Tom Wenseleers | KU Leuven (original) (raw)

Papers by Tom Wenseleers

Research paper thumbnail of An Introduction to Animal Behavior: An Integrative Approach . By Michael J. Ryan and Walter Wilczynski . Cold Spring Harbor (New York): Cold Spring Harbor Laboratory Press. <span class="katex"><span class="katex-mathml"><math xmlns="http://www.w3.org/1998/Math/MathML"><semantics><mrow><mn>79.00</mn><mo stretchy="false">(</mo><mi>h</mi><mi>a</mi><mi>r</mi><mi>d</mi><mi>c</mi><mi>o</mi><mi>v</mi><mi>e</mi><mi>r</mi><mo stretchy="false">)</mo><mo separator="true">;</mo></mrow><annotation encoding="application/x-tex">79.00 (hardcover); </annotation></semantics></math></span><span class="katex-html" aria-hidden="true"><span class="base"><span class="strut" style="height:1em;vertical-align:-0.25em;"></span><span class="mord">79.00</span><span class="mopen">(</span><span class="mord mathnormal">ha</span><span class="mord mathnormal" style="margin-right:0.02778em;">r</span><span class="mord mathnormal">d</span><span class="mord mathnormal">co</span><span class="mord mathnormal" style="margin-right:0.03588em;">v</span><span class="mord mathnormal" style="margin-right:0.02778em;">er</span><span class="mclose">)</span><span class="mpunct">;</span></span></span></span>45.00 (paper). xi + 258 p.; ill.; index. ISBN: 978-1-936113-18-7 (hc); 978-0-879698-58-4 (pb). 2011

The Quarterly Review of Biology, 2012

Research paper thumbnail of The origin and evolution of queen and fertility signals in Corbiculate bees

BMC Evolutionary Biology, 2015

In social Hymenoptera (ants, bees and wasps), various chemical compounds present on the cuticle h... more In social Hymenoptera (ants, bees and wasps), various chemical compounds present on the cuticle have been shown to act as fertility signals. In addition, specific queen-characteristic hydrocarbons have been implicated as sterility-inducing queen signals in ants, wasps and bumblebees. In Corbiculate bees, however, the chemical nature of queen-characteristic and fertility-linked compounds appears to be more diverse than in ants and wasps. Moreover, it remains unknown how queen signals evolved across this group and how they might have been co-opted from fertility signals in solitary ancestors. Here, we perform a phylogenetic analysis of fertility-linked compounds across 16 species of solitary and eusocial bee species, comprising both literature data as well as new primary data from a key solitary outgroup species, the oil-collecting bee Centris analis, and the highly eusocial stingless bee Scaptotrigona depilis. Our results demonstrate the presence of fertility-linked compounds belonging to 12 different chemical classes. In addition, we find that some classes of compounds (linear and branched alkanes, alkenes, esters and fatty acids) were already present as fertility-linked signals in the solitary ancestors of Corbiculate bees, while others appear to be specific to certain species. Overall, our results suggest that queen signals in Corbiculate bees are likely derived from ancestral fertility-linked compounds present in solitary bees that lacked reproductive castes. These original fertility-linked cues or signals could have been produced either as a by-product of ovarian activation or could have served other communicative purposes, such as in mate recognition or the regulation of egg-laying.

Research paper thumbnail of The origin and evolution of social insect queen pheromones: Novel hypotheses and outstanding problems

BioEssays : news and reviews in molecular, cellular and developmental biology, Jan 27, 2015

Queen pheromones, which signal the presence of a fertile queen and induce daughter workers to rem... more Queen pheromones, which signal the presence of a fertile queen and induce daughter workers to remain sterile, are considered to play a key role in regulating the reproductive division of labor of insect societies. Although queen pheromones were long thought to be highly taxon-specific, recent studies have shown that structurally related long-chain hydrocarbons act as conserved queen signals across several independently evolved lineages of social insects. These results imply that social insect queen pheromones are very ancient and likely derived from an ancestral signalling system that was already present in their common solitary ancestors. Based on these new insights, we here review the literature and speculate on what signal precursors social insect queen pheromones may have evolved from. Furthermore, we provide compelling evidence that these pheromones should best be seen as honest signals of fertility as opposed to suppressive agents that chemically sterilize the workers against ...

Research paper thumbnail of Dual Effect of Wasp Queen Pheromone in Regulating Insect Sociality

Research paper thumbnail of Variability in growth/no growth boundaries of 188 different Escherichia coli strains reveals that approximately 75 % have a higher growth probability under low pH conditions than E. coli O157:H7 strain ATCC 43888

Food microbiology, 2015

This study investigated the variation in growth/no growth boundaries of 188 Escherichia coli stra... more This study investigated the variation in growth/no growth boundaries of 188 Escherichia coli strains. Experiments were conducted in Luria-Bertani media under 36 combinations of lactic acid (LA) (0 and 25 mM), pH (3.8, 3.9, 4.0, 4.1, 4.2 and 4.3 for 0 mM LA and 4.3, 4.4, 4.5, 4.6, 4.7 and 4.8 for 25 mM LA) and temperature (20, 25 and 30 °C). After 3 days of incubation, growth was monitored through optical density measurements. For each strain, a so-called purposeful selection approach was used to fit a logistic regression model that adequately predicted the likelihood for growth. Further, to assess the growth/no growth variability for all the strains at once, a generalized linear mixed model was fitted to the data. Strain was fitted as a fixed factor and replicate as a random blocking factor. E. coli O157:H7 strain ATCC 43888 was used as reference strain allowing a comparison with the other strains. Out of the 188 strains tested, 140 strains (∼75%) presented a significantly higher pr...

Research paper thumbnail of Fitness trade-offs explain low levels of persister cells in the opportunistic pathogen Pseudomonas aeruginosa

Molecular Ecology, 2015

Microbial populations often contain a fraction of slow-growing persister cells that withstand ant... more Microbial populations often contain a fraction of slow-growing persister cells that withstand antibiotics and other stress factors. Current theoretical models predict that persistence levels should reflect a stable state in which the survival advantage of persisters under adverse conditions is balanced with the direct growth cost impaired under favourable growth conditions, caused by the nonreplication of persister cells. Based on this direct growth cost alone, however, it remains challenging to explain the observed low levels of persistence (&amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;lt;1%) seen in the populations of many species. Here, we present data from the opportunistic human pathogen Pseudomonas aeruginosa that can explain this discrepancy by revealing various previously unknown costs of persistence. In particular, we show that in the absence of antibiotic stress, increased persistence is traded off against a lengthened lag phase as well as a reduced survival ability during stationary phase. We argue that these pleiotropic costs contribute to the very low proportions of persister cells observed among natural P. aeruginosa isolates (3 × 10(-8) -3 × 10(-4) ) and that they can explain why strains with higher proportions of persister cells lose out very quickly in competition assays under favourable growth conditions, despite a negligible difference in maximal growth rate. We discuss how incorporating these trade-offs could lead to models that can better explain the evolution of persistence in nature and facilitate the rational design of alternative therapeutic strategies for treating infectious diseases.

Research paper thumbnail of Fitness trade-offs explain low levels of persister cells in the opportunistic pathogen Pseudomonas aeruginosa

Molecular Ecology

Microbial populations often contain a fraction of slow-growing persister cells that withstand ant... more Microbial populations often contain a fraction of slow-growing persister cells that withstand antibiotics and other stress factors. Current theoretical models predict that persistence levels should reflect a stable state in which the survival advantage of persisters under adverse conditions is balanced with the direct growth cost impaired under favorable growth conditions, caused by the non-replication of persister cells. Based on this direct growth cost alone, however, it remains challenging to explain the observed low levels of persistence (<1%) seen in the populations of many species. Here, we present data from the opportunistic human pathogen Pseudomonas aeruginosa that can explain this discrepancy by revealing various previously unknown costs of persistence. In particular, we show that in the absence of antibiotic stress, increased persistence is traded off against a lengthened lag phase as well as a reduced survival ability during stationary phase. We argue that these pleio...

Research paper thumbnail of Frequency of antibiotic application drives rapid evolutionary adaptation of Escherichia coli persistence

Nature Microbiology, 2016

Research paper thumbnail of Worker honeybee sterility: a proteomic analysis of suppressed ovary activation

Insect Biochemistry and Molecular Biology, 2012

Eusocial behavior is extensively studied in the honeybee, Apis mellifera, as it displays an extre... more Eusocial behavior is extensively studied in the honeybee, Apis mellifera, as it displays an extreme form of altruism. Honeybee workers are generally obligatory sterile in a bee colony headed by a queen, but the inhibition of ovary activation is lifted upon the absence of queen and larvae. Worker bees are then able to develop mature, viable eggs. The detailed repressive physiological mechanisms that are responsible for this remarkable phenomenon are as of yet largely unknown. Physiological studies today mainly focus on the transcriptome, while the proteome stays rather unexplored. Here, we present a quantitative 2-dimensional differential gel electrophoresis comparison between activated and inactivated worker ovaries and brains of reproductive and sterile worker bees, including a spot map of ovaries, containing 197 identified spots. Our findings suggest that suppression of ovary activation might involve a constant interplay between primordial oogenesis and subsequent degradation, which is probably mediated through steroid and neuropeptide hormone signaling. Additionally, the observation of higher viral protein loads in both the brains and ovaries of sterile workers is particularly noteworthy. This data set will be of great value for future research unraveling the physiological mechanisms underlying the altruistic sterility in honeybee workers.

Research paper thumbnail of Evolution of Self-Organized Task Specialization in Robot Swarms

PLOS Computational Biology, 2015

Division of labor is ubiquitous in biological systems, as evidenced by various forms of complex t... more Division of labor is ubiquitous in biological systems, as evidenced by various forms of complex task specialization observed in both animal societies and multicellular organisms. Although clearly adaptive, the way in which division of labor first evolved remains enigmatic, as it requires the simultaneous co-occurrence of several complex traits to achieve the required degree of coordination. Recently, evolutionary swarm robotics has emerged as an excellent test bed to study the evolution of coordinated group-level behavior. Here we use this framework for the first time to study the evolutionary origin of behavioral task specialization among groups of identical robots. The scenario we study involves an advanced form of division of labor, common in insect societies and known as "task partitioning", whereby two sets of tasks have to be carried out in sequence by different individuals. Our results show that task partitioning is favored whenever the environment has features that, when exploited, reduce switching costs and increase the net efficiency of the group, and that an optimal mix of task specialists is achieved most readily when the behavioral repertoires aimed at carrying out the different subtasks are available as pre-adapted building blocks. Nevertheless, we also show for the first time that self-organized task specialization could be evolved entirely from scratch, starting only from basic, low-level behavioral primitives, using a nature-inspired evolutionary method known as Grammatical Evolution. Remarkably, division of labor was achieved merely by selecting on overall group performance, and without providing any prior information on how the global object retrieval task was best divided into smaller subtasks. We discuss the potential of our method for engineering adaptively behaving robot swarms and interpret our results in relation to the likely path that nature took to evolve complex sociality and task specialization.

Research paper thumbnail of Differential diagnosis of the honey bee trypanosomatids Crithidia mellificae and Lotmaria passim

Journal of Invertebrate Pathology, 2015

Trypanosomatids infecting honey bees have been poorly studied with molecular methods until recent... more Trypanosomatids infecting honey bees have been poorly studied with molecular methods until recently. After the description of Crithidia mellificae (Langridge and McGhee, 1967) it took about forty years until molecular data for honey bee trypanosomatids became available and were used to identify and describe a new trypanosomatid species from honey bees, Lotmaria passim (Evans and Schwarz, 2014). However, an easy method to distinguish them without sequencing is not yet available. Research on the related bumble bee parasites Crithidia bombi and Crithidia expoeki revealed a fragment length polymorphism in the internal transcribed spacer 1 (ITS1), which enabled species discrimination. In search of fragment length polymorphisms for differential diagnostics in honey bee trypanosomatids, we studied honey bee trypanosomatid cell cultures of C. mellificae and L. passim. This research resulted in the identification of fragment length polymorphisms in ITS1 and ITS1-2 markers, which enabled us to develop a diagnostic method to differentiate both honey bee trypanosomatid species without the need for sequencing. However, the amplification success of the ITS1 marker depends probably on the trypanosomatid infection level. Further investigation confirmed that L. passim is the dominant species in Belgium, Japan and Switzerland. We found C. mellificae only rarely in Belgian honey bee samples, but not in honey bee samples from other countries. C. mellificae was also detected in mason bees (Osmia bicornis and Osmia cornuta) besides in honey bees. Further, the characterization and comparison of additional markers from L. passim strain SF (published as C. mellificae strain SF) and a Belgian honey bee sample revealed very low divergence in the 18S rRNA, ITS1-2, 28S rRNA and cytochrome b sequences. Nevertheless, a variable stretch was observed in the gp63 virulence factor.

Research paper thumbnail of No Evidence of Enemy Release in Pathogen and Microbial Communities of Common Wasps (Vespula vulgaris) in Their Native and Introduced Range

PloS one, 2015

When invasive species move to new environments they typically experience population bottlenecks t... more When invasive species move to new environments they typically experience population bottlenecks that limit the probability that pathogens and parasites are also moved. The invasive species may thus be released from biotic interactions that can be a major source of density-dependent mortality, referred to as enemy release. We examined for evidence of enemy release in populations of the common wasp (Vespula vulgaris), which attains high densities and represents a major threat to biodiversity in its invaded range. Mass spectrometry proteomic methods were used to compare the microbial communities in wasp populations in the native (Belgium and England) and invaded range (Argentina and New Zealand). We found no evidence of enemy release, as the number of microbial taxa was similar in both the introduced and native range. However, some evidence of distinctiveness in the microbial communities was observed between countries. The pathogens observed were similar to a variety of taxa observed i...

Research paper thumbnail of Genome sequence heterogeneity of Lake Sinai Virus found in honey bees and Orf1/RdRP-based polymorphisms in a single host

Virus research, Jan 25, 2015

Honey bees (Apis mellifera) are susceptible to a wide range of pathogens, including a broad set o... more Honey bees (Apis mellifera) are susceptible to a wide range of pathogens, including a broad set of viruses. Recently, next-generation sequencing has expanded the list of viruses with, for instance, two strains of Lake Sinai Virus. Soon after its discovery in the USA, LSV was also discovered in other countries and in other hosts. In the present study, we assemble four almost complete LSV genomes, and show that there is remarkable sequence heterogeneity based on the Orf1, RNA-dependent RNA polymerase and capsid protein sequences in comparison to the previously identified LSV 1 and 2 strains. Phylogenetic analyses of LSV sequences obtained from single honey bee specimens further revealed that up to three distinctive clades could be present in a single bee. Such superinfections have not previously been identified for other honey bee viruses. In a search for the putative routes of LSV transmission, we were able to demonstrate the presence of LSV in pollen pellets and in Varroa destructor...

Research paper thumbnail of Self-organized flocking with conflicting goal directions

Proceedings of the European Conference on Complex Systems 2012, 2013

In flocking, a large number of individuals move cohesively in a common direction. Many examples c... more In flocking, a large number of individuals move cohesively in a common direction. Many examples can be found in nature: from simple organisms such as crickets and locusts to more complex ones such as birds, fish and quadrupeds.

Research paper thumbnail of GESwarm

Proceeding of the fifteenth annual conference on Genetic and evolutionary computation conference - GECCO '13, 2013

In this paper we propose GESwarm, a novel tool that can automatically synthesize collective behav... more In this paper we propose GESwarm, a novel tool that can automatically synthesize collective behaviors for swarms of autonomous robots through evolutionary robotics. Evolutionary robotics typically relies on artificial evolution for tuning the weights of an artificial neural network that is then used as individual behavior representation. The main caveat of neural networks is that they are very difficult to reverse engineer, meaning that once a suitable solution is found, it is very difficult to analyze, to modify, and to tease apart the inherent principles that lead to the desired collective behavior. In contrast, our representation is based on completely readable and analyzable individual-level rules that lead to a desired collective behavior.

Research paper thumbnail of The Fungal Aroma Gene ATF1 Promotes Dispersal of Yeast Cells through Insect Vectors

Cell Reports, 2014

Highlights The S. cerevisiae ATF1 gene controls the production of volatile acetate esters Aroma o... more Highlights The S. cerevisiae ATF1 gene controls the production of volatile acetate esters Aroma of ATF1 mutants elicits different neuronal activity in the fly antennal lobe Flies are significantly more attracted to wild-type yeast than to atf1-null mutants Addition of isoamyl acetate and ethyl acetate restores attraction of Drosophila SUMMARY Yeast cells produce various volatile metabolites that are key contributors to the pleasing fruity and flowery aroma of fermented beverages. Several of these fruity metabolites, including isoamyl acetate and ethyl acetate, are produced by a dedicated enzyme, the alcohol acetyl transferase Atf1. However, despite much research, the physiological role of acetate ester formation in yeast remains unknown. Using a combination of molecular biology, neurobiology, and behavioral tests, we demonstrate that deletion of ATF1 alters the olfactory response in the antennal lobe of fruit flies that feed on yeast cells. The flies are much less attracted to the mutant yeast cells, and this in turn results in reduced dispersal of the mutant yeast cells by the flies. Together, our results uncover the molecular details of an intriguing aroma-based communication and mutualism between microbes and their insect vectors. Similar mechanisms may exist in other microbes, including microbes on flowering plants and pathogens.

Research paper thumbnail of Widespread occurrence of honey bee pathogens in solitary bees

Journal of Invertebrate Pathology, 2014

Solitary bees and honey bees from a neighbouring apiary were screened for a broad set of putative... more Solitary bees and honey bees from a neighbouring apiary were screened for a broad set of putative pathogens including protists, fungi, spiroplasmas and viruses. Most sampled bees appeared to be infected with multiple parasites. Interestingly, viruses exclusively known from honey bees such as Apis mellifera Filamentous Virus and Varroa destructor Macula-like Virus were also discovered in solitary bees. A microsporidium found in Andrena vaga showed most resemblance to Nosema thomsoni. Our results suggest that bee hives represent a putative source of pathogens for other pollinators. Similarly, solitary bees may act as a reservoir of honey bee pathogens.

Research paper thumbnail of Towards greater realism in inclusive fitness models: the case of worker reproduction in insect societies

Biology letters, 2013

The conflicts over sex allocation and male production in insect societies have long served as an ... more The conflicts over sex allocation and male production in insect societies have long served as an important test bed for Hamilton's theory of inclusive fitness, but have for the most part been considered separately. Here, we develop new coevolutionary models to examine the interaction between these two conflicts and demonstrate that sex ratio and colony productivity costs of worker reproduction can lead to vastly different outcomes even in species that show no variation in their relatedness structure. Empirical data on worker-produced males in eight species of Melipona bees support the predictions from a model that takes into account the demographic details of colony growth and reproduction. Overall, these models contribute significantly to explaining behavioural variation that previous theories could not account for.

Research paper thumbnail of Evolutionary synthesis of multi-agent systems for dynamic dial-a-ride problems

Proceedings of the fourteenth international conference on Genetic and evolutionary computation conference companion - GECCO Companion '12, 2012

In dynamic dial-a-ride problems a fleet of vehicles need to handle transportation requests within... more In dynamic dial-a-ride problems a fleet of vehicles need to handle transportation requests within time. We research how to create a decentralized multi-agent system that can solve the dynamic dial-a-ride problem. Normally multi-agent systems are hand designed for each specific application. In this paper we research the applicability of genetic programming to automatically program a multi-agent system that solves dial-a-ride problems. We evaluated the evolved system by running a number of simulations and compared it's performance to a selection hyper-heuristic. The results shows that genetic programming can be a viable alternative to hand constructing multi-agent systems.

Research paper thumbnail of Bourgeois Behavior and Freeloading in the Colonial Orb Web Spider Parawixia bistriata (Araneae, Araneidae)

The American Naturalist, 2013

Online enhancement: appendix. Dryad data: http://dx.doi.org/10.5061/dryad.1205d.

Research paper thumbnail of An Introduction to Animal Behavior: An Integrative Approach . By Michael J. Ryan and Walter Wilczynski . Cold Spring Harbor (New York): Cold Spring Harbor Laboratory Press. <span class="katex"><span class="katex-mathml"><math xmlns="http://www.w3.org/1998/Math/MathML"><semantics><mrow><mn>79.00</mn><mo stretchy="false">(</mo><mi>h</mi><mi>a</mi><mi>r</mi><mi>d</mi><mi>c</mi><mi>o</mi><mi>v</mi><mi>e</mi><mi>r</mi><mo stretchy="false">)</mo><mo separator="true">;</mo></mrow><annotation encoding="application/x-tex">79.00 (hardcover); </annotation></semantics></math></span><span class="katex-html" aria-hidden="true"><span class="base"><span class="strut" style="height:1em;vertical-align:-0.25em;"></span><span class="mord">79.00</span><span class="mopen">(</span><span class="mord mathnormal">ha</span><span class="mord mathnormal" style="margin-right:0.02778em;">r</span><span class="mord mathnormal">d</span><span class="mord mathnormal">co</span><span class="mord mathnormal" style="margin-right:0.03588em;">v</span><span class="mord mathnormal" style="margin-right:0.02778em;">er</span><span class="mclose">)</span><span class="mpunct">;</span></span></span></span>45.00 (paper). xi + 258 p.; ill.; index. ISBN: 978-1-936113-18-7 (hc); 978-0-879698-58-4 (pb). 2011

The Quarterly Review of Biology, 2012

Research paper thumbnail of The origin and evolution of queen and fertility signals in Corbiculate bees

BMC Evolutionary Biology, 2015

In social Hymenoptera (ants, bees and wasps), various chemical compounds present on the cuticle h... more In social Hymenoptera (ants, bees and wasps), various chemical compounds present on the cuticle have been shown to act as fertility signals. In addition, specific queen-characteristic hydrocarbons have been implicated as sterility-inducing queen signals in ants, wasps and bumblebees. In Corbiculate bees, however, the chemical nature of queen-characteristic and fertility-linked compounds appears to be more diverse than in ants and wasps. Moreover, it remains unknown how queen signals evolved across this group and how they might have been co-opted from fertility signals in solitary ancestors. Here, we perform a phylogenetic analysis of fertility-linked compounds across 16 species of solitary and eusocial bee species, comprising both literature data as well as new primary data from a key solitary outgroup species, the oil-collecting bee Centris analis, and the highly eusocial stingless bee Scaptotrigona depilis. Our results demonstrate the presence of fertility-linked compounds belonging to 12 different chemical classes. In addition, we find that some classes of compounds (linear and branched alkanes, alkenes, esters and fatty acids) were already present as fertility-linked signals in the solitary ancestors of Corbiculate bees, while others appear to be specific to certain species. Overall, our results suggest that queen signals in Corbiculate bees are likely derived from ancestral fertility-linked compounds present in solitary bees that lacked reproductive castes. These original fertility-linked cues or signals could have been produced either as a by-product of ovarian activation or could have served other communicative purposes, such as in mate recognition or the regulation of egg-laying.

Research paper thumbnail of The origin and evolution of social insect queen pheromones: Novel hypotheses and outstanding problems

BioEssays : news and reviews in molecular, cellular and developmental biology, Jan 27, 2015

Queen pheromones, which signal the presence of a fertile queen and induce daughter workers to rem... more Queen pheromones, which signal the presence of a fertile queen and induce daughter workers to remain sterile, are considered to play a key role in regulating the reproductive division of labor of insect societies. Although queen pheromones were long thought to be highly taxon-specific, recent studies have shown that structurally related long-chain hydrocarbons act as conserved queen signals across several independently evolved lineages of social insects. These results imply that social insect queen pheromones are very ancient and likely derived from an ancestral signalling system that was already present in their common solitary ancestors. Based on these new insights, we here review the literature and speculate on what signal precursors social insect queen pheromones may have evolved from. Furthermore, we provide compelling evidence that these pheromones should best be seen as honest signals of fertility as opposed to suppressive agents that chemically sterilize the workers against ...

Research paper thumbnail of Dual Effect of Wasp Queen Pheromone in Regulating Insect Sociality

Research paper thumbnail of Variability in growth/no growth boundaries of 188 different Escherichia coli strains reveals that approximately 75 % have a higher growth probability under low pH conditions than E. coli O157:H7 strain ATCC 43888

Food microbiology, 2015

This study investigated the variation in growth/no growth boundaries of 188 Escherichia coli stra... more This study investigated the variation in growth/no growth boundaries of 188 Escherichia coli strains. Experiments were conducted in Luria-Bertani media under 36 combinations of lactic acid (LA) (0 and 25 mM), pH (3.8, 3.9, 4.0, 4.1, 4.2 and 4.3 for 0 mM LA and 4.3, 4.4, 4.5, 4.6, 4.7 and 4.8 for 25 mM LA) and temperature (20, 25 and 30 °C). After 3 days of incubation, growth was monitored through optical density measurements. For each strain, a so-called purposeful selection approach was used to fit a logistic regression model that adequately predicted the likelihood for growth. Further, to assess the growth/no growth variability for all the strains at once, a generalized linear mixed model was fitted to the data. Strain was fitted as a fixed factor and replicate as a random blocking factor. E. coli O157:H7 strain ATCC 43888 was used as reference strain allowing a comparison with the other strains. Out of the 188 strains tested, 140 strains (∼75%) presented a significantly higher pr...

Research paper thumbnail of Fitness trade-offs explain low levels of persister cells in the opportunistic pathogen Pseudomonas aeruginosa

Molecular Ecology, 2015

Microbial populations often contain a fraction of slow-growing persister cells that withstand ant... more Microbial populations often contain a fraction of slow-growing persister cells that withstand antibiotics and other stress factors. Current theoretical models predict that persistence levels should reflect a stable state in which the survival advantage of persisters under adverse conditions is balanced with the direct growth cost impaired under favourable growth conditions, caused by the nonreplication of persister cells. Based on this direct growth cost alone, however, it remains challenging to explain the observed low levels of persistence (&amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;lt;1%) seen in the populations of many species. Here, we present data from the opportunistic human pathogen Pseudomonas aeruginosa that can explain this discrepancy by revealing various previously unknown costs of persistence. In particular, we show that in the absence of antibiotic stress, increased persistence is traded off against a lengthened lag phase as well as a reduced survival ability during stationary phase. We argue that these pleiotropic costs contribute to the very low proportions of persister cells observed among natural P. aeruginosa isolates (3 × 10(-8) -3 × 10(-4) ) and that they can explain why strains with higher proportions of persister cells lose out very quickly in competition assays under favourable growth conditions, despite a negligible difference in maximal growth rate. We discuss how incorporating these trade-offs could lead to models that can better explain the evolution of persistence in nature and facilitate the rational design of alternative therapeutic strategies for treating infectious diseases.

Research paper thumbnail of Fitness trade-offs explain low levels of persister cells in the opportunistic pathogen Pseudomonas aeruginosa

Molecular Ecology

Microbial populations often contain a fraction of slow-growing persister cells that withstand ant... more Microbial populations often contain a fraction of slow-growing persister cells that withstand antibiotics and other stress factors. Current theoretical models predict that persistence levels should reflect a stable state in which the survival advantage of persisters under adverse conditions is balanced with the direct growth cost impaired under favorable growth conditions, caused by the non-replication of persister cells. Based on this direct growth cost alone, however, it remains challenging to explain the observed low levels of persistence (<1%) seen in the populations of many species. Here, we present data from the opportunistic human pathogen Pseudomonas aeruginosa that can explain this discrepancy by revealing various previously unknown costs of persistence. In particular, we show that in the absence of antibiotic stress, increased persistence is traded off against a lengthened lag phase as well as a reduced survival ability during stationary phase. We argue that these pleio...

Research paper thumbnail of Frequency of antibiotic application drives rapid evolutionary adaptation of Escherichia coli persistence

Nature Microbiology, 2016

Research paper thumbnail of Worker honeybee sterility: a proteomic analysis of suppressed ovary activation

Insect Biochemistry and Molecular Biology, 2012

Eusocial behavior is extensively studied in the honeybee, Apis mellifera, as it displays an extre... more Eusocial behavior is extensively studied in the honeybee, Apis mellifera, as it displays an extreme form of altruism. Honeybee workers are generally obligatory sterile in a bee colony headed by a queen, but the inhibition of ovary activation is lifted upon the absence of queen and larvae. Worker bees are then able to develop mature, viable eggs. The detailed repressive physiological mechanisms that are responsible for this remarkable phenomenon are as of yet largely unknown. Physiological studies today mainly focus on the transcriptome, while the proteome stays rather unexplored. Here, we present a quantitative 2-dimensional differential gel electrophoresis comparison between activated and inactivated worker ovaries and brains of reproductive and sterile worker bees, including a spot map of ovaries, containing 197 identified spots. Our findings suggest that suppression of ovary activation might involve a constant interplay between primordial oogenesis and subsequent degradation, which is probably mediated through steroid and neuropeptide hormone signaling. Additionally, the observation of higher viral protein loads in both the brains and ovaries of sterile workers is particularly noteworthy. This data set will be of great value for future research unraveling the physiological mechanisms underlying the altruistic sterility in honeybee workers.

Research paper thumbnail of Evolution of Self-Organized Task Specialization in Robot Swarms

PLOS Computational Biology, 2015

Division of labor is ubiquitous in biological systems, as evidenced by various forms of complex t... more Division of labor is ubiquitous in biological systems, as evidenced by various forms of complex task specialization observed in both animal societies and multicellular organisms. Although clearly adaptive, the way in which division of labor first evolved remains enigmatic, as it requires the simultaneous co-occurrence of several complex traits to achieve the required degree of coordination. Recently, evolutionary swarm robotics has emerged as an excellent test bed to study the evolution of coordinated group-level behavior. Here we use this framework for the first time to study the evolutionary origin of behavioral task specialization among groups of identical robots. The scenario we study involves an advanced form of division of labor, common in insect societies and known as "task partitioning", whereby two sets of tasks have to be carried out in sequence by different individuals. Our results show that task partitioning is favored whenever the environment has features that, when exploited, reduce switching costs and increase the net efficiency of the group, and that an optimal mix of task specialists is achieved most readily when the behavioral repertoires aimed at carrying out the different subtasks are available as pre-adapted building blocks. Nevertheless, we also show for the first time that self-organized task specialization could be evolved entirely from scratch, starting only from basic, low-level behavioral primitives, using a nature-inspired evolutionary method known as Grammatical Evolution. Remarkably, division of labor was achieved merely by selecting on overall group performance, and without providing any prior information on how the global object retrieval task was best divided into smaller subtasks. We discuss the potential of our method for engineering adaptively behaving robot swarms and interpret our results in relation to the likely path that nature took to evolve complex sociality and task specialization.

Research paper thumbnail of Differential diagnosis of the honey bee trypanosomatids Crithidia mellificae and Lotmaria passim

Journal of Invertebrate Pathology, 2015

Trypanosomatids infecting honey bees have been poorly studied with molecular methods until recent... more Trypanosomatids infecting honey bees have been poorly studied with molecular methods until recently. After the description of Crithidia mellificae (Langridge and McGhee, 1967) it took about forty years until molecular data for honey bee trypanosomatids became available and were used to identify and describe a new trypanosomatid species from honey bees, Lotmaria passim (Evans and Schwarz, 2014). However, an easy method to distinguish them without sequencing is not yet available. Research on the related bumble bee parasites Crithidia bombi and Crithidia expoeki revealed a fragment length polymorphism in the internal transcribed spacer 1 (ITS1), which enabled species discrimination. In search of fragment length polymorphisms for differential diagnostics in honey bee trypanosomatids, we studied honey bee trypanosomatid cell cultures of C. mellificae and L. passim. This research resulted in the identification of fragment length polymorphisms in ITS1 and ITS1-2 markers, which enabled us to develop a diagnostic method to differentiate both honey bee trypanosomatid species without the need for sequencing. However, the amplification success of the ITS1 marker depends probably on the trypanosomatid infection level. Further investigation confirmed that L. passim is the dominant species in Belgium, Japan and Switzerland. We found C. mellificae only rarely in Belgian honey bee samples, but not in honey bee samples from other countries. C. mellificae was also detected in mason bees (Osmia bicornis and Osmia cornuta) besides in honey bees. Further, the characterization and comparison of additional markers from L. passim strain SF (published as C. mellificae strain SF) and a Belgian honey bee sample revealed very low divergence in the 18S rRNA, ITS1-2, 28S rRNA and cytochrome b sequences. Nevertheless, a variable stretch was observed in the gp63 virulence factor.

Research paper thumbnail of No Evidence of Enemy Release in Pathogen and Microbial Communities of Common Wasps (Vespula vulgaris) in Their Native and Introduced Range

PloS one, 2015

When invasive species move to new environments they typically experience population bottlenecks t... more When invasive species move to new environments they typically experience population bottlenecks that limit the probability that pathogens and parasites are also moved. The invasive species may thus be released from biotic interactions that can be a major source of density-dependent mortality, referred to as enemy release. We examined for evidence of enemy release in populations of the common wasp (Vespula vulgaris), which attains high densities and represents a major threat to biodiversity in its invaded range. Mass spectrometry proteomic methods were used to compare the microbial communities in wasp populations in the native (Belgium and England) and invaded range (Argentina and New Zealand). We found no evidence of enemy release, as the number of microbial taxa was similar in both the introduced and native range. However, some evidence of distinctiveness in the microbial communities was observed between countries. The pathogens observed were similar to a variety of taxa observed i...

Research paper thumbnail of Genome sequence heterogeneity of Lake Sinai Virus found in honey bees and Orf1/RdRP-based polymorphisms in a single host

Virus research, Jan 25, 2015

Honey bees (Apis mellifera) are susceptible to a wide range of pathogens, including a broad set o... more Honey bees (Apis mellifera) are susceptible to a wide range of pathogens, including a broad set of viruses. Recently, next-generation sequencing has expanded the list of viruses with, for instance, two strains of Lake Sinai Virus. Soon after its discovery in the USA, LSV was also discovered in other countries and in other hosts. In the present study, we assemble four almost complete LSV genomes, and show that there is remarkable sequence heterogeneity based on the Orf1, RNA-dependent RNA polymerase and capsid protein sequences in comparison to the previously identified LSV 1 and 2 strains. Phylogenetic analyses of LSV sequences obtained from single honey bee specimens further revealed that up to three distinctive clades could be present in a single bee. Such superinfections have not previously been identified for other honey bee viruses. In a search for the putative routes of LSV transmission, we were able to demonstrate the presence of LSV in pollen pellets and in Varroa destructor...

Research paper thumbnail of Self-organized flocking with conflicting goal directions

Proceedings of the European Conference on Complex Systems 2012, 2013

In flocking, a large number of individuals move cohesively in a common direction. Many examples c... more In flocking, a large number of individuals move cohesively in a common direction. Many examples can be found in nature: from simple organisms such as crickets and locusts to more complex ones such as birds, fish and quadrupeds.

Research paper thumbnail of GESwarm

Proceeding of the fifteenth annual conference on Genetic and evolutionary computation conference - GECCO '13, 2013

In this paper we propose GESwarm, a novel tool that can automatically synthesize collective behav... more In this paper we propose GESwarm, a novel tool that can automatically synthesize collective behaviors for swarms of autonomous robots through evolutionary robotics. Evolutionary robotics typically relies on artificial evolution for tuning the weights of an artificial neural network that is then used as individual behavior representation. The main caveat of neural networks is that they are very difficult to reverse engineer, meaning that once a suitable solution is found, it is very difficult to analyze, to modify, and to tease apart the inherent principles that lead to the desired collective behavior. In contrast, our representation is based on completely readable and analyzable individual-level rules that lead to a desired collective behavior.

Research paper thumbnail of The Fungal Aroma Gene ATF1 Promotes Dispersal of Yeast Cells through Insect Vectors

Cell Reports, 2014

Highlights The S. cerevisiae ATF1 gene controls the production of volatile acetate esters Aroma o... more Highlights The S. cerevisiae ATF1 gene controls the production of volatile acetate esters Aroma of ATF1 mutants elicits different neuronal activity in the fly antennal lobe Flies are significantly more attracted to wild-type yeast than to atf1-null mutants Addition of isoamyl acetate and ethyl acetate restores attraction of Drosophila SUMMARY Yeast cells produce various volatile metabolites that are key contributors to the pleasing fruity and flowery aroma of fermented beverages. Several of these fruity metabolites, including isoamyl acetate and ethyl acetate, are produced by a dedicated enzyme, the alcohol acetyl transferase Atf1. However, despite much research, the physiological role of acetate ester formation in yeast remains unknown. Using a combination of molecular biology, neurobiology, and behavioral tests, we demonstrate that deletion of ATF1 alters the olfactory response in the antennal lobe of fruit flies that feed on yeast cells. The flies are much less attracted to the mutant yeast cells, and this in turn results in reduced dispersal of the mutant yeast cells by the flies. Together, our results uncover the molecular details of an intriguing aroma-based communication and mutualism between microbes and their insect vectors. Similar mechanisms may exist in other microbes, including microbes on flowering plants and pathogens.

Research paper thumbnail of Widespread occurrence of honey bee pathogens in solitary bees

Journal of Invertebrate Pathology, 2014

Solitary bees and honey bees from a neighbouring apiary were screened for a broad set of putative... more Solitary bees and honey bees from a neighbouring apiary were screened for a broad set of putative pathogens including protists, fungi, spiroplasmas and viruses. Most sampled bees appeared to be infected with multiple parasites. Interestingly, viruses exclusively known from honey bees such as Apis mellifera Filamentous Virus and Varroa destructor Macula-like Virus were also discovered in solitary bees. A microsporidium found in Andrena vaga showed most resemblance to Nosema thomsoni. Our results suggest that bee hives represent a putative source of pathogens for other pollinators. Similarly, solitary bees may act as a reservoir of honey bee pathogens.

Research paper thumbnail of Towards greater realism in inclusive fitness models: the case of worker reproduction in insect societies

Biology letters, 2013

The conflicts over sex allocation and male production in insect societies have long served as an ... more The conflicts over sex allocation and male production in insect societies have long served as an important test bed for Hamilton's theory of inclusive fitness, but have for the most part been considered separately. Here, we develop new coevolutionary models to examine the interaction between these two conflicts and demonstrate that sex ratio and colony productivity costs of worker reproduction can lead to vastly different outcomes even in species that show no variation in their relatedness structure. Empirical data on worker-produced males in eight species of Melipona bees support the predictions from a model that takes into account the demographic details of colony growth and reproduction. Overall, these models contribute significantly to explaining behavioural variation that previous theories could not account for.

Research paper thumbnail of Evolutionary synthesis of multi-agent systems for dynamic dial-a-ride problems

Proceedings of the fourteenth international conference on Genetic and evolutionary computation conference companion - GECCO Companion '12, 2012

In dynamic dial-a-ride problems a fleet of vehicles need to handle transportation requests within... more In dynamic dial-a-ride problems a fleet of vehicles need to handle transportation requests within time. We research how to create a decentralized multi-agent system that can solve the dynamic dial-a-ride problem. Normally multi-agent systems are hand designed for each specific application. In this paper we research the applicability of genetic programming to automatically program a multi-agent system that solves dial-a-ride problems. We evaluated the evolved system by running a number of simulations and compared it's performance to a selection hyper-heuristic. The results shows that genetic programming can be a viable alternative to hand constructing multi-agent systems.

Research paper thumbnail of Bourgeois Behavior and Freeloading in the Colonial Orb Web Spider Parawixia bistriata (Araneae, Araneidae)

The American Naturalist, 2013

Online enhancement: appendix. Dryad data: http://dx.doi.org/10.5061/dryad.1205d.