Abundant small RNAs in the reproductive tissues and eggs of the honey bee, Apis mellifera

Background: Polyandrous social insects such as the honey bee are prime candidates for parental manipulation of gene expression in offspring. Although there is good evidence for parent-of-origin effects in honey bees the epigenetic mechanisms that underlie these effects remain a mystery. Small RNA molecules such as miRNAs, piRNAs and siRNAs play important roles in transgenerational epigenetic inheritance and in the regulation of gene expression during development. Results: Here we present the first characterisation of small RNAs present in honey bee reproductive tissues: ovaries, spermatheca, semen, fertilised and unfertilised eggs, and testes. We show that semen contains fewer piRNAs relative to eggs and ovaries, and that piRNAs and miRNAs which map antisense to genes involved in DNA regulation and developmental processes are differentially expressed between tissues. tRNA fragments are highly abundant in semen and have a similar profile to those seen in the semen of other animals. Intriguingly we also find abundant piRNAs that target the sex determination locus, suggesting that piRNAs may play a role in honey bee sex determination. Conclusions: We conclude that small RNAs may play a fundamental role in honey bee gametogenesis and reproduction and provide a plausible mechanism for parent-of-origin effects on gene expression and reproductive physiology

Conflicts, cooperation and recognition systems in ants of the neoponera apicalis species complex

La coopération et les conflits sont les deux facettes de l’évolution sociale. L’objectif principal de cette thèse a été d’étudier chez les fourmis du complexe d’espèces Neoponera apicalis les mécanismes de régulation permettant de maintenir la coopération dans les groupes sociaux face aux risques d’exploitation internes et externes au groupe, à travers une approche comparative et intégrative. Nous montrons que la structure génétique des colonies entraine des conflits d’intérêts liés à la reproduction, notamment en ce qui concerne la production des mâles. L’étude de la régulation du partage de la reproduction révèle que les décisions reproductives des individus sont principalement basées sur la détection de signaux associés à la fertilité grâce à des capacités fines de discrimination de statut. Ces informations permettent aux ouvrières d’ajuster leur comportement reproducteur selon le contexte social et en fonction de leurs intérêts en termes d’inclusive fitness. En effet, alors qu’une auto-restriction reproductive des ouvrières est observée en présence d’une reine fertile, un conflit ouvert se déclare quand celle-ci disparait, régulé par la mise en place d’une hiérarchie reproductive linéaire dans laquelle les ouvrières de haut rang accèdent à la reproduction. Le signalement du statut reproducteur parait jouer un rôle capital dans la régulation des interactions de dominance/subordination, et donc dans la détermination des rangs hiérarchiques. Les signaux associés à la fertilité sont par ailleurs fortement conservés entre les différentes espèces de ce complexe, ce qui souligne leur honnêteté et donc leur stabilité évolutive. Nous montrons enfin l’existence d’une reconnaissance coloniale chez ces espèces, basée sur les mêmes indices de reconnaissance, et permettant de moduler la réponse territoriale selon le niveau de familiarité des colonies étrangères. Cette étude démontre donc l’importance des mécanismes de reconnaissance dans la régulation de la vie sociale.ASocial evolution implies both cooperation and conflicts. The main objective of this thesis was to study the regulatory mechanisms allowing to maintain cooperation in social groups against exploitation from within and outside. We choose a comparative and integrative approach using ants of the Neoponera apicalis species complex. We show that the colony genetic structure gives rise to reproductive conflicts, particularly over male production. The study of the regulation of the partitioning of reproduction reveals that the individuals’ reproductive decisions are mainly based on the detection of fertility-associated signals through fine-scale status discrimination abilities. This information allows the workers to adjust their reproductive behaviour according to the social context and following their inclusive fitness interests. Whereas worker reproductive self-restraint is observed with a fertile queen, an overt conflict arises in queenless conditions, which is regulated through the formation of a linear reproductive hierarchy where high-ranking workers reproduce. Reproductive status signalling seems to play a crucial role in the regulation of the dominance/subordination relationships, and thus in the determination of hierarchical ranks. Furthermore, fertility-associated signals are highly conserved among the species of the complex, which highlights their honesty and thus their evolutionary stability. We finally show that the nestmate recognition processes in these species are based on the same recognition cues and allow to modulate the territorial response depending on the familiarity with non-nestmates. This study demonstrates the importance of recognition mechanisms in the regulation of social life

Conflits, coopération et systèmes de reconnaissance chez les fourmis du complexe d’espèces neoponera apicalis

ASocial evolution implies both cooperation and conflicts. The main objective of this thesis was to study the regulatory mechanisms allowing to maintain cooperation in social groups against exploitation from within and outside. We choose a comparative and integrative approach using ants of the Neoponera apicalis species complex. We show that the colony genetic structure gives rise to reproductive conflicts, particularly over male production. The study of the regulation of the partitioning of reproduction reveals that the individuals’ reproductive decisions are mainly based on the detection of fertility-associated signals through fine-scale status discrimination abilities. This information allows the workers to adjust their reproductive behaviour according to the social context and following their inclusive fitness interests. Whereas worker reproductive self-restraint is observed with a fertile queen, an overt conflict arises in queenless conditions, which is regulated through the formation of a linear reproductive hierarchy where high-ranking workers reproduce. Reproductive status signalling seems to play a crucial role in the regulation of the dominance/subordination relationships, and thus in the determination of hierarchical ranks. Furthermore, fertility-associated signals are highly conserved among the species of the complex, which highlights their honesty and thus their evolutionary stability. We finally show that the nestmate recognition processes in these species are based on the same recognition cues and allow to modulate the territorial response depending on the familiarity with non-nestmates. This study demonstrates the importance of recognition mechanisms in the regulation of social life.La coopération et les conflits sont les deux facettes de l’évolution sociale. L’objectif principal de cette thèse a été d’étudier chez les fourmis du complexe d’espèces Neoponera apicalis les mécanismes de régulation permettant de maintenir la coopération dans les groupes sociaux face aux risques d’exploitation internes et externes au groupe, à travers une approche comparative et intégrative. Nous montrons que la structure génétique des colonies entraine des conflits d’intérêts liés à la reproduction, notamment en ce qui concerne la production des mâles. L’étude de la régulation du partage de la reproduction révèle que les décisions reproductives des individus sont principalement basées sur la détection de signaux associés à la fertilité grâce à des capacités fines de discrimination de statut. Ces informations permettent aux ouvrières d’ajuster leur comportement reproducteur selon le contexte social et en fonction de leurs intérêts en termes d’inclusive fitness. En effet, alors qu’une auto-restriction reproductive des ouvrières est observée en présence d’une reine fertile, un conflit ouvert se déclare quand celle-ci disparait, régulé par la mise en place d’une hiérarchie reproductive linéaire dans laquelle les ouvrières de haut rang accèdent à la reproduction. Le signalement du statut reproducteur parait jouer un rôle capital dans la régulation des interactions de dominance/subordination, et donc dans la détermination des rangs hiérarchiques. Les signaux associés à la fertilité sont par ailleurs fortement conservés entre les différentes espèces de ce complexe, ce qui souligne leur honnêteté et donc leur stabilité évolutive. Nous montrons enfin l’existence d’une reconnaissance coloniale chez ces espèces, basée sur les mêmes indices de reconnaissance, et permettant de moduler la réponse territoriale selon le niveau de familiarité des colonies étrangères. Cette étude démontre donc l’importance des mécanismes de reconnaissance dans la régulation de la vie sociale

Social context and reproductive potential affect worker reproductive decisions in a eusocial insect.

Context-dependent decision-making conditions individual plasticity and is an integrant part of alternative reproductive strategies. In eusocial Hymenoptera (ants, bees and wasps), the discovery of worker reproductive parasitism recently challenged the view of workers as a homogeneous collective entity and stressed the need to consider them as autonomous units capable of elaborate choices which influence their fitness returns. The reproductive decisions of individual workers thus need to be investigated and taken into account to understand the regulation of reproduction in insect societies. However, we know virtually nothing about the proximate mechanisms at the basis of worker reproductive decisions. Here, we test the hypothesis that the capacity of workers to reproduce in foreign colonies lies in their ability to react differently according to the colonial context and whether this reaction is influenced by a particular internal state. Using the bumble bee Bombus terrestris, we show that workers exhibit an extremely high reproductive plasticity which is conditioned by the social context they experience. Fertile workers reintroduced into their mother colony reverted to sterility, as expected. On the contrary, a high level of ovary activity persisted in fertile workers introduced into a foreign nest, and this despite more frequent direct contacts with the queen and the brood than control workers. Foreign workers' reproductive decisions were not affected by the resident queen, their level of fertility being similar whether or not the queen was removed from the host colony. Workers' physiological state at the time of introduction is also of crucial importance, since infertile workers failed to develop a reproductive phenotype in a foreign nest. Therefore, both internal and environmental factors appear to condition individual reproductive strategies in this species, suggesting that more complex decision-making mechanisms are involved in the regulation of worker reproduction than previously thought

Subfamily-dependent alternative reproductive strategies in worker honeybees

Functional worker sterility is the defining feature of insect societies. Yet, workers are sometimes found reproducing in their own or foreign colonies. The proximate mechanisms underlying these alternative reproductive phenotypes are keys to understanding how reproductive altruism and selfishness are balanced in eusocial insects. In this study, we show that in honeybee (Apis mellifera) colonies, the social environment of a worker, that is, the presence and relatedness of the queens in a worker's natal colony and in surrounding colonies, significantly influences her fertility and drifting behaviour. Furthermore, subfamilies vary in the frequency of worker ovarian activation, propensity to drift and the kind of host colony that is targeted for reproductive parasitism. Our results show that there is an interplay between a worker's subfamily, reproductive state and social environment that substantially affects her reproductive phenotype. Our study further indicates that honeybee populations show substantial genetic variance for worker reproductive strategies, suggesting that no one strategy is optimal under all the circumstances that a typical worker may encounter

Data from: Subfamily-dependent alternative reproductive strategies in worker honey bees

Functional worker sterility is the defining feature of insect societies. Yet, workers are sometimes found reproducing in their own or foreign colonies. The proximate mechanisms underlying these alternative reproductive phenotypes are key to understanding how reproductive altruism and selfishness are balanced in eusocial insects. In this study we show that in honey bee (Apis mellifera) colonies the social environment of a worker, i.e. the presence and relatedness of the queens in a worker’s natal colony and in surrounding colonies, significantly influences her fertility and drifting behaviour. Furthermore, subfamilies vary in the frequency of worker ovarian activation, propensity to drift, and the kind of host colony that is targeted for reproductive parasitism. Our results show that there is an interplay between a worker’s subfamily, reproductive state and social environment that substantially affects her reproductive phenotype. Our study further indicate that honey bee populations show substantial genetic variance for worker reproductive strategies, suggesting that no one strategy is optimal under all the circumstances that a typical worker may encounter

Data

This data file contains 19 worksheets. Worksheet "Data" contains the raw data for all individuals showing their identity, patriline, fertility status (0 = ovaries non-activated, 1 = ovaries activated), drifting status (0 = collected in natal nest, 1 = collected in foreign nest), natal colony identity, social context of the natal colony, host colony identity (if applicable), social context of the host colony (if applicable), distance of drifting in metres (if applicable), and replicate number. Worksheets "QR1" to "HQL6" contain the genotypes of all workers for all microsatellite loci, respectively for each colony (n = 18). The queens' deduced genotypes are also reported for each colony

Behaviour and localization of the bees in the mother condition.

<p>Rate of antennation with the queen (per scan per bee), task allocation (percentage of scans) for all behavioural tasks recorded, and presence on the brood (percentage of scans) for resident and introduced bees in the mother condition. Rare activities (representing <1% of total acts) were excluded from the analysis (exact permutation tests). Data are presented as mean ± standard error.</p

Behaviour and localization of the bees in the infertile foreign condition.

<p>Rate of antennation with the queen (per scan per bee), task allocation (percentage of scans) for all behavioural tasks recorded, and presence on the brood (percentage of scans) for resident and introduced bees in the infertile foreign condition. Rare activities (representing <1% of total acts) were excluded from the analysis (exact permutation tests). Data are presented as mean ± standard error.</p

Ovarian development of control, resident and introduced bees in the various conditions.

<p>Groups of five fertile or infertile bees were introduced into their mother colony or a foreign colony containing or lacking the queen. Resident bees were native workers from the host colony. Infertile control bees were randomly taken from non-manipulated colonies before the competition phase (see Materials and Methods). Fertile control bees were laying workers taken from triads of isolated workers. All workers were of the same age. The different letters denote statistical differences; each analysis (one-way ANOVA with the Monte Carlo procedure followed by post-hoc exact permutation tests corrected for multiple comparisons with the Bonferroni sequential method) is represented by uppercase or lowercase letters. Comparisons between resident and introduced bees for each condition were performed by exact permutation tests. QL, queenless; n.s., not significant; * <i>p</i><0.05; ** <i>p</i><0.01. Data are represented as mean ± standard error.</p