Biology subjects

Libbrecht, R.

Publications and source records attributed to Libbrecht, R..

10 recordsLinked to original sources

bioRxiv2024

Queen number shapes worker longevity, fecundity and gene expression in the invasive, highly polygynous ant Tapinoma magnum

In social animals, reproductive activity and ageing patterns are influenced by group composition. A well-documented phenomenon in monogynous (one-queen) insect societies is that queen presence affects worker fecundity and longevity. Little is known about whether and how workers respond to queen number variation in polygynous (multi-queen) species and how their queens age. We created queenless, one-queen, and two-queen colonies of the invasive, polygynous ant Tapinoma magnum to examine worker survival, fecundity, oxidative stress resistance, and fat body gene expression. Additionally, we compared fecundity and brain and fat body transcriptomes of young and old queens. Queenless workers experienced the highest mortality, contrasting with monogynous species where queen removal typically extends lifespan. Workers in single-queen colonies lived longer and were more fertile than in two-queen colonies. Queen number did not directly affect oxidative stress resistance or fat body transcription, though the latter depended on an interaction with worker task. Furthermore, younger nurses demonstrated higher fecundity, oxidative stress resistance and upregulated antioxidant genes compared to older foragers. Absent or minor shifts in fecundity and transcription with queen age, respectively, indicated physiological stability with age. Our research highlights distinct caste- and tissue-specific ageing patterns in this supercolonial species, deviating from typical monogynous ants.

evolutionary biology↗

bioRxiv2024

Queen loss fails to elicit physiological and transcriptional responses in workers of the invasive garden ant Lasius neglectus

Insect colonies with morphologically distinct castes have been called superorganisms because their queens and workers are functionally analogous to the germline and soma in metazoan bodies. In the haplodiploid ants, workers typically lost the sperm storage organ but retained ovaries so they can lay unfertilized eggs. Worker reproduction often occurs after queen loss and is accompanied by a number of physiological changes. However, in some evolutionarily derived ants, workers have become functionally sterile and in many of these species colonies contain multiple queens and can readily raise replacement queens - a syndrome characteristic for invasive ants. We hypothesized that the combination of full worker sterility and regular queen replacement should have eliminated important aspects of the physiological interdependence between queens and workers. We tested this hypothesis by analysing fat body gene expression and worker resistance to oxidative stress in colonies of the invasive ant Lasius neglectus with and without queens. We found age-related transcriptional shifts between young and old queens and young and old workers, suggesting rapid ageing in all castes. However, the removal of any queens in controlled experiments failed to elicit changes in the transcriptional activity and oxidative stress resistance of workers, consistent with our hypothesis. The invasive syndrome of this ant may thus have led to a somatic work force that evolved to be physiologically independent of queen presence.

evolutionary biology↗

bioRxiv2023

The influence of parasite load on transcriptional activity and morphology of a cestode and its ant intermediate host

Parasites with complex life cycles are known to induce phenotypic changes in their intermediate hosts to increase transmission to the final host. The magnitude of these changes could increase with the number of parasites, which would be beneficial to co-infecting parasites. Yet, adverse effects of high parasite load (i.e., many parasites in a single host) might stress both hosts and parasites (e.g., through an increased immune response). We investigated the consequences of parasite load on the transcriptional activity and morphology of the cestode Anomotaenia brevis and its intermediate host, the ant Temnothorax nylanderi. We demonstrated that many differentially expressed host genes shifted with parasite load, and their functions indicate a stronger immune response and fight against oxidative stress in heavily infected hosts. The expression of other host genes responded to infection in an all-or-nothing manner, as did the morphology of the host workers. However, the cestodes became smaller when they competed with other parasites for resources from a single host. Their expression profile further indicated shifts in host immune avoidance, starvation resistance and vesicle-mediated transport. In summary, our study reveals clear consequences of parasite load and highlights specific processes and traits affected by this.

evolutionary biology↗

bioRxiv2023

Task-specific patterns of odorant receptor expression in worker antennae indicates a sensory filter regulating division of labor in ants

Division of labor (DOL) is a characteristic trait of insect societies, where tasks are generally performed by groups of specialized individuals. In social insects, young workers perform duties within the safety of the nest (e.g., brood care), while older ones undertake riskier tasks (e.g., foraging for food). This DOL remains dynamic, and workers may switch back and forth when colony needs require. Theoretical models propose that workers differ in their thresholds to take on certain tasks when confronted to task-related stimuli, resulting in variation in their response to such stimuli, task-specialization, and thus DOL. Such models assume that workers differ in how they respond to task-related information rather than in how they perceive such information. Here, we test the hypothesis that DOL rather stems from workers differing in their efficiency to detect task-related stimuli. We used transcriptomics to compare gene expression in the antennae and in the brain between nurses and foragers in the ant Temnothorax longispinosus. We found that seven times as many genes were differentially expressed between the behavioral phenotypes in the antennae compared to the brain. Moreover, nearly half of all odorant receptors genes were differentially expressed, with an overrepresentation of the 9-exon gene subfamily upregulated in the antennae of nurses. These findings suggest that nurses and foragers differ in how they perceive their olfactory environment, and task-related signals. The results of this study support the hypothesis that a sensory filter in the antennaepredisposes workers to specialize in specific tasks, and may improve our understanding of DOL in insect societies.

evolutionary biology↗

bioRxiv2022

Ontogeny of superorganisms:Social control of queen specialization in ants

A central question in life sciences is to understand the ontogeny of biological systems, which exist at multiple phenotypic scales and function via the cooperation of specialized entities. Examples of such systems include multicellular organisms, which consist of specialized cells, and insect societies (or superorganisms), which are composed of specialized individuals. Both systems are products of major evolutionary transitions, and they share commonalities in their ontogeny, as both develop from a single, pluripotent unit. While the ontogeny of multicellular organisms is well understood, the factors and mechanisms that control the ontogeny of superorganisms remain poorly studied. Here, we report experimental investigations of the process of colony foundation in ants. In most ant species, a new colony is established by a solitary founding queen that expresses behavioral pluripotency to produce the first workers, at which point the queen becomes strictly specialized in egg production. We demonstrate that the presence of workers is necessary and sufficient to induce this specialization of queens. Moreover, workers also maintain the queen specialization in mature colonies, as established queens isolated from their workers revert to expressing behavioral pluripotency. Our results also suggest that this underappreciated social control of queen specialization may be common in ants and regulated by ancestral mechanisms. These findings stand in contrast to the traditional view of social insect queens as being intrinsically specialized in egg production and may reshape our understanding of division of labor in insect societies. Significance statementInsect societies are characterized by division of labor between queens that specialize in producing eggs and workers that perform all non-reproductive tasks. Studies of division of labor traditionally focused on fully established colonies and there is limited information on the factors and mechanisms that initiate division of labor during colony foundation. Here, we report that the presence of workers not only initiates the queen specialization, but also maintains it continually throughout the colony life. Finding such a social control of the specialization of queens contradicts the commonly accepted view of social insect queens as intrinsically specialized egg-laying machines. Our study has the potential to reshape our understanding of the functioning and evolution of insect societies.

evolutionary biology↗

bioRxiv2021

Identification of functional residues using machine learning provides insights into the evolution of odorant receptor gene families in solitary and social insects

The gene family of insect odorant receptors (ORs) has greatly expanded in the course of evolution. ORs allow insects to detect volatile chemicals and therefore play an important role in social interactions, the detection of enemies and preys, and during foraging. The sequences of several thousand ORs are known, but their specific function or ligands have been identified only for very few of them. To advance the functional characterization of ORs, we compiled, curated and aligned the sequences of 3,902 ORs from 21 insect species. We identified the amino acid positions that best predict the response to ligands using machine learning on sets of functionally characterized proteins from the fly Drosophila melanogaster, the mosquito Anopheles gambiae and the ant Harpegnathos saltator. We studied the conservation of these predicted relevant residues across all OR subfamilies and show that the subfamilies that expanded strongly in social insects exhibit high levels of conservation in their binding sites. This indicates that ORs of social insect families are typically finely tuned and exhibit a sensitivity to very similar odorants. Our novel approach provides a powerful tool to use functional information from a limited number of genes to investigate the functional evolution of large gene families.

bioinformatics↗

bioRxiv2021

Experimental increase of worker diversity benefits brood production in ants

The reproductive division of labor of eusocial insects, whereby one or several queens monopolize reproduction, evolved in a context of high genetic relatedness. However, many extant eusocial species have developed strategies that decrease genetic relatedness in their colonies, suggesting some benefits of the increased diversity. Multiple studies support this hypothesis by showing positive correlations between genetic diversity and colony fitness, as well as finding effects of experimental manipulations of diversity on colony performance. However, alternative explanations could account for most of these reports, and the benefits of diversity on fitness in eusocial insects still await validation. In this study, we experimentally increased worker diversity in the ant Lasius niger while controlling for typical confounding factors. We found that experimental colonies composed of workers coming from three different source colonies produced more larvae and showed more variation in size compared to groups of workers coming from a single colony. We propose that the benefits of increased diversity stemmed from an improved division of labor. Our study confirms that worker diversity enhances colony performance, thus providing a possible explanation for the evolution of multiply mated queens and multiple-queen colonies in many species of eusocial insects.

evolutionary biology↗

bioRxiv2020

Fecundity determines the outcome of 10 founding queen associations in ants

Animal cooperation evolved because of its benefits to the cooperators. Pleometrosis in ants - the cooperation of queens to found a colony - benefits colony growth, but also incurs costs for some of the cooperators because only one queen usually survives the association. While several traits are associated with queen survival, they tend to be confounded and it is unclear which factor specifically determines the outcome of pleometrosis. In this study, we used the ant Lasius niger to monitor offspring production in colonies founded by one or two queens. Then, we experimentally paired queens that differed in fecundity but not in size, and vice versa, to disentangle the effect of these factors on queen survival. Finally, we investigated how fecundity and size differed between queens depending on whether they were chosen as pleometrotic partners. Our results indicate that pleometrosis increased and accelerated worker production via a nutritional boost to the larvae. The most fecund queens more frequently survived the associations, even when controlling for size and worker parentage, and queens selected as pleometrotic partners were less fecund. Our results are consistent with fecundity being central to the onset and outcome of pleometrosis, a typical case of cooperation among unrelated animals.

evolutionary biology↗

bioRxiv2018

Gene expression is stronger associated with behaviour than with age and fertility in ant workers

The ecological success of social insects is based on division of labour, not only between queens and workers, but also among workers. Whether a worker tends the brood or forages is strongly influenced by age, fertility and nutritional status, with brood carers being younger, more fecund and corpulent. Here, we experimentally disentangle behaviour from age and fertility in Temnothorax longispinosus ant workers and analyse how these parameters are linked to whole-body gene expression. Our transcriptome analysis reveals four times more genes associated with behaviour than with age and only few fertility-associated genes. Brood carers exhibited an upregulation of genes involved in lipid biosynthesis, whereas foragers invested in metabolism. Additional simulations revealed that the experimental disassociation of co-varying factors reduces transcriptomic noise, potentially explaining discrepancies between transcriptomic studies on worker behaviour in other social insects. Our study highlights the influence of nutritional status on task choice in ant workers.

evolutionary biology↗

bioRxiv2017

Time course analysis of the brain transcriptome during transitions between brood care and reproduction in the clonal raider ant

Division of labor between reproductive queens and non-reproductive workers that perform brood care is the hallmark of insect societies. However, the molecular basis of this fundamental dichotomy remains poorly understood, in part because the caste of an individual cannot typically be experimentally manipulated at the adult stage. Here we take advantage of the unique biology of the clonal raider ant, Ooceraea biroi, where reproduction and brood care behavior can be experimentally manipulated in adults. To study the molecular regulation of reproduction and brood care, we induced transitions between both states, and monitored brain gene expression at multiple time points. We found that introducing larvae that inhibit reproduction and induce brood care behavior caused much faster changes in adult gene expression than removing larvae. The delayed response to the removal of the larval signal prevents untimely activation of reproduction in O. biroi colonies. This resistance to change when removing a signal also prevents premature modifications in many other biological processes. Furthermore, we found that the general patterns of gene expression differ depending on whether ants transition from reproduction to brood care or vice versa, indicating that gene expression changes between phases are cyclic rather than pendular. Our analyses also identify genes with large and early expression changes in one or both transitions. These genes likely play upstream roles in regulating reproduction and behavior, and thus constitute strong candidates for future molecular studies of the evolution and regulation of reproductive division of labor in insect societies.

evolutionary biology↗