changes in a network of behavioral and life-history traits that have been described as forming a "polygyny syndrome". In chapter 2, we demonstrate that multiple-queen colonies profoundly differ from single-queen ones in terms of size, nest density and lifespan of colonies, in weight of queens produced, as well as in allocation to reproductive individuals relative to workers. These multifaceted changes in life-history traits can provide various fitness benefits to members of multiple-queen colonies. Increasing the number of queens in a colony usually results in a decreased level of aggression towards non-nestmates. The phenotype matching hypothesis predicts that, compared to single-queen colonies, multiple-queen colonies have more diverse genetically-derived cues used for recognition, resulting in a lower ability to discriminate non-nestmates. In sharp contrast to this hypothesis, we show in chapter 3 that single- and multiple-queen colonies exhibit on average similar levels of aggression. Moreover, stronger aggression is recorded between colonies of different social structure than between colonies of the same social structure. Several hypotheses propose that the evolution of multiple-queen colonies is at least partly due to benefits resulting from an increase in colony genetic diversity. The task-efficiency hypothesis holds that genetic variation improves task performance due to a more complete or more sensitive expression of the genetically-based division of labor. In .chapter 4, we evaluate if higher colony genetic diversity increases worker size polymorphism and thus may improve division of labor. We show that despite the fact that worker size has a heritable component, higher levels of genetic diversity do not result in more polymorphic workers. The smaller size and lower polymorphism levels of workers of multiple-queen colonies compared to single-queen ones further indicate that an increase in colony genetic diversity does not increase worker size polymorphism but might improve colony homeostasis. In chapter 5, we provide clear evidence for an ongoing conflict between queens and workers on sex allocation, as predicted by kin selection theory. Our data show that queens of F. selysi strongly influence colony sex allocation by biasing the sex ratio of their eggs. However, there is also evidence that workers eliminated some male brood, resulting in a population sex-investment ratio that is between the queens' and workers' equilibria. Résumé L'évolution des structures sociales et systèmes d'accouplement chez les animaux est un processus complexe combinant à la fois des facteurs écologiques, génétiques et sociaux. Cette thèse met en lumière des changements importants dans la génétique des populations, les traits d'histoire de vie et les comportements sociaux qui sont associés à des variations de structure sociale chez les fourmis. Durant ce travail, nous avons étudié une population de Formica selysi composée à la fois de colonies à une reine et de colonies à plusieurs reines. La transition de colonie à une reine à colonie à plusieurs reines est généralement associée à des changements profonds dans le comportement de dispersion ainsi que le mode de fondation des sociétés. Dans le chapitre 1, nous examinons les conséquences génétiques de la variation de structure sociale tant au niveau de la colonie qu'au niveau de la population. Une analyse détaillée à l'aide de marqueurs microsatellites nous révèle que les deux types de colonies ont des systèmes d'accouplements similaires avec peu ou pas de renouvellement de reines. L'absence totale de différenciation génétique entre les colonies à une et à plusieurs reines n'apporte aucun support à l'hypothèse selon laquelle un changement dans le nombre de reines conduit à un flux de gènes restreint entre les deux formes sociales. A côté de changements dans la composition génétique de la colonie, la variation du nombre de reines dans une colonie est associée à une multitude de changements comportementaux et de traits d'histoire de vie qui ont été décrits comme formant un "syndrome polygyne". Dans le chapitre 2, nous démontrons que les colonies à plusieurs reines diffèrent profondément des colonies à une reine en terme de taille, densité de nids, longévité des colonies, poids des nouvelles reines produites ainsi que dans l'allocation entre les individus reproducteurs et les ouvrières. Ces changements multiples dans les traits d'histoire de vie peuvent apporter des bénéfices variés en terme de fitness aux colonies à plusieurs reines. L'augmentation du nombre de reines dans une colonie est généralement associée à une baisse du degré d'agressivité envers les fourmis étrangères au nid. L'hypothèse "phénotype matching" prédit que les colonies à plusieurs reines ont une plus grande diversité dans les facteurs d'origine génétique utilisés pour la reconnaissance, résultant en une capacité diminuée à discriminer une fourmi étrangère au nid. Contrairement à cette hypothèse, nous montrons dans le chapitre 3 que les colonies à une et à plusieurs reines ont des niveaux d'agressivité similaires. De plus, une agressivité accrue est observée entre colonies de structures sociales différentes comparée à des colonies de même structure sociale. Plusieurs hypothèses ont proposé que l'évolution de colonies ä plusieurs reines soit en partie due aux bénéfices résultant d'une augmentation de la diversité génétique dans la colonie. L'hypothèse "task efficiency" prédit que la diversité génétique améliore l'efficacité à effectuer certaines tâches grâce à une expression plus complète et plus souple d'une division du travail génétiquement déterminée. Nous évaluons dans le chapitre 4 si un accroissement de la diversité génétique augmente le polymorphisme de taille des ouvrières, d'où peut ainsi découler une meilleure division du travail. Nous montrons qu'en dépit du fait que la taille des ouvrières soit un caractère héritable, une forte diversité génétique ne se traduit pas par un plus fort polymorphisme chez les ouvrières. Les ouvrières de colonies à plusieurs reines sont plus petites et moins polymorphes que celles des colonies à une seule reine. Dans le chapitre 5, nous démontrons l'existence d'un conflit ouvert entre reines et ouvrières à propos de l'allocation dans les sexes, comme le prédit la théorie de la sélection de parentèle. Nos données révèlent que les reines de F. selysi influencent fortement l'allocation dans les sexes en biaisant la sexe ratio des oeufs. Cependant, certains indices indiquent que les ouvrières éliminent une partie du couvain mâle, ce qui a pour effet d'avoir un investissement dans les sexes au niveau de la population intermédiaire entre les intérêts des reines et des ouvrières.

Genotyping faeces reveals facultative kin association on capercaillie's leks

The role that kin selection might play in the evolution of lekking in birds remains controversial. Recent molecular data suggest that males displaying on leks are related. Here we investigated the genetic structure and pattern of relatedness on leks of a declining population of capercaillie (Tetrao urogallus) using microsatellite genetic markers. Since the species is highly sensitive to disturbance, we adopted a non-invasive method by using faecal samples collected in the field. Based on a dataset of 50 males distributed in 6 sub-populations, we found significant genetic structuring among sub-populations, and a significant pattern of isolation by distance among leks. Estimates of relatedness showed that males displaying on the same lek were related, even when controlling for the effects of genetical differentiation among sub-populations. In addition, the frequency distribution of relatedness values indicated that leks contain a mixture of close kin and unrelated individuals (34 and 66%, respectively). This pattern is consistent with the hypothesis that leks often contain kin associations, which might be due to very restricted dispersal of some of the males or to joint dispersal of kin. The results are discussed with respect to their implication for the conservation of endangered populations.

Queen execution in the Argentine ant, Iridomyrmex humilis

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.

Bidirectional shifts in colony queen number in a socially polymorphic ant population.

The breeding system of social organisms affects many important aspects of social life. Some species vary greatly in the number of breeders per group, but the mechanisms and selective pressures contributing to the maintenance of this polymorphism in social structure remain poorly understood. Here, we take advantage of a genetic dataset that spans 15 years to investigate the dynamics of colony queen number within a socially polymorphic ant species. Our study population of Formica selysi has single- and multiple-queen colonies. We found that the social structure of this species is somewhat flexible: on average, each year 3.2% of the single-queen colonies became polygynous, and conversely 1.4% of the multiple-queen colonies became monogynous. The annualized queen replacement rates were 10.3% and 11.9% for single- and multiple-queen colonies, respectively. New queens were often but not always related to previous colony members. At the population level, the social polymorphism appeared stable. There was no genetic differentiation between single- and multiple-queen colonies at eight microsatellite loci, suggesting ongoing gene flow between social forms. Overall, the regular and bidirectional changes in queen number indicate that social structure is a labile trait in F. selysi, with neither form being favored within a time-frame of 15 years.

The role of territory choice mate choice and arrival date on breeding success in the Savi's warbler (Locustella luscinioides)

We investigated how territory quality, settlement date and morphometry affected several components of yearly breeding success of a Swiss population of Savi's Warblers Locustella luscinioides. Territories occupied by males differed from unoccupied sites of similar size and location by having higher and denser reeds, a more extensive straw litter, and a thicker cover of dead sedge leaves. Territories with these characteristics were the ones first chosen by males upon spring arrival. These males, however, did not differ in morphometry from those that arrived later. Availability of suitable nesting sites; rather than food availability, appears to be an important choice criterion for territories. Early arriving males had higher breeding success than late males because of a higher mating success and more successful clutches. The positive correlation between male breeding success and territory quality was thus mediated through their common dependence on occupancy date. Female breeding success decreased with the date of first-clutch laying, mainly because late-nesting females fledged fewer broods. Breeding success in either sex did not correlate with morphometry. Our results provide clear support for territory choice by males, but not for mate or territory choice by females, and show the crucial role played by individual settlement date on many aspects of the breeding cycle of both sexes. We propose a lottery model of mate choice. arriving females obtain the best available territories even without choosing mates or territories; since males occupy territories sequentially and in order of decreasing quality, the few unpaired males available at any moment also occupy the best available territories.

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.

Polymorphic social organization in an ant.

Identifying species exhibiting variation in social organization is an important step towards explaining the genetic and environmental factors underlying social evolution. In most studied populations of the ant Leptothorax acervorum, reproduction is shared among queens in multiple queen colonies (polygyny). By contrast, reports from other populations, but based on weaker evidence, suggest a single queen may monopolize all reproduction in multiple queen colonies (functional monogyny). Here we identify a marked polymorphism in social organization in this species, by conclusively showing that functional monogyny is exhibited in a Spanish population, showing that the social organization is stable and not purely a consequence of daughter queens overwintering, that daughter queen re-adoption is frequent and queen turnover is low. Importantly, we show that polygynous and functionally monogynous populations are not genetically distinct from one another based on mtDNA and nDNA. This suggests a recent evolutionary divergence between social phenotypes. Finally, when functionally monogynous and polygynous colonies were kept under identical laboratory conditions, social organization did not change, suggesting a genetic basis for the polymorphism. We discuss the implications of these findings to the study of reproductive skew.

Breeding system and genetic variance in the monogamous, semi-social shrew, Crocidura russula

The population-genetic consequences of monogamy and male philopatry (a rare breeding system in mammals) were investigated using microsatellite markers in the semisocial and anthropophilic shrew Crocidura russula. A hierarchical sampling design over a 16-km geographical transect revealed a large genetic diversity (h = 0.813) with significant differentiation among subpopulations (F-ST = 5-6%), which suggests an exchange of 4.4 migrants per generation. Demic effective-size estimates were very high, due both to this limited gene inflow and to the inner structure of subpopulations. These were made of 13-20 smaller units (breeding groups), comprising an estimate of four breeding pairs each. Members of the same breeding groups displayed significant coancestries (F-LS = 9-10%), which was essentially due to strong male kinship: syntopic males were on average related at the half-sib level. Female dispersal among breeding groups was not complete (similar to 39%), and insufficient to prevent inbreeding. From our results, the breeding strategy of C. russula seems less efficient than classical mammalian systems (polygyny and male dispersal) in disentangling coancestry from inbreeding, but more so in retaining genetic variance.