Spatial pattern of floral morphology: a possible insight into the effects of pollinators on plant distribution

Pollination syndromes involve convergent evolution towards phenotypes composed of specific scents, colours or floral morphologies that attract or restrict pollinator access to reward. How these traits might influence the distributions of plant species in interaction with pollinators has rarely been investigated. We sampled 870 vegetation plots in the western Swiss Alps and classified the plant species into seven blossom types according to their floral morphology (wind, disk, funnel, tube, bilabiate, head or brush). We investigated the environmental features of plots with functional diversity (FD) lower than expected by chance alone to detect potential pollination filtering and related the proportions of the seven blossom types to a combination of environmental descriptors. From these results, we inferred the potential effect of the pollinator on the spatial distribution of plant species. The vegetation plots with significantly lower FD of blossom types than expected by chance were found at higher altitudes, and the proportions of blossom types were strongly patterned along the same gradient. These results support a biotic filtering effect on plant species assemblages through pollination: disk blossoms became dominant at higher altitudes, resulting in a lower FD. In harsh conditions at high altitudes, pollinators usually decrease in activity, and the openness of the disk blossom grants access to any available pollinator. Inversely, bilabiate blossoms, which are mostly pollinated by bees, were more abundant at lower elevations, which are characterised by greater abundance and diversity of bees. Generalisation through openness of the blossom could be advantageous at high elevations, while specialisation could be a successful alternative strategy at lower elevations. The approach used in this study is purely correlative, and further investigations should be conducted to infer the nature of the causal relationship between plant and pollinator distributions.

Division of labor in insect societies : genetic components and physiological regulation

The shift from solitary to social organisms constitutes one of the major transitions in evolution. The highest level of sociality is found in social insects (ants, termites and some species of bees and wasps). Division of labor is central to the organization of insect societies and is thought to be at the root of their ecological success. There are two main levels of division of labor in social insect colonies. The first relates to reproduction and involves the coexistence of queen and worker castes: while reproduction is usually monopolized by one or several queens, functionally sterile workers perform all the tasks to maintain the colony, such as nest building, foraging or brood care. The second level of division of labor, relating to such non-reproductive duties, is characterized by the performance of different tasks or roles by different groups of workers. This PhD aims to better understand the mechanisms underlying division of labor in insect societies, by investigating how genes and physiology influence caste determination and worker behavior in ants. In the first axis of this PhD, we studied the nature of genetic effects on division of labor. We used the Argentine ant Linepithema humile to conduct controlled crosses in the laboratory, which revealed the existence of non-additive genetic effects, such as parent-of-origin and genetic compatibility effects, on caste determination and worker behavior. In the second axis, we focused on the physiological regulation of division of labor. Using Pogonomyrmex seed- harvester ants, we performed experimental manipulation of hibernation, hormonal treatments, gene expression analyses and protein quantification to identify the physiological pathways regulating maternal effects on caste determination. Finally, comparing gene expression between nurses and foragers allowed us to reveal the association between vitellogenin and worker behavior in Pogonomyrmex ants. This PhD provides important insights into the role of genes and physiology in the regulation of division of labor in social insect colonies, helping to better understand the organization, evolution and ecological success of insect societies. - L'une des principales transitions évolutives est le passage de la vie solitaire à la vie sociale. La socialité atteint son paroxysme chez les insectes sociaux que sont les fourmis, les termites et certaines espèces d'abeilles et de guêpes. La division du travail est la clé de voûte de l'organisation de ces sociétés d'insectes et la raison principale de leur succès écologique. La division du travail s'effectue à deux niveaux dans les colonies d'insectes sociaux. Le premier niveau concerne la reproduction et implique la coexistence de deux castes : les reines et les ouvrières. Tandis que la reproduction est le plus souvent monopolisée par une ou plusieurs reines, les ouvrières stériles effectuent les tâches nécessaires au bon fonctionnement de la colonie, telles que la construction du nid, la recherche de nourriture ou le soin au couvain. Le second niveau de division du travail, qui concerne les tâches autres que la reproduction, implique la réalisation de différents travaux par différents groupes d'ouvrières. Le but de ce doctorat est de mieux comprendre les mécanismes sous-jacents de la division du travail dans les sociétés d'insectes en étudiant comment les gènes et la physiologie influencent la détermination de la caste et le comportement des ouvrières chez les fourmis. Dans le premier axe de ce doctorat, nous avons étudié la nature des influences génétiques sur la division du travail. Nous avons utilisé la fourmi d'Argentine, Linepithema humile, pour effectuer des croisements contrôlés en laboratoire. Cette méthode nous a permis de révéler l'existence d'influences génétiques non additives, telles que des influences dépendantes de l'origine parentale ou des effets de compatibilité génétique, sur la détermination de la caste et le comportement des ouvrières. Dans le second axe, nous nous sommes intéressés à la régulation physiologique de la division du travail. Nous avons utilisé des fourmis moissonneuses du genre Pogonomyrmex pour effectuer des hibernations artificieHes, des traitements hormonaux, des analyses d'expression de gènes et des mesures de vitellogénine, ce qui nous a permis d'identifier les mécanismes physiologiques régulant les effets maternels sur la détermination de la caste. Enfin, la comparaison d'expression de gènes entre nourrices et fourrageuses suggère un rôle de la vitellogénine dans la régulation du comportement des ouvrières chez les fourmis moissonneuses. En détaillant les influences des gènes et de la physiologie dans la régulation de la division du travail dans les colonies d'insectes sociaux, ce doctorat fournit d'importantes informations permettant de mieux comprendre l'organisation, l'évolution et le succès écologique des sociétés d'insectes.

The Bacterium Frischella perrara Causes Scab Formation in the Gut of its Honeybee Host.

UNLABELLED: Honeybees harbor well-defined bacterial communities in their guts. The major members of these communities appear to benefit the host, but little is known about how they interact with the host and specifically how they interface with the host immune system. In the pylorus, a short region between the midgut and hindgut, honeybees frequently exhibit scab-like structures on the epithelial gut surface. These structures are reminiscent of a melanization response of the insect immune system. Despite the wide distribution of this phenotype in honeybee populations, its cause has remained elusive. Here, we show that the presence of a common member of the bee gut microbiota, the gammaproteobacterium Frischella perrara, correlates with the appearance of the scab phenotype. Bacterial colonization precedes scab formation, and F. perrara specifically localizes to the melanized regions of the host epithelium. Under controlled laboratory conditions, we demonstrate that exposure of microbiota-free bees to F. perrara but not to other bacteria results in scab formation. This shows that F. perrara can become established in a spatially restricted niche in the gut and triggers a morphological change of the epithelial surface, potentially due to a host immune response. As an intermittent colonizer, this bacterium holds promise for addressing questions of community invasion in a simple yet relevant model system. Moreover, our results show that gut symbionts of bees engage in differential host interactions that are likely to affect gut homeostasis. Future studies should focus on how these different gut bacteria impact honeybee health. IMPORTANCE: As pollinators, honeybees are key species for agricultural and natural ecosystems. Their guts harbor simple communities composed of characteristic bacterial species. Because of these features, bees are ideal systems for studying fundamental aspects of gut microbiota-host interactions. However, little is known about how these bacteria interact with their host. Here, we show that a common member of the bee gut microbiota causes the formation of a scab-like structure on the gut epithelium of its host. This phenotype was first described in 1946, but since then it has not been much further characterized, despite being found in bee populations worldwide. The scab phenotype is reminiscent of melanization, a conserved innate immune response of insects. Our results show that high abundance of one member of the bee gut microbiota triggers this specific phenotype, suggesting that the gut microbiota composition can affect the immune status of this key pollinator species.

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Studies aiming at explaining specialization along latitudinal gradients of plant-herbivore interactions have, to date, yielded inconclusive results. Here we propose the use of steep altitudinal gradients for dissecting factors driving evolution of polyphagy in insect herbivores. First, we test whether colonization of high elevation environment favours increased niche-breadth in two disparate insect groups - the wood-boring beetles and the pollinator group of bees - and show increased polyphagy at higher altitudes in both groups. We then assess classic assumptions transferred from the 'latitude-niche-breadth hypothesis', particularly the increase in environmental variability at high, compared to low, altitude. Finally, we discuss alternative mechanisms shaping the observed pattern of increased polyphagy in altitude, including variation in plant quality and predator pressure at different altitudes. We thus suggest evidence for the 'altitude niche-breadth hypothesis', in which both abiotic and biotic conditions, including increased variability and an increase of the potential feeding niche-breadth, promote evolution for increased insect polyphagy in altitude.

Phylogenomics Controlling for Base Compositional Bias Reveals a Single Origin of Eusociality in Corbiculate Bees.

As increasingly large molecular data sets are collected for phylogenomics, the conflicting phylogenetic signal among gene trees poses challenges to resolve some difficult nodes of the Tree of Life. Among these nodes, the phylogenetic position of the honey bees (Apini) within the corbiculate bee group remains controversial, despite its considerable importance for understanding the emergence and maintenance of eusociality. Here, we show that this controversy stems in part from pervasive phylogenetic conflicts among GC-rich gene trees. GC-rich genes typically have a high nucleotidic heterogeneity among species, which can induce topological conflicts among gene trees. When retaining only the most GC-homogeneous genes or using a nonhomogeneous model of sequence evolution, our analyses reveal a monophyletic group of the three lineages with a eusocial lifestyle (honey bees, bumble bees, and stingless bees). These phylogenetic relationships strongly suggest a single origin of eusociality in the corbiculate bees, with no reversal to solitary living in this group. To accurately reconstruct other important evolutionary steps across the Tree of Life, we suggest removing GC-rich and GC-heterogeneous genes from large phylogenomic data sets. Interpreted as a consequence of genome-wide variations in recombination rates, this GC effect can affect all taxa featuring GC-biased gene conversion, which is common in eukaryotes.

Life-history evolution and the polyphenic regulation of somatic maintenance and survival.

Here we discuss life-history evolution from the perspective of adaptive phenotypic plasticity, with a focus on polyphenisms for somatic maintenance and survival. Polyphenisms are adaptive discrete alternative phenotypes that develop in response to changes in the environment. We suggest that dauer larval diapause and its associated adult phenotypes in the nematode (Caenorhabditis elegans), reproductive dormancy in the fruit fly (Drosophila melanogaster) and other insects, and the worker castes of the honey bee (Apis mellifera) are examples of what may be viewed as the polyphenic regulation of somatic maintenance and survival. In these and other cases, the same genotype can--depending upon its environment--express either of two alternative sets of life-history phenotypes that differ markedly with respect to somatic maintenance, survival ability, and thus life span. This plastic modulation of somatic maintenance and survival has traditionally been underappreciated by researchers working on aging and life history. We review the current evidence for such adaptive life-history switches and their molecular regulation and suggest that they are caused by temporally and/or spatially varying, stressful environments that impose diversifying selection, thereby favoring the evolution of plasticity of somatic maintenance and survival under strong regulatory control. By considering somatic maintenance and survivorship from the perspective of adaptive life-history switches, we may gain novel insights into the mechanisms and evolution of aging.

Web decoration of Micrathena sexpinosa (Araneae: Araneidae): a frame-web-choice experiment with stingless bees

The function of silk web decorations in orb weaving spiders has been debated for decades. The most accepted hypothesized functions are that web decorations I) provide camouflage against predators, 2) are an advertisement for vertebrates to avoid web damage, or 3) increase the attraction of prey to the web. Most studies have focused on only a few genera, Argiope being the most common. In this study, I evaluated the prey attraction hypothesis of silk decorations for a species of a poorly studied genus in this topic, Micrathena sexpinosa Hahn 1822. I used a web-choice experiment in which I presented empty or web-bearing frames at the end of a tunnel to stingless bees (Tetragonisca angustula). This frame-choice experiment consisted of the following comparisons: decorated web vs. empty frame, decorated web vs. undecorated web, and undecorated web vs. empty frame. Webs with decoration intercepted significantly more bees than empty frames and undecorated webs. Therefore, the decorations of Micrathena sexpinosa might play a role in increasing foraging success.

Molecular and social regulation of worker division of labour in fire ants.

Reproductive and worker division of labour (DOL) is a hallmark of social insect societies. Despite a long-standing interest in worker DOL, the molecular mechanisms regulating this process have only been investigated in detail in honey bees, and little is known about the regulatory mechanisms operating in other social insects. In the fire ant Solenopsis invicta, one of the most studied ant species, workers are permanently sterile and the tasks performed are modulated by the worker's internal state (age and size) and the outside environment (social environment), which potentially includes the effect of the queen presence through chemical communication via pheromones. However, the molecular mechanisms underpinning these processes are unknown. Using a whole-genome microarray platform, we characterized the molecular basis for worker DOL and we explored how a drastic change in the social environment (i.e. the sudden loss of the queen) affects global gene expression patterns of worker ants. We identified numerous genes differentially expressed between foraging and nonforaging workers in queenright colonies. With a few exceptions, these genes appear to be distinct from those involved in DOL in bees and wasps. Interestingly, after the queen was removed, foraging workers were no longer distinct from nonforaging workers at the transcriptomic level. Furthermore, few expression differences were detected between queenright and queenless workers when we did not consider the task performed. Thus, the social condition of the colony (queenless vs. queenright) appears to impact the molecular pathways underlying worker task performance, providing strong evidence for social regulation of DOL in S. invicta.

Bartonella apis sp. nov., a honey bee gut symbiont of the class Alphaproteobacteria.

Here, we report the culture and characterization of an alphaproteobacterium of the order Rhizobiales, isolated from the gut of the honey bee Apis mellifera. Strain PEB0122T shares >95 % 16S rRNA gene sequence similarity with species of the genus Bartonella, a group of mammalian pathogens transmitted by bloodsucking arthropods. Phylogenetic analyses showed that PEB0122T and related strains from the honey bee gut form a sister clade of the genus Bartonella. Optimal growth of strain PEB0122T was obtained on solid media supplemented with defibrinated sheep blood under microaerophilic conditions at 35-37 °C, which is consistent with the cultural characteristics of other species of the genus Bartonella. Reduced growth of strain PEB0122T also occurred under aerobic conditions. The rod-shaped cells of strain PEB0122T had a mean length of 1.2-1.8 μm and revealed hairy surface structures. Strain PEB0122T was positive for catalase, cytochrome c oxidase, urease and nitrate reductase. The fatty acid composition was comparable to those of other species of the genus Bartonella, with palmitic acid (C16 : 0) and isomers of 18- and 19-carbon chains being the most abundant. The genomic DNA G+C content of PEB0122T was determined to be about 45.5 mol%. The high 16S rRNA gene sequence similarity with species of Bartonella and its close phylogenetic position suggest that strain PEB0122T represents a novel species within the genus Bartonella, for which we propose the name Bartonella apis sp. nov. The type strain is PEB0122T ( = NCIMB 14961T = DSM 29779T).

Cooperation among selfish individuals in insect societies

Kin selection is the key to understanding the evolution of cooperation in insect societies. However, kin selection also predicts potential kin conflict, and understanding how these conflicts are resolved is a major goal of current research on social insects

Sociogenomics of Cooperation and Conflict during Colony Founding in the Fire Ant Solenopsis invicta.

One of the fundamental questions in biology is how cooperative and altruistic behaviors evolved. The majority of studies seeking to identify the genes regulating these behaviors have been performed in systems where behavioral and physiological differences are relatively fixed, such as in the honey bee. During colony founding in the monogyne (one queen per colony) social form of the fire ant Solenopsis invicta, newly-mated queens may start new colonies either individually (haplometrosis) or in groups (pleometrosis). However, only one queen (the "winner") in pleometrotic associations survives and takes the lead of the young colony while the others (the "losers") are executed. Thus, colony founding in fire ants provides an excellent system in which to examine the genes underpinning cooperative behavior and how the social environment shapes the expression of these genes. We developed a new whole genome microarray platform for S. invicta to characterize the gene expression patterns associated with colony founding behavior. First, we compared haplometrotic queens, pleometrotic winners and pleometrotic losers. Second, we manipulated pleometrotic couples in order to switch or maintain the social ranks of the two cofoundresses. Haplometrotic and pleometrotic queens differed in the expression of genes involved in stress response, aging, immunity, reproduction and lipid biosynthesis. Smaller sets of genes were differentially expressed between winners and losers. In the second experiment, switching social rank had a much greater impact on gene expression patterns than the initial/final rank. Expression differences for several candidate genes involved in key biological processes were confirmed using qRT-PCR. Our findings indicate that, in S. invicta, social environment plays a major role in the determination of the patterns of gene expression, while the queen's physiological state is secondary. These results highlight the powerful influence of social environment on regulation of the genomic state, physiology and ultimately, social behavior of animals.

Transitions in social complexity along elevational gradients reveal a combined impact of season length and development time on social evolution.

Eusociality is taxonomically rare, yet associated with great ecological success. Surprisingly, studies of environmental conditions favouring eusociality are often contradictory. Harsh conditions associated with increasing altitude and latitude seem to favour increased sociality in bumblebees and ants, but the reverse pattern is found in halictid bees and polistine wasps. Here, we compare the life histories and distributions of populations of 176 species of Hymenoptera from the Swiss Alps. We show that differences in altitudinal distributions and development times among social forms can explain these contrasting patterns: highly social taxa develop more quickly than intermediate social taxa, and are thus able to complete the reproductive cycle in shorter seasons at higher elevations. This dual impact of altitude and development time on sociality illustrates that ecological constraints can elicit dynamic shifts in behaviour, and helps explain the complex distribution of sociality across ecological gradients.

Evolutionary ecology of learning: insights from fruit flies

Ecologically and evolutionarily oriented research on learning has traditionally been carried out on vertebrates and bees. While less sophisticated than those animals, fruit flies (Drosophila) are capable of several forms of learning, and have an advantage of a short generation time, which makes them an ideal system for experimental evolution studies. This review summarizes the insights into evolutionary questions about learning gained in the last decade from evolutionary experiments on Drosophila. These experiments demonstrate that Drosophila have the genetic potential to evolve substantially improved learning performance in ecologically relevant learning tasks. In at least one set of selected populations the improved learning generalized to another task than that used to impose selection, involving a different behavior, different stimuli, and a different sensory channel for the aversive reinforcement. This improvement in learning ability was associated with reduction in other fitness-related traits, such as larval competitive ability and lifespan, pointing out to evolutionary trade-offs of improved learning. These trade-offs were confirmed by other evolutionary experiments where reduction in learning performance was observed as a correlated response to selection for tolerance to larval nutritional stress or for delayed aging. Such trade-offs could be one reason why fruit flies have not fully used up their evolutionary potential for learning ability. Finally, another evolutionary experiment with Drosophila provided the first direct evidence for the long-standing ideas that learning can under some circumstances accelerate and in other slow down genetically-based evolutionary change. These results demonstrate the usefulness of fruit flies as a model system to address evolutionary questions about learning.

Impact of helpers on colony productivity in a primitively eusocial bee

Small societies of totipotent individuals are good systems in which to study the costs and benefits of group living that are central to the origin and maintenance of eusociality. For instance, in eusocial halictid bees, some females remain in their natal nest to help rear the next brood. Why do helpers stay in the nest? Do they really help, and if yes, is their contribution large enough to voluntarily forfeit direct reproduction? Here, we estimate the impact of helpers on colony survival and productivity in the sweat bee Halictus scabiosae. The number of helpers was positively associated with colony survival and productivity. Colonies from which we experimentally removed one helper produced significantly fewer offspring. However, the effect of helper removal was very small, on average. From the removal experiment, we estimated that one helper increased colony productivity by 0.72 additional offspring in colonies with one to three helpers, while the increase was smaller and not statistically significant in larger colonies. We conclude that helpers do actually help in this primitively eusocial bee, particularly in small colonies. However, the resulting increase in colony productivity is low, which suggests that helpers may be constrained in their role or may attempt to reproduce.

Decoupled post-glacial history in mutualistic plant-insect interactions: insights from the yellow loosestrife (Lysimachia vulgaris) and its associated oil-collecting bees (Macropis europaea and M-fulvipes)

AimWe take a comparative phylogeographical approach to assess whether three species involved in a specialized oil-rewarding pollination system (i.e. Lysimachia vulgaris and two oil-collecting bees within the genus Macropis) show congruent phylogeographical trajectories during post-glacial colonization processes. Our working hypothesis is that within specialized mutualistic interactions, where each species relies on the co-occurrence of the other for survival and/or reproduction, partners are expected to show congruent evolutionary trajectories, because they are likely to have followed parallel migration routes and to have shared glacial refugia. LocationWestern Palaearctic. MethodsOur analysis relies on the extensive sampling of 104 Western Palaearctic populations (totalling 434, 159 and 74 specimens of Lysimachiavulgaris, Macropiseuropaea and Macropisfulvipes, respectively), genotyped with amplified fragment length polymorphism. Based on this, we evaluated the regional genetic diversity (Shannon diversity and allele rarity index) and genetic structure (assessed using structure, population networks, isolation-by-distance and spatial autocorrelation metrics) of each species. Finally, we compared the general phylogeographical patterns obtained. ResultsContrary to our expectations, the analyses revealed phylogeographical signals suggesting that the investigated organisms demonstrate independent post-glacial trajectories as well as distinct contemporaneous demographic parameters, despite their mutualistic interaction. Main conclusionsThe mutualistic partners investigated here are likely to be experiencing distinct and independent evolutionary dynamics because of their contrasting life-history traits (e.g. dispersal abilities), as well as distinct hubs and migration routes. Such conditions would prevent and/or erase any signature of co-structuring of lineages in space and time. As a result, the lack of phylogeographical congruence driven by differences in life-history traits might have arisen irrespective of the three species having shared similar Pleistocene glacial refugia.