About
146
Publications
19,393
Reads
How we measure 'reads'
A 'read' is counted each time someone views a publication summary (such as the title, abstract, and list of authors), clicks on a figure, or views or downloads the full-text. Learn more
3,664
Citations
Introduction
I am an evolutionary biologist applying cutting-edge genomics and bioinformatics technologies to understand the genetic basis of social behavior in colonies of insects (mostly ants & bumblebees).
https://wurmlab.github.io
Current institution
Additional affiliations
January 2012 - present
January 2007 - December 2011
January 2005 - December 2011
Publications
Publications (146)
The >15 000 ant species are all highly social and show great variation in colony organization, complexity and behavior. The mechanisms by which such sociality evolved, as well as those underpinning the elaboration of ant societies since their ∼140 million year old common ancestor, have long been pondered. Here, we review recent insights generated u...
Variation in social behavior is common yet little is known about the genetic architectures underpinning its evolution. A rare exception is in the fire ant Solenopsis invicta: Alternative variants of a supergene region determine whether a colony will have exactly one or up to dozens of queens. The two variants of this region are carried by a pair of...
Variation in social behavior is common yet our knowledge of the mechanisms underpinning its evolution is limited. The fire ant Solenopsis invicta provides a textbook example of a Mendelian element controlling social organization: alternate alleles of a genetic element first identified as encoding an odorant binding protein (OBP) named Gp-9 determin...
Complex adaptive polymorphisms are common in nature, but what mechanisms maintain the underlying favorable allelic combinations [1-4]? The convergent evolution of polymorphic social organization in two independent ant species provides a great opportunity to investigate how genomes evolved under parallel selection. Here, we demonstrate that a large,...
Intraspecific variability in social organization is common, yet the underlying causes are rarely known. In the fire ant Solenopsis invicta, the existence of two divergent forms of social organization is under the control of a single Mendelian genomic element marked by two variants of an odorant-binding protein gene. Here we characterize the genomic...
Background
Beneficial insects, including pollinators, encounter various pesticide exposure conditions, from brief high-concentration acute exposure to continuous low-level chronic exposure. To effectively assess the environmental risks of pesticides, it is critical to understand how different exposure schemes influence their effects. Unfortunately,...
Beneficial wild insects including pollinators encounter various pesticide exposure conditions, from brief high concentrations to continuous low-level exposure. To effectively assess the environmental risks of pesticides, it is critical to understand how different exposure patterns influence their effects. Unfortunately, this knowledge remains limit...
Pesticides often harm beneficial insect pollinators, impairing their ability to navigate the environment, learn, fight off disease, and reproduce. Understanding the mechanisms behind these disorders is essential for improving pesticide risk assessments. To test whether pesticide exposure induces similar or distinct transcriptional responses across...
The waggle dances of honeybees are a strikingly complex form of animal communication that underlie the collective foraging behaviour of colonies. The mechanisms by which bees assess the locations of forage sites that they have visited for representation on the dancefloor are now well-understood, but few studies have considered the remarkable backwa...
Ant colonies ancestrally contained one queen and her non-reproductive workers. This is also the case for many but not all colonies of the Mediterranean big-headed ant Pheidole pallidula. Indeed, this species also has a derived form of social organization with multiple reproductive queens in the colony. The co-existence of two social forms also inde...
Ants are among the most successful organisms on Earth. It has been suggested that forming symbioses with nutrient-supplementing microbes may have contributed to their success, by allowing ants to invade otherwise inaccessible niches. However, it is unclear whether ants have evolved symbioses repeatedly to overcome the same nutrient limitations. Her...
Ants, bees, wasps, bark beetles, and other species have haploid males and diploid females. Although such haplodiploid species play key ecological roles and are threatened by environmental changes, no general framework exists for simulating their genetic evolution. Here, we use the SLiM simulation environment to build a novel model for individual-ba...
Introgression has been proposed as an essential source of adaptive genetic variation. However, a key barrier to adaptive introgression is that recombination can break down combinations of alleles that underpin many traits. This barrier might be overcome in supergene regions, where suppressed recombination leads to joint inheritance across many loci...
Environmental changes threaten insect pollinators, creating risks for agriculture and ecosystem stability. Despite their importance, we know little about how wild insects respond to environmental pressures. To understand the genomic bases of adaptation in an ecologically important pollinator, we analyzed genomes of Bombus terrestris bumblebees coll...
The benefits of cooperative living for foraging, nesting, defence, and buffering environmental challenges lead animals with the most highly social lifestyles to dominate many ecosystems. However, living in larger, more highly connected groups should also increase the risks of pathogen exposure and transmission. While over long timescales, selective...
Ants, bees, wasps, bark beetles, and other species have haploid males and diploid females. Although such haplodiploid species play key ecological roles and are threatened by environmental changes, no general framework exists for simulating their genetic evolution. Here, we use the SLiM simulation environment to build a novel model for individual-ba...
Ants are among the most successful organisms on earth. It has been suggested that forming symbioses with nutrient-supplementing microbes may have contributed to their success, by allowing ants to invade otherwise inaccessible niches. However, it is unclear whether ants have repeatedly evolved symbioses to overcome the same nutrient limitations. Her...
Social life and isolation pose a complex suite of challenges to organisms prompting significant changes in neural state. However, plasticity in how brains respond to social challenges remains largely unexplored. The fire ants Solenopsis invicta provide an ideal scenario for examining this. Fire ant queens may found colonies individually or in group...
Long-molecule sequencing is now routinely applied to generate high-quality reference genome assemblies. However, datasets differ in repeat composition, heterozygosity, read lengths and error profiles. The assembly parameters that provide the best results could thus differ across datasets. By integrating four complementary and biologically meaningfu...
Behavioral experiments and analyses of observation records have shown that environmental changes threaten insect pollinators, creating risks for agriculture and ecosystem stability. Despite their importance, we know little about how wild insects or other animals can adapt in response to environmental pressures. To understand the genomic bases of ad...
Introgression has been proposed as an essential source of trait adaptation. However, a key barrier to adaptive introgression is that recombination can break down combinations of alleles that underpin many traits. Supergene regions, where suppressed recombination leads to joint inheritance of alleles at many loci, could overcome this challenge. Here...
A symbiotic partnership with Blochmannia bacteria is thought to underpin the ecological success of carpenter ants. Disentangling the molecular interactions between the mutualistic partners supports an old hypothesis that many other ants also had similar symbioses and lost them.
Supergene regions maintain alleles of multiple genes in tight linkage through suppressed recombination. Despite their importance in determining complex phenotypes, our empirical understanding of early supergene evolution is limited. Here we focus on the young "social" supergene of fire ants, a powerful system for disentangling the effects of evolut...
Supergene regions maintain alleles of multiple genes in tight linkage through suppressed recombination. Despite their importance in determining complex phenotypes, our empirical understanding of early supergene evolution is limited. Here we focus on the young ‘social’ supergene of fire ants, a powerful system for disentangling the effects of evolut...
Supergene regions maintain alleles of multiple genes in tight linkage through suppressed recombination. Despite their importance in determining complex phenotypes, our empirical understanding of early supergene evolution is limited. Here we focus on the young ‘social’ supergene of fire ants, a powerful system for disentangling the effects of evolut...
DNA/RNA extraction protocol from Trizol/ Tri reagent, as used on fire ants in Martinez-Ruiz et al: "Genomic architecture and evolutionary antagonism drive allelic expression bias in the social supergene of red fire ants" Derived from an initial protocol developped by John Wang & Christine LaMendola.
Taxonomically restricted genes (TRGs) are genes that are present only in one clade. Protein-coding TRGs may evolve de novo from previously non-coding sequences: functional ncRNA, introns or alternative reading frames of older protein-coding genes, or intergenic sequences. A major challenge in studying de novo genes is the need to avoid both false p...
Supergenes are genomic regions of suppressed recombination that underlie complex polymorphisms. Despite the importance of such regions, our empirical understanding of their early evolution is limited. The young “social” supergene of the fire ant Solenopsis invicta provides a powerful system for disentangling the roles of evolutionary conflict and t...
Pollinators have been declining worldwide, and pesticides have contributed to these declines. High-resolution approaches from molecular medicine can provide unparalleled insight into organismal physiology and health. Applying these approaches to pollinators can significantly improve the efficiency and sensitivity of pesticide research and evaluatio...
Comparing newly obtained and previously known nucleotide and amino-acid sequences underpins modern biological research. BLAST is a well-established tool for such comparisons but is challenging to use on new datasets. We combined a user-centric design philosophy with sustainable software development approaches to create Sequenceserver, a tool for ru...
GeneValidator is a tool for determining whether the characteristics of newly predicted protein-coding genes are consistent with those of similar sequences in public databases. For this, it runs up to seven comparisons per gene. Results are shown in an HTML report containing summary statistics and graphical visualizations that aim to be useful for c...
Background
Adapting to changes in the environment is the foundation of species survival, and is usually thought to be a gradual process. However, transposable elements (TEs), epigenetic modifications, and/or genetic material acquired from other organisms by means of horizontal gene transfer (HGTs), can also lead to novel adaptive traits. Social ins...
Social bees are important insect pollinators of wildflowers and agricultural crops, making their reported declines a global concern. A major factor implicated in these declines is the widespread use of neonicotinoid pesticides. Indeed, recent research has demonstrated that exposure to low doses of these neurotoxic pesticides impairs bee behaviours...
Long-term suppression of recombination ultimately leads to gene loss, as demonstrated by the depauperate Y and W chromosomes of long-established pairs of XY and ZW chromosomes. The young social supergene of the Solenopsis invicta red fire ant provides a powerful system to examine the effects of suppressed recombination over a shorter timescale. The...
The wood ant Formica exsecta (Formicidae; Hymenoptera), is a common ant species throughout the Palearctic region. The species is a well established model for studies of ecological characteristics and evolutionary conflict. In this study, we sequenced and assembled draft genomes for Formica exsecta and its endosymbiont Wolbachia . The draft F. exsec...
Electronic supplementary material is available online at https://dx. Social bees represent an important group of pollinating insects that can be exposed to potentially harmful pesticides when foraging on treated or contaminated flowering plants. To investigate if such exposure is detrimental to bees, many studies have exclusively fed individuals wi...
SI: Foraging bumblebees acquire a preference for neonicotinoid treated food with prolonged exposure
Suppressed recombination ultimately leads to gene loss, as demonstrated by the depauperate Y chromosomes of long-established XY pairs. To understand the shorter term effects, we used high-resolution optical mapping and k-mer distribution analysis in a young non-recombining region of fire ant social chromosomes. Instead of shrinking, the region has...
Table S1. Summary of correspondences between identifiers of sequences produced in this project and previously published sequences, including the number of sequence differences between the two groups.
Table S2. Accession numbers of the gene expression data used. “Project” and “SRA” columns indicate NCBI identifiers. The descriptions provided and th...
Figure S1. Density distribution of the p‐values for differential expression between social forms in queens for OBPs (in green) and all other protein‐coding genes (red). The p‐values for OBPs are strongly skewed towards 0. This result is based on the expression levels from the Morandin et al. (2016) dataset.
Figure S2. Correspondence between queen...
Fig. S1 Filtering the data by quality values and assembly quality removes sites with very low coverage calls.
Fig. S2 Differentiation and diversity in linkage group 1 and linkage group 16 (the social chromosome) in 30 kb sliding windows with a step of 10 kb.
Fig. S3 Differentiation and diversity in linkage group 1 and linkage group 16 (the social...
Pesticide exposure has been implicated as a contributor to insect pollinator declines. In social bees, which are crucial pollination service providers, the effect of low‐level chronic exposure is typically non‐lethal leading researchers to consider whether exposure induces sublethal effects on behaviour and whether such impairment can affect colony...
Neuropeptides are evolutionarily ancient mediators of neuronal signalling in nervous systems. With recent advances in genomics/transcriptomics, an increasingly wide range of species has become accessible for molecular analysis. The deuterostomian invertebrates are of particular interest in this regard because they occupy an 'intermediate' position...
Genomes of emerging model organisms are now being sequenced at very low cost. However, obtaining accurate gene predictions remains challenging: even the best gene prediction algorithms make substantial errors and can jeopardize subsequent analyses. Therefore, many predicted genes must be time-consumingly visually inspected and manually curated. We...
The dramatic drop in DNA sequencing costs has created many opportunities for novel biological research. These opportunities largely rest upon the ability to effectively compare newly obtained and previously known sequences. This is commonly done with BLAST, yet using BLAST directly on new datasets requires substantial technical skills or helpful co...
Myrmecologists have long studied the systematics, behavior, ecology, and evolution of ants. This first involved fundamental approaches including morphological description or behavioral observation, perhaps with the help of microscopes or marking ants with paint or wire. Many discoveries over the past 20 years have been accomplished with the help of...
Within the Environmental 'omics community Bio-Linux is a widely used tool. This has the advantage of providing in a single deliverable package all necessary software and tools to support common analyses. With the growth in data volumes within the community and increasing constraints on user access and control over their own desktops an alternative...
Retracted vs robust reproducible research.
Males in many animal species differ greatly from females in morphology, physiology and behaviour. Ants, bees and wasps have a haplodiploid mechanism of sex determination whereby unfertilized eggs become males while fertilized eggs become females. However, many species also have a low frequency of diploid males, which are thought to develop from dip...
Adaptation requires genetic variation, but founder populations are generally genetically depleted. Here we sequence two populations of an inbred ant that diverge in phenotype to determine how variability is generated. Cardiocondyla obscurior has the smallest of the sequenced ant genomes and its structure suggests a fundamental role of transposable...
Paralog-specific primers used for qRT-PCR (5′-3′ order).
(DOCX)
Transcripts upregulated in haplometrotic queens. Expression patterns of 2280 significantly differentially regulated transcripts grouped in cluster 1 by k-means clustering in Genesis (for a GO analysis of these transcripts see Table S4).
(EPS)
Quantitative real-time PCR validation of expression levels of genes of interest. Expression levels of the following genes associated with GO terms of interest were analyzed using quantitative real-time PCR (see Table S10 for detailed information about these genes and the primers we used): Indy and Sod2 (determination of adult life span); Dredd and...
Microarray hybridization scheme for experiment 2. For each group of queens, 6 individuals where hybridized in a loop design: 3 individuals were labeled with the Cy3 dye and other 3 with the Cy5 dye. 12-plex array slides with 135,000 probe capacity where designed by Roche NimbleGen, Inc. (Madison WI). win/los = winners switched to losers; win/win =...
Microarray hybridization scheme for experiment 1. For each group of queens, 8 individuals where hybridized in a loop design: 4 individuals were labeled with the Cy3 dye and other 4 with the Cy5 dye. 12-plex array slides with 135,000 probe capacity where designed by Roche NimbleGen, Inc. (Madison WI). haplo = haplometrotic queens; los = pleometrotic...
Movie clip showing the occurrence of aggressive interactions among cofoundresses after the emergence of workers. Note the difference between pair #9, where pleometrotic queens clearly perform fighting behavior and the two other pairs of cofounding queens, where the interactions are still cooperative.
(WMV)
Experiment 1: significantly differentially regulated transcripts (P<0.001).
(XLSX)
Experiment 1, output of the cateGOrizer analysis: representation of GO_slim2 ancestor terms.
(XLSX)
Experiment 1, k-means clustering, cluster 1 (genes upregulated in haplo): significantly enriched GO terms (Functional Annotation Clustering, medium stringency, P<0.05).
(XLSX)
Experiment 1: GO terms significantly enriched (Functional Annotation Clustering, medium stringency, P<0.05) and significantly differentially regulated transcripts (P<0.001) between winners and losers.
(XLSX)
Experiment 1, cluster 1: significantly enriched KEGG pathways and GO terms that were used in the analyses with the cateGOrizer “Immune system gene classes” (Functional Annotation Chart, P<0.05).
(XLSX)
Quantitative real-time PCR validation of expression levels of genes of interest from experiment 1: gene lists and primers' sequences.
(XLSX)
Comparative studies: GO analysis of overlapping transcripts that were significantly differentially regulated (P<0.1) between win and los in experiment 1 and experiment 2.
(XLSX)
Transcripts downregulated in haplometrotic queens. Expression patterns of 912 significantly differentially regulated transcripts grouped in cluster 2 by k-means clustering in Genesis (for a GO analysis of these transcripts see Table S5).
(EPS)
Experiment 1: significantly enriched GO terms and KEGG pathways (Functional Annotation Chart, P<0.05).
(XLSX)
Behavioral observation of pleometrotic couples. Just before the emergence of the first workers, haplometrotic queens and pleometrotic couples were placed in pencil boxes where it was easier to observe queen-queen and queen-workers interactions. As shown in the figure, in pleometrotic couples the winner queen was usually found inside the nest chambe...
Experiment 1, cluster 2: significantly enriched KEGG pathways and GO terms that were used in the analyses with the cateGOrizer “Immune system gene classes” (Functional Annotation Chart, P<0.05).
(XLSX)
Experiment 2: significantly differentially regulated transcripts (P<0.1).
(XLSX)