Publications by authors named "Jürgen Gadau"

52 Publications

Inhibition of HSP90 causes morphological variation in the invasive ant Cardiocondyla obscurior.

J Exp Zool B Mol Dev Evol 2021 06 23;336(4):333-340. Epub 2021 Feb 23.

Institute for Evolution and Biodiversity, University of Münster, Münster, Germany.

Canalization underlies the expression of steady phenotypes in the face of unsteady environmental conditions or varying genetic backgrounds. The chaperone HSP90 has been identified as a key component of the molecular machinery regulating canalization and a growing body of research suggests that HSP90 could act as a general capacitator in evolution. However, empirical data about HSP90-dependent phenotypic variation and its evolutionary impact is still scarce, particularly for non-model species. Here we report how pharmacological suppression of HSP90 increases morphological variation up to 87% in the invasive ant Cardiocondyla obscurior. We show that workers treated with the HSP90 inhibitor 17-DMAG are significantly more diverse compared to untreated workers in two of four measured traits: maximal eye distance and maximal propodeal spine distance. We further find morphological differentiation between natural populations of C. obscurior in the same traits that responded to our pharmacological treatment. These findings add support for the putative impact of HSP90 on canalization, the modularity of phenotypic traits, and its potential role in morphological evolution of ants.
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http://dx.doi.org/10.1002/jez.b.23035DOI Listing
June 2021

Genome assembly and annotation of the California harvester ant Pogonomyrmex californicus.

G3 (Bethesda) 2021 01;11(1)

Faculty of Medicine, Institute of Bioinformatics, University of Münster, 48149 Münster, Germany.

The harvester ant genus Pogonomyrmex is endemic to arid and semiarid habitats and deserts of North and South America. The California harvester ant Pogonomyrmex californicus is the most widely distributed Pogonomyrmex species in North America. Pogonomyrmex californicus colonies are usually monogynous, i.e. a colony has one queen. However, in a few populations in California, primary polygyny evolved, i.e. several queens cooperate in colony founding after their mating flights and continue to coexist in mature colonies. Here, we present a genome assembly and annotation of P. californicus. The size of the assembly is 241 Mb, which is in agreement with the previously estimated genome size. We were able to annotate 17,889 genes in total, including 15,688 protein-coding ones with BUSCO (Benchmarking Universal Single-Copy Orthologs) completeness at a 95% level. The presented P. californicus genome assembly will pave the way for investigations of the genomic underpinnings of social polymorphism in the number of queens, regulation of aggression, and the evolution of adaptations to dry habitats.
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http://dx.doi.org/10.1093/g3journal/jkaa019DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8022709PMC
January 2021

Comprehensive phylogeny of Myrmecocystus honey ants highlights cryptic diversity and infers evolution during aridification of the American Southwest.

Mol Phylogenet Evol 2021 02 3;155:107036. Epub 2020 Dec 3.

School of Life Sciences, Arizona State University, 427 E Tyler Mall, Tempe, AZ 85287-1501, USA; Department of Entomology, Plant Pathology and Nematology, University of Idaho, 875 Perimeter Drive, Moscow, ID 83844-2329, USA; Institute for Bioinformatics and Evolutionary Studies (IBEST), University of Idaho, 875 Perimeter Drive, Moscow, ID 83844-2329, USA. Electronic address:

The New World ant genus Myrmecocystus Wesmael, 1838 (Formicidae: Formicinae: Lasiini) is endemic to arid and semi-arid habitats of the western United States and Mexico. Several intriguing life history traits have been described for the genus, the best-known of which are replete workers, that store liquified food in their largely expanded crops and are colloquially referred to as "honeypots". Despite their interesting biology and ecological importance for arid ecosystems, the evolutionary history of Myrmecocystus ants is largely unknown and the current taxonomy presents an unsatisfactory systematic framework. We use ultraconserved elements to infer the evolutionary history of Myrmecocystus ants and provide a comprehensive, dated phylogenetic framework that clarifies the molecular systematics within the genus with high statistical support, reveals cryptic diversity, and reconstructs ancestral foraging activity. Using maximum likelihood, Bayesian and species tree approaches on a data set of 134 ingroup specimens (including samples from natural history collections and type material), we recover largely identical topologies that leave the position of only few clades uncertain and cover the intra- and interspecific variation of 28 of the 29 described and six undescribed species. In addition to traditional support values, such as bootstrap and posterior probability, we quantify genealogical concordance to estimate the effects of conflicting evolutionary histories on phylogenetic inference. Our analyses reveal that the current taxonomic classification of the genus is inconsistent with the molecular phylogenetic inference, and we identify cryptic diversity in seven species. Divergence dating suggests that the split between Myrmecocystus and its sister taxon Lasius occurred in the early Miocene. Crown group Myrmecocystus started diversifying about 14.08 Ma ago when the gradual aridification of the southwestern United States and northern Mexico led to formation of the American deserts and to adaptive radiations of many desert taxa.
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http://dx.doi.org/10.1016/j.ympev.2020.107036DOI Listing
February 2021

The Power of Infochemicals in Mediating Individualized Niches.

Trends Ecol Evol 2020 11 26;35(11):981-989. Epub 2020 Jul 26.

Department of Behavioural Biology, University of Münster, Badestr. 13, 48149 Münster, Germany.

Infochemicals, including hormones, pheromones, and allelochemicals, play a central role in mediating information and shaping interactions within and between individuals. Due to their high plasticity, infochemicals are predestined mediators in facilitating individualized niches of organisms. Only recently it has become clear that individual differences are essential to understand how and why individuals realize a tiny subset of the species' niche. Moreover, individual differences have a central role in both ecological adjustment and evolutionary adaptation in a rapidly changing world. Here we highlight that infochemicals act as key signals or cues and empower the realization of the individualized niche through three proposed processes: niche choice, niche conformance, and niche construction.
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http://dx.doi.org/10.1016/j.tree.2020.07.001DOI Listing
November 2020

Individual learning phenotypes drive collective behavior.

Proc Natl Acad Sci U S A 2020 07 15;117(30):17949-17956. Epub 2020 Jul 15.

School of Life Sciences, Arizona State University, Tempe, AZ 85287.

Individual differences in learning can influence how animals respond to and communicate about their environment, which may nonlinearly shape how a social group accomplishes a collective task. There are few empirical examples of how differences in collective dynamics emerge from variation among individuals in cognition. Here, we use a naturally variable and heritable learning behavior called latent inhibition (LI) to show that interactions among individuals that differ in this cognitive ability drive collective foraging behavior in honey bee colonies. We artificially selected two distinct phenotypes: high-LI bees that ignore previously familiar stimuli in favor of novel ones and low-LI bees that learn familiar and novel stimuli equally well. We then provided colonies differentially composed of different ratios of these phenotypes with a choice between familiar and novel feeders. Colonies of predominantly high-LI individuals preferred to visit familiar food locations, while low-LI colonies visited novel and familiar food locations equally. Interestingly, in colonies of mixed learning phenotypes, the low-LI individuals showed a preference to visiting familiar feeders, which contrasts with their behavior when in a uniform low-LI group. We show that the shift in feeder preference of low-LI bees is driven by foragers of the high-LI phenotype dancing more intensely and attracting more followers. Our results reveal that cognitive abilities of individuals and their social interactions, which we argue relate to differences in attention, drive emergent collective outcomes.
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http://dx.doi.org/10.1073/pnas.1920554117DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7395545PMC
July 2020

Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum.

BMC Genomics 2020 May 29;21(1):376. Epub 2020 May 29.

Department of Sciences, University of Basilicata, 85100, Potenza, Italy.

Background: Parasitoid wasps have fascinating life cycles and play an important role in trophic networks, yet little is known about their genome content and function. Parasitoids that infect aphids are an important group with the potential for biological control. Their success depends on adapting to develop inside aphids and overcoming both host aphid defenses and their protective endosymbionts.

Results: We present the de novo genome assemblies, detailed annotation, and comparative analysis of two closely related parasitoid wasps that target pest aphids: Aphidius ervi and Lysiphlebus fabarum (Hymenoptera: Braconidae: Aphidiinae). The genomes are small (139 and 141 Mbp) and the most AT-rich reported thus far for any arthropod (GC content: 25.8 and 23.8%). This nucleotide bias is accompanied by skewed codon usage and is stronger in genes with adult-biased expression. AT-richness may be the consequence of reduced genome size, a near absence of DNA methylation, and energy efficiency. We identify missing desaturase genes, whose absence may underlie mimicry in the cuticular hydrocarbon profile of L. fabarum. We highlight key gene groups including those underlying venom composition, chemosensory perception, and sex determination, as well as potential losses in immune pathway genes.

Conclusions: These findings are of fundamental interest for insect evolution and biological control applications. They provide a strong foundation for further functional studies into coevolution between parasitoids and their hosts. Both genomes are available at https://bipaa.genouest.org.
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http://dx.doi.org/10.1186/s12864-020-6764-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7257214PMC
May 2020

Detection of very long-chain hydrocarbons by laser mass spectrometry reveals novel species-, sex-, and age-dependent differences in the cuticular profiles of three Nasonia species.

Anal Bioanal Chem 2019 May 8;411(13):2981-2993. Epub 2019 Apr 8.

Institute for Hygiene, University of Münster, Robert-Koch-Str. 41, 48149, Münster, Germany.

Long-chain cuticular hydrocarbons (CHC) are key components of chemical communication in many insects. The parasitoid jewel wasps from the genus Nasonia use their CHC profile as sex pheromone and for species recognition. The standard analytical tool to analyze CHC is gas chromatography coupled with mass spectrometric detection (GC/MS). This method reliably identifies short- to long-chain alkanes and alkenes, but CHC with more than 40 carbon atoms are usually not detected. Here, we applied two laser mass spectrometry (MS) techniques, namely direct laser desorption/ionization (d)LDI and silver-assisted (Ag-)LDI MS, respectively, to analyze CHC profiles of N. vitripennis, N. giraulti, and N. longicornis directly from the cuticle or extracts. Furthermore, we applied direct analysis in real-time (DART) MS as another orthogonal technique for extracts. The three methods corroborated previous results based on GC/MS, i.e., the production of CHC with carbon numbers between C25 and C40. However, we discovered a novel series of long-chain CHC ranging from C41 to C51/C52. Additionally, several previously unreported singly and doubly unsaturated alkenes in the C31-C39 range were found. Use of principal component analysis (PCA) revealed that the composition of the newly discovered CHC varies significantly between species, sex, and age of the animals. Our study adds to the growing literature on the presence of very long-chain CHC in insects and hints at putative roles in insect communication. Graphical abstract.
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http://dx.doi.org/10.1007/s00216-019-01736-yDOI Listing
May 2019

Genetic Incompatibilities Between Mitochondria and Nuclear Genes: Effect on Gene Flow and Speciation.

Front Genet 2019 13;10:62. Epub 2019 Feb 13.

School of Economics and Management, Kochi University of Technology, Kami, Japan.

The process of speciation is, according to the biological species concept, the reduction in gene flow between genetically diverging populations. Most of the previous theoretical studies analyzed the effect of nuclear genetic incompatibilities on gene flow. There is, however, an increasing number of empirical examples suggesting that cytoplasmically inherited genetic elements play an important role in speciation. Here, we present a theoretical analysis of mitochondrial driven speciation, in which genetic incompatibilities occur between mitochondrial haplotypes and nuclear alleles. Four population genetic models with mainland-island structure were analyzed that differ with respect to the type of incompatibility and the underlying genetics. Gene flow reduction was measured on selectively neutral alleles of an unlinked locus and quantified by the effective migration rate. Analytical formulae for the different scenarios were derived using the fitness graph method. For the models with haploid genetics, we found that mito-nuclear incompatibilities (MtNI) are as strong as nuclear-nuclear incompatibilities (NNI) in reducing gene flow at the unlinked locus, but only if males and females migrate in equal number. For models with diploid genetics, we found that MtNI reduce gene flow stronger than NNI when incompatibilities are recessive, but weaker when they are dominant. For both haploid and diploid MtNI, we found that gene flow reduction is stronger if females are the migrating sex, but weaker than NNI when males are the migrating sex. These results encourage further examination on the role of mitochondria on genetic divergence and speciation and point toward specific factors (e.g., migrating sex) that could be the focus of an empirical test.
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http://dx.doi.org/10.3389/fgene.2019.00062DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6396729PMC
February 2019

Individual differences in learning and biogenic amine levels influence the behavioural division between foraging honeybee scouts and recruits.

J Anim Ecol 2019 02 2;88(2):236-246. Epub 2018 Nov 2.

School of Life Sciences, Arizona State University, Tempe, Arizona.

Animals must effectively balance the time they spend exploring the environment for new resources and exploiting them. One way that social animals accomplish this balance is by allocating these two tasks to different individuals. In honeybees, foraging is divided between scouts, which tend to explore the landscape for novel resources, and recruits, which tend to exploit these resources. Exploring the variation in cognitive and physiological mechanisms of foraging behaviour will provide a deeper understanding of how the division of labour is regulated in social insect societies. Here, we uncover how honeybee foraging behaviour may be shaped by predispositions in performance of latent inhibition (LI), which is a form of non-associative learning by which individuals learn to ignore familiar information. We compared LI between scouts and recruits, hypothesizing that differences in learning would correlate with differences in foraging behaviour. Scouts seek out and encounter many new odours while locating novel resources, while recruits continuously forage from the same resource, even as its quality degrades. We found that scouts show stronger LI than recruits, possibly reflecting their need to discriminate forage quality. We also found that scouts have significantly elevated tyramine compared to recruits. Furthermore, after associative odour training, recruits have significantly diminished octopamine in their brains compared to scouts. These results suggest that individual variation in learning behaviour shapes the phenotypic behavioural differences between different types of honeybee foragers. These differences in turn have important consequences for how honeybee colonies interact with their environment. Uncovering the proximate mechanisms that influence individual variation in foraging behaviour is crucial for understanding the ecological context in which societies evolve.
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http://dx.doi.org/10.1111/1365-2656.12911DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6379132PMC
February 2019

Task allocation and site fidelity jointly influence foraging regulation in honeybee colonies.

R Soc Open Sci 2017 Aug 30;4(8):170344. Epub 2017 Aug 30.

Department of Ecology and Evolutionary Biology, University of California Los Angeles, Los Angeles, CA, USA.

Variation in behaviour among group members often impacts collective outcomes. Individuals may vary both in the task that they perform and in the persistence with which they perform each task. Although both the distribution of individuals among tasks and differences among individuals in behavioural persistence can each impact collective behaviour, we do not know if and how they jointly affect collective outcomes. Here, we use a detailed computational model to examine the joint impact of colony-level distribution among tasks and behavioural persistence of individuals, specifically their fidelity to particular resource sites, on the collective trade-off between exploring for new resources and exploiting familiar ones. We developed an agent-based model of foraging honeybees, parametrized by data from five colonies, in which we simulated scouts, who search the environment for new resources, and individuals who are recruited by the scouts to the newly found resources, i.e. recruits. We varied the persistence of returning to a particular food source of both scouts and recruits and found that, for each value of persistence, there is a different optimal ratio of scouts to recruits that maximizes resource collection by the colony. Furthermore, changes to the persistence of scouts induced opposite effects from changes to the persistence of recruits on the collective foraging of the colony. The proportion of scouts that resulted in the most resources collected by the colony decreased as the persistence of recruits increased. However, this optimal proportion of scouts increased as the persistence of scouts increased. Thus, behavioural persistence and task participation can interact to impact a colony's collective behaviour in orthogonal directions. Our work provides new insights and generates new hypotheses into how variations in behaviour at both the individual and colony levels jointly impact the trade-off between exploring for new resources and exploiting familiar ones.
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http://dx.doi.org/10.1098/rsos.170344DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5579100PMC
August 2017

Expression differences in (Hymenoptera: Braconidae) females reared on different aphid host species.

PeerJ 2017 21;5:e3640. Epub 2017 Aug 21.

Instituto de Ciencias Biológicas, Universidad de Talca, Talca, Chile.

The molecular mechanisms that allow generalist parasitoids to exploit many, often very distinct hosts are practically unknown. The wasp a generalist koinobiont parasitoid of aphids, was introduced from Europe into Chile in the late 1970s to control agriculturally important aphid species. A recent study showed significant differences in host preference and host acceptance (infectivity) depending on the host were reared on. In contrast, no genetic differentiation between populations parasitizing different aphid species and aphids of the same species reared on different host plants was found in Chile. Additionally, the same study did not find any fitness effects in if offspring were reared on a different host as their mothers. Here, we determined the effect of aphid host species ( versus reared on two different host plants alfalfa and pea) on the transcriptome of adult females. We found a large number of differentially expressed genes (between host species: head: 2,765; body: 1,216; within the same aphid host species reared on different host plants: alfalfa versus pea: head 593; body 222). As expected, the transcriptomes from parasitoids reared on the same host species (pea aphid) but originating from different host plants (pea versus alfalfa) were more similar to each other than the transcriptomes of parasitoids reared on a different aphid host and host plant (head: 648 and 1,524 transcripts; body: 566 and 428 transcripts). We found several differentially expressed odorant binding proteins and olfactory receptor proteins in particular, when we compared parasitoids from different host species. Additionally, we found differentially expressed genes involved in neuronal growth and development as well as signaling pathways. These results point towards a significant rewiring of the transcriptome of depending on aphid-plant complex where parasitoids develop, even if different biotypes of a certain aphid host species () are reared on the same host plant. This difference seems to persist even after the different wasp populations were reared on the same aphid host in the laboratory for more than 50 generations. This indicates that either the imprinting process is very persistent or there is enough genetic/allelic variation between populations. The role of distinct molecular mechanisms is discussed in terms of the formation of host fidelity.
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http://dx.doi.org/10.7717/peerj.3640DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5572533PMC
August 2017

The hologenome concept: we need to incorporate function.

Theory Biosci 2017 Dec 19;136(3-4):89-98. Epub 2016 Dec 19.

Institute for Evolution and Biodiversity, University of Münster, Hüfferstraße 1, 48149, Münster, Germany.

Are we in the midst of a paradigm change in biology and have animals and plants lost their individuality, i.e., are even so-called 'typical' organisms no longer organisms in their own right? Is the study of the holobiont-host plus its symbiotic microorganisms-no longer optional, but rather an obligatory path that must be taken for a comprehensive understanding of the ecology and evolution of the individual components that make up a holobiont? Or are associated microbes merely a component of their host's environment, and the holobiont concept is just a beautiful idea that does not add much or anything to our understanding of evolution? This article explores different aspects of the concept of the holobiont. We focus on the aspect of functional integration, a central holobiont property, which is only rarely considered thoroughly. We conclude that the holobiont comes in degrees, i.e., we regard the property of being a holobiont as a continuous trait that we term holobiontness, and that holobiontness is differentiated in several dimensions. Although the holobiont represents yet another level of selection (different from classical individual or group selection because it acts on a system that is composed of multiple species), it depends on the grade of functional integration whether or not the holobiont concept helps to cast light on the various degrees of interactions between symbiotic partners.
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http://dx.doi.org/10.1007/s12064-016-0240-zDOI Listing
December 2017

Gene expression and variation in social aggression by queens of the harvester ant Pogonomyrmex californicus.

Mol Ecol 2016 08 30;25(15):3716-30. Epub 2016 Jun 30.

School of Life Sciences, Arizona State University, 427 East Tyler Mall, Tempe, AZ, 85287, USA.

A key requirement for social cooperation is the mitigation and/or social regulation of aggression towards other group members. Populations of the harvester ant Pogonomyrmex californicus show the alternate social phenotypes of queens founding nests alone (haplometrosis) or in groups of unrelated yet cooperative individuals (pleometrosis). Pleometrotic queens display an associated reduction in aggression. To understand the proximate drivers behind this variation, we placed foundresses of the two populations into social environments with queens from the same or the alternate population, and measured their behaviour and head gene expression profiles. A proportion of queens from both populations behaved aggressively, but haplometrotic queens were significantly more likely to perform aggressive acts, and conflict escalated more frequently in pairs of haplometrotic queens. Whole-head RNA sequencing revealed variation in gene expression patterns, with the two populations showing moderate differentiation in overall transcriptional profile, suggesting that genetic differences underlie the two founding strategies. The largest detected difference, however, was associated with aggression, regardless of queen founding type. Several modules of coregulated genes, involved in metabolism, immune system and neuronal function, were found to be upregulated in highly aggressive queens. Conversely, nonaggressive queens exhibited a striking pattern of upregulation in chemosensory genes. Our results highlight that the social phenotypes of cooperative vs. solitary nest founding tap into a set of gene regulatory networks that seem to govern aggression level. We also present a number of highly connected hub genes associated with aggression, providing opportunity to further study the genetic underpinnings of social conflict and tolerance.
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http://dx.doi.org/10.1111/mec.13700DOI Listing
August 2016

Genetic architecture of key social trait differs significantly between primitive and advanced eusocial species.

Authors:
Jürgen Gadau

Proc Natl Acad Sci U S A 2015 Nov 30;112(45):13755-6. Epub 2015 Oct 30.

School of Life Sciences, Arizona State University, Tempe, AZ 85287

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http://dx.doi.org/10.1073/pnas.1519065112DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4653205PMC
November 2015

Phylogeography of Pogonomyrmex barbatus and P. rugosus harvester ants with genetic and environmental caste determination.

Ecol Evol 2015 Jul 25;5(14):2798-826. Epub 2015 Jun 25.

USDA-ARS Carl Hayden Bee Research Center Tucson, Arizona, 85719 ; Center for Insect Science, University of Arizona Tucson, Arizona, 85721.

We present a phylogeographic study of at least six reproductively isolated lineages of new world harvester ants within the Pogonomyrmex barbatus and P. rugosus species group. The genetic and geographic relationships within this clade are complex: Four of the identified lineages show genetic caste determination (GCD) and are divided into two pairs. Each pair has evolved under a mutualistic system that necessitates sympatry. These paired lineages are dependent upon one another because their GCD requires interlineage matings for the production of F1 hybrid workers, and intralineage matings are required to produce queens. This GCD system maintains genetic isolation among these interdependent lineages, while simultaneously requiring co-expansion and emigration as their distributions have changed over time. It has also been demonstrated that three of these four GCD lineages have undergone historical hybridization, but the narrower sampling range of previous studies has left questions on the hybrid parentage, breadth, and age of these groups. Thus, reconstructing the phylogenetic and geographic history of this group allows us to evaluate past insights and hypotheses and to plan future inquiries in a more complete historical biogeographic context. Using mitochondrial DNA sequences sampled across most of the morphospecies' ranges in the U.S.A. and Mexico, we conducted a detailed phylogeographic study. Remarkably, our results indicate that one of the GCD lineage pairs has experienced a dramatic range expansion, despite the genetic load and fitness costs of the GCD system. Our analyses also reveal a complex pattern of vicariance and dispersal in Pogonomyrmex harvester ants that is largely concordant with models of late Miocene, Pliocene, and Pleistocene range shifts among various arid-adapted taxa in North America.
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http://dx.doi.org/10.1002/ece3.1507DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4541987PMC
July 2015

The genomes of two key bumblebee species with primitive eusocial organization.

Genome Biol 2015 Apr 24;16:76. Epub 2015 Apr 24.

Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, 14040-901, Ribeirão Preto, Brazil.

Background: The shift from solitary to social behavior is one of the major evolutionary transitions. Primitively eusocial bumblebees are uniquely placed to illuminate the evolution of highly eusocial insect societies. Bumblebees are also invaluable natural and agricultural pollinators, and there is widespread concern over recent population declines in some species. High-quality genomic data will inform key aspects of bumblebee biology, including susceptibility to implicated population viability threats.

Results: We report the high quality draft genome sequences of Bombus terrestris and Bombus impatiens, two ecologically dominant bumblebees and widely utilized study species. Comparing these new genomes to those of the highly eusocial honeybee Apis mellifera and other Hymenoptera, we identify deeply conserved similarities, as well as novelties key to the biology of these organisms. Some honeybee genome features thought to underpin advanced eusociality are also present in bumblebees, indicating an earlier evolution in the bee lineage. Xenobiotic detoxification and immune genes are similarly depauperate in bumblebees and honeybees, and multiple categories of genes linked to social organization, including development and behavior, show high conservation. Key differences identified include a bias in bumblebee chemoreception towards gustation from olfaction, and striking differences in microRNAs, potentially responsible for gene regulation underlying social and other traits.

Conclusions: These two bumblebee genomes provide a foundation for post-genomic research on these key pollinators and insect societies. Overall, gene repertoires suggest that the route to advanced eusociality in bees was mediated by many small changes in many genes and processes, and not by notable expansion or depauperation.
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http://dx.doi.org/10.1186/s13059-015-0623-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4414376PMC
April 2015

Transposable element islands facilitate adaptation to novel environments in an invasive species.

Nat Commun 2014 Dec 16;5:5495. Epub 2014 Dec 16.

Institut für Zoologie, Universität Regensburg, 93053 Regensburg, Germany.

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 elements (TEs) in adaptive evolution. Accumulations of TEs (TE islands) comprising 7.18% of the genome evolve faster than other regions with regard to single-nucleotide variants, gene/exon duplications and deletions and gene homology. A non-random distribution of gene families, larvae/adult specific gene expression and signs of differential methylation in TE islands indicate intragenomic differences in regulation, evolutionary rates and coalescent effective population size. Our study reveals a tripartite interplay between TEs, life history and adaptation in an invasive species.
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http://dx.doi.org/10.1038/ncomms6495DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4284661PMC
December 2014

Evolution of the insect desaturase gene family with an emphasis on social Hymenoptera.

Mol Biol Evol 2015 Feb 24;32(2):456-71. Epub 2014 Nov 24.

School of Life Sciences, Arizona State University.

Desaturase genes are essential for biological processes, including lipid metabolism, cell signaling, and membrane fluidity regulation. Insect desaturases are particularly interesting for their role in chemical communication, and potential contribution to speciation, symbioses, and sociality. Here, we describe the acyl-CoA desaturase gene families of 15 insects, with a focus on social Hymenoptera. Phylogenetic reconstruction revealed that the insect desaturases represent an ancient gene family characterized by eight subfamilies that differ strongly in their degree of conservation and frequency of gene gain and loss. Analyses of genomic organization showed that five of these subfamilies are represented in a highly microsyntenic region conserved across holometabolous insect taxa, indicating an ancestral expansion during early insect evolution. In three subfamilies, ants exhibit particularly large expansions of genes. Despite these expansions, however, selection analyses showed that desaturase genes in all insect lineages are predominantly undergoing strong purifying selection. Finally, for three expanded subfamilies, we show that ants exhibit variation in gene expression between species, and more importantly, between sexes and castes within species. This suggests functional differentiation of these genes and a role in the regulation of reproductive division of labor in ants. The dynamic pattern of gene gain and loss of acyl-CoA desaturases in ants may reflect changes in response to ecological diversification and an increased demand for chemical signal variability. This may provide an example of how gene family expansions can contribute to lineage-specific adaptations through structural and regulatory changes acting in concert to produce new adaptive phenotypes.
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http://dx.doi.org/10.1093/molbev/msu315DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4298175PMC
February 2015

Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality.

Genome Res 2013 Aug 1;23(8):1235-47. Epub 2013 May 1.

Department of Cell and Developmental Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA.

Genomes of eusocial insects code for dramatic examples of phenotypic plasticity and social organization. We compared the genomes of seven ants, the honeybee, and various solitary insects to examine whether eusocial lineages share distinct features of genomic organization. Each ant lineage contains ∼4000 novel genes, but only 64 of these genes are conserved among all seven ants. Many gene families have been expanded in ants, notably those involved in chemical communication (e.g., desaturases and odorant receptors). Alignment of the ant genomes revealed reduced purifying selection compared with Drosophila without significantly reduced synteny. Correspondingly, ant genomes exhibit dramatic divergence of noncoding regulatory elements; however, extant conserved regions are enriched for novel noncoding RNAs and transcription factor-binding sites. Comparison of orthologous gene promoters between eusocial and solitary species revealed significant regulatory evolution in both cis (e.g., Creb) and trans (e.g., fork head) for nearly 2000 genes, many of which exhibit phenotypic plasticity. Our results emphasize that genomic changes can occur remarkably fast in ants, because two recently diverged leaf-cutter ant species exhibit faster accumulation of species-specific genes and greater divergence in regulatory elements compared with other ants or Drosophila. Thus, while the "socio-genomes" of ants and the honeybee are broadly characterized by a pervasive pattern of divergence in gene composition and regulation, they preserve lineage-specific regulatory features linked to eusociality. We propose that changes in gene regulation played a key role in the origins of insect eusociality, whereas changes in gene composition were more relevant for lineage-specific eusocial adaptations.
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http://dx.doi.org/10.1101/gr.155408.113DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3730098PMC
August 2013

Behavioural and genetic analyses of Nasonia shed light on the evolution of sex pheromones.

Nature 2013 Feb 13;494(7437):345-8. Epub 2013 Feb 13.

Centre for Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig, 53113 Bonn, Germany.

Sex pheromones play a pivotal role in the communication of many sexually reproducing organisms. Accordingly, speciation is often accompanied by pheromone diversification enabling proper mate finding and recognition. Current theory implies that chemical signals are under stabilizing selection by the receivers who thereby maintain the integrity of the signals. How the tremendous diversity of sex pheromones seen today evolved is poorly understood. Here we unravel the genetics of a newly evolved pheromone phenotype in wasps and present results from behavioural experiments indicating how the evolution of a new pheromone component occurred in an established sender-receiver system. We show that male Nasonia vitripennis evolved an additional pheromone compound differing only in its stereochemistry from a pre-existing one. Comparative behavioural studies show that conspecific females responded neutrally to the new pheromone phenotype when it evolved. Genetic mapping and gene knockdown show that a cluster of three closely linked genes accounts for the ability to produce this new pheromone phenotype. Our data suggest that new pheromone compounds can persist in a sender's population, without being selected against by the receiver and without the receiver having a pre-existing preference for the new pheromone phenotype, by initially remaining unperceived. Our results thus contribute valuable new insights into the evolutionary mechanisms underlying the diversification of sex pheromones. Furthermore, they indicate that the genetic basis of new pheromone compounds can be simple, allowing them to persist long enough in a population for receivers to evolve chemosensory adaptations for their exploitation.
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http://dx.doi.org/10.1038/nature11838DOI Listing
February 2013

Fine-scale mapping of the Nasonia genome to chromosomes using a high-density genotyping microarray.

G3 (Bethesda) 2013 Feb 1;3(2):205-15. Epub 2013 Feb 1.

Department of Biology, University of Rochester, Rochester, New York 14627, USA.

Nasonia, a genus of four closely related parasitoid insect species, is a model system for genetic research. Their haplodiploid genetics (haploid males and diploid females) and interfertile species are advantageous for the genetic analysis of complex traits and the genetic basis of species differences. A fine-scale genomic map is an important tool for advancing genetic studies in this system. We developed and used a hybrid genotyping microarray to generate a high-resolution genetic map that covers 79% of the sequenced genome of Nasonia vitripennis. The microarray is based on differential hybridization of species-specific oligos between N. vitripennis and Nasonia giraulti at more than 20,000 markers spanning the Nasonia genome. The map places 729 scaffolds onto the five linkage groups of Nasonia, including locating many smaller scaffolds that would be difficult to map by other means. The microarray was used to characterize 26 segmental introgression lines containing chromosomal regions from one species in the genetic background of another. These segmental introgression lines have been used for rapid screening and mapping of quantitative trait loci involved in species differences. Finally, the microarray is extended to bulk-segregant analysis and genotyping of other Nasonia species combinations. These resources should further expand the usefulness of Nasonia for studies of the genetic basis and architecture of complex traits and speciation.
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http://dx.doi.org/10.1534/g3.112.004739DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3564981PMC
February 2013

Mechanisms and dynamics of orphan gene emergence in insect genomes.

Genome Biol Evol 2013 ;5(2):439-55

Institute for Evolution and Biodiversity, University of Muenster, Muenster, Germany.

Orphan genes are defined as genes that lack detectable similarity to genes in other species and therefore no clear signals of common descent (i.e., homology) can be inferred. Orphans are an enigmatic portion of the genome because their origin and function are mostly unknown and they typically make up 10% to 30% of all genes in a genome. Several case studies demonstrated that orphans can contribute to lineage-specific adaptation. Here, we study orphan genes by comparing 30 arthropod genomes, focusing in particular on seven recently sequenced ant genomes. This setup allows analyzing a major metazoan taxon and a comparison between social Hymenoptera (ants and bees) and nonsocial Diptera (flies and mosquitoes). First, we find that recently split lineages undergo accelerated genomic reorganization, including the rapid gain of many orphan genes. Second, between the two insect orders Hymenoptera and Diptera, orphan genes are more abundant and emerge more rapidly in Hymenoptera, in particular, in leaf-cutter ants. With respect to intragenomic localization, we find that ant orphan genes show little clustering, which suggests that orphan genes in ants are scattered uniformly over the genome and between nonorphan genes. Finally, our results indicate that the genetic mechanisms creating orphan genes-such as gene duplication, frame-shift fixation, creation of overlapping genes, horizontal gene transfer, and exaptation of transposable elements-act at different rates in insects, primates, and plants. In Formicidae, the majority of orphan genes has their origin in intergenic regions, pointing to a high rate of de novo gene formation or generalized gene loss, and support a recently proposed dynamic model of frequent gene birth and death.
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http://dx.doi.org/10.1093/gbe/evt009DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3590893PMC
September 2013

Patterns of DNA methylation in development, division of labor and hybridization in an ant with genetic caste determination.

PLoS One 2012 3;7(8):e42433. Epub 2012 Aug 3.

Department of Biology, Earlham College, Richmond, Indiana, United States of America.

Background: DNA methylation is a common regulator of gene expression, including acting as a regulator of developmental events and behavioral changes in adults. Using the unique system of genetic caste determination in Pogonomyrmex barbatus, we were able to document changes in DNA methylation during development, and also across both ancient and contemporary hybridization events.

Methodology/principal Findings: Sodium bisulfite sequencing demonstrated in vivo methylation of symmetric CG dinucleotides in P. barbatus. We also found methylation of non-CpG sequences. This validated two bioinformatics methods for predicting gene methylation, the bias in observed to expected ratio of CpG dinucleotides and the density of CpG/TpG single nucleotide polymorphisms (SNP). Frequencies of genomic DNA methylation were determined for different developmental stages and castes using ms-AFLP assays. The genetic caste determination system (GCD) is probably the product of an ancestral hybridization event between P. barbatus and P. rugosus. Two lineages obligately co-occur within a GCD population, and queens are derived from intra-lineage matings whereas workers are produced from inter-lineage matings. Relative DNA methylation levels of queens and workers from GCD lineages (contemporary hybrids) were not significantly different until adulthood. Virgin queens had significantly higher relative levels of DNA methylation compared to workers. Worker DNA methylation did not vary among developmental stages within each lineage, but was significantly different between the currently hybridizing lineages. Finally, workers of the two genetic caste determination lineages had half as many methylated cytosines as workers from the putative parental species, which have environmental caste determination.

Conclusions/significance: These results suggest that DNA methylation may be a conserved regulatory mechanism moderating division of labor in both bees and ants. Current and historic hybridization appear to have altered genomic methylation levels suggesting a possible link between changes in overall DNA methylation and the origin and regulation of genetic caste determination in P. barbatus.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0042433PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3411777PMC
January 2013

Quantitative trait locus analysis in haplodiploid hymenoptera.

Methods Mol Biol 2012 ;871:313-28

School of Life Sciences, Arizona State University, Tempe, AZ 58285, USA.

This article describes QTL analyses for solitary (Nasonia, a parasitoid wasp) and social hymenopteran species (honeybee and bumblebee). These exemplar QTL analyses determined the genetic basis of morphological, behavioral, and colony level traits. Mapping populations were derived either from lab crosses between highly inbred strains (Nasonia spp.), lab crosses of individuals caught in the field (bumblebees), or offspring from artificially inseminated queens from a managed honeybee population. Using these examples, we demonstrate the importance of a clear understanding of the life history, breeding, and reproductive system of the organism used for a QTL analysis, e.g., haplo-diploidy or reproductive division of labor in social insects. We lead the reader step by step through the process of multiple QTL analyses and describe potential problems and roadblocks (e.g., data handling, statistical, and biological problems) that can obscure or severely impair the results of a QTL study and how to detect and deal with those problems.In particular, we provide a way to empirically estimate the Beavis effect for a larger QTL mapping population and how to estimate a more accurate value of the explained phenotypic variance of each detected QTL using a resampling procedure.
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http://dx.doi.org/10.1007/978-1-61779-785-9_16DOI Listing
August 2012

Developmental evolution in social insects: regulatory networks from genes to societies.

J Exp Zool B Mol Dev Evol 2012 May;318(3):159-69

Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania, USA.

The evolution and development of complex phenotypes in social insect colonies, such as queen-worker dimorphism or division of labor, can, in our opinion, only be fully understood within an expanded mechanistic framework of Developmental Evolution. Conversely, social insects offer a fertile research area in which fundamental questions of Developmental Evolution can be addressed empirically. We review the concept of gene regulatory networks (GRNs) that aims to fully describe the battery of interacting genomic modules that are differentially expressed during the development of individual organisms. We discuss how distinct types of network models have been used to study different levels of biological organization in social insects, from GRNs to social networks. We propose that these hierarchical networks spanning different organizational levels from genes to societies should be integrated and incorporated into full GRN models to elucidate the evolutionary and developmental mechanisms underlying social insect phenotypes. Finally, we discuss prospects and approaches to achieve such an integration.
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http://dx.doi.org/10.1002/jez.b.22001DOI Listing
May 2012

The genomic impact of 100 million years of social evolution in seven ant species.

Trends Genet 2012 Jan 5;28(1):14-21. Epub 2011 Oct 5.

School of Life Sciences, Arizona State University, Tempe, AZ 85287, USA.

Ants (Hymenoptera, Formicidae) represent one of the most successful eusocial taxa in terms of both their geographic distribution and species number. The publication of seven ant genomes within the past year was a quantum leap for socio- and ant genomics. The diversity of social organization in ants makes them excellent model organisms to study the evolution of social systems. Comparing the ant genomes with those of the honeybee, a lineage that evolved eusociality independently from ants, and solitary insects suggests that there are significant differences in key aspects of genome organization between social and solitary insects, as well as among ant species. Altogether, these seven ant genomes open exciting new research avenues and opportunities for understanding the genetic basis and regulation of social species, and adaptive complex systems in general.
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http://dx.doi.org/10.1016/j.tig.2011.08.005DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3314025PMC
January 2012

The genome sequence of the leaf-cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle.

PLoS Genet 2011 Feb 10;7(2):e1002007. Epub 2011 Feb 10.

Department of Bacteriology, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.

Leaf-cutter ants are one of the most important herbivorous insects in the Neotropics, harvesting vast quantities of fresh leaf material. The ants use leaves to cultivate a fungus that serves as the colony's primary food source. This obligate ant-fungus mutualism is one of the few occurrences of farming by non-humans and likely facilitated the formation of their massive colonies. Mature leaf-cutter ant colonies contain millions of workers ranging in size from small garden tenders to large soldiers, resulting in one of the most complex polymorphic caste systems within ants. To begin uncovering the genomic underpinnings of this system, we sequenced the genome of Atta cephalotes using 454 pyrosequencing. One prediction from this ant's lifestyle is that it has undergone genetic modifications that reflect its obligate dependence on the fungus for nutrients. Analysis of this genome sequence is consistent with this hypothesis, as we find evidence for reductions in genes related to nutrient acquisition. These include extensive reductions in serine proteases (which are likely unnecessary because proteolysis is not a primary mechanism used to process nutrients obtained from the fungus), a loss of genes involved in arginine biosynthesis (suggesting that this amino acid is obtained from the fungus), and the absence of a hexamerin (which sequesters amino acids during larval development in other insects). Following recent reports of genome sequences from other insects that engage in symbioses with beneficial microbes, the A. cephalotes genome provides new insights into the symbiotic lifestyle of this ant and advances our understanding of host-microbe symbioses.
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http://dx.doi.org/10.1371/journal.pgen.1002007DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3037820PMC
February 2011

Draft genome of the red harvester ant Pogonomyrmex barbatus.

Proc Natl Acad Sci U S A 2011 Apr 31;108(14):5667-72. Epub 2011 Jan 31.

Department of Biology, Earlham College, Richmond, IN 47374, USA.

We report the draft genome sequence of the red harvester ant, Pogonomyrmex barbatus. The genome was sequenced using 454 pyrosequencing, and the current assembly and annotation were completed in less than 1 y. Analyses of conserved gene groups (more than 1,200 manually annotated genes to date) suggest a high-quality assembly and annotation comparable to recently sequenced insect genomes using Sanger sequencing. The red harvester ant is a model for studying reproductive division of labor, phenotypic plasticity, and sociogenomics. Although the genome of P. barbatus is similar to other sequenced hymenopterans (Apis mellifera and Nasonia vitripennis) in GC content and compositional organization, and possesses a complete CpG methylation toolkit, its predicted genomic CpG content differs markedly from the other hymenopterans. Gene networks involved in generating key differences between the queen and worker castes (e.g., wings and ovaries) show signatures of increased methylation and suggest that ants and bees may have independently co-opted the same gene regulatory mechanisms for reproductive division of labor. Gene family expansions (e.g., 344 functional odorant receptors) and pseudogene accumulation in chemoreception and P450 genes compared with A. mellifera and N. vitripennis are consistent with major life-history changes during the adaptive radiation of Pogonomyrmex spp., perhaps in parallel with the development of the North American deserts.
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http://dx.doi.org/10.1073/pnas.1007901108DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3078412PMC
April 2011

Draft genome of the globally widespread and invasive Argentine ant (Linepithema humile).

Proc Natl Acad Sci U S A 2011 Apr 31;108(14):5673-8. Epub 2011 Jan 31.

Department of Biology and Computer Science, San Francisco State University, San Francisco, CA 94132, USA.

Ants are some of the most abundant and familiar animals on Earth, and they play vital roles in most terrestrial ecosystems. Although all ants are eusocial, and display a variety of complex and fascinating behaviors, few genomic resources exist for them. Here, we report the draft genome sequence of a particularly widespread and well-studied species, the invasive Argentine ant (Linepithema humile), which was accomplished using a combination of 454 (Roche) and Illumina sequencing and community-based funding rather than federal grant support. Manual annotation of >1,000 genes from a variety of different gene families and functional classes reveals unique features of the Argentine ant's biology, as well as similarities to Apis mellifera and Nasonia vitripennis. Distinctive features of the Argentine ant genome include remarkable expansions of gustatory (116 genes) and odorant receptors (367 genes), an abundance of cytochrome P450 genes (>110), lineage-specific expansions of yellow/major royal jelly proteins and desaturases, and complete CpG DNA methylation and RNAi toolkits. The Argentine ant genome contains fewer immune genes than Drosophila and Tribolium, which may reflect the prominent role played by behavioral and chemical suppression of pathogens. Analysis of the ratio of observed to expected CpG nucleotides for genes in the reproductive development and apoptosis pathways suggests higher levels of methylation than in the genome overall. The resources provided by this genome sequence will offer an abundance of tools for researchers seeking to illuminate the fascinating biology of this emerging model organism.
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http://dx.doi.org/10.1073/pnas.1008617108DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3078359PMC
April 2011

Origin and evolution of the dependent lineages in the genetic caste determination system of Pogonomyrmex ants.

Evolution 2011 Mar 17;65(3):869-84. Epub 2010 Nov 17.

Department of Biology, University of Oulu 90014, Linnanmaa P.O. Box 3000, Finland.

Hybridizing harvester ants of the Pogonomyrmex barbatus/rugosus complex have an exceptional genetic caste determination (GCD) mechanism. We combined computer simulations, population genomics, and linkage mapping using >1000 nuclear AFLP markers and a partial mtDNA sequence to explore the genetic architecture and origin of the dependent lineages. Our samples included two pairs of hybridizing lineages, and the mitochondrial and nuclear data showed contradicting affinities between them. Clustering of individual genotypes based on nuclear markers indicated some exceptions to the general GCD system, that is, interlineage hybrid genes as well as some pure-line workers. A genetic linkage map of P. rugosus showed one of the highest recombination rates ever measured in insects (14.0 cM/Mb), supporting the view that social insects are characterized by high recombination rates. The population data had 165 markers in which sibling pairs showed a significant genetic difference depending on the caste. The differences were scattered in the genome; 13 linkage groups had loci with F(ST)>0.9 between the hybridizing lineages J1 and J2.The mapping results and the population data indicate that the dependent lineages have been initially formed through hybridization at different points in time but the role of introgression has been insignificant in their later evolution.
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http://dx.doi.org/10.1111/j.1558-5646.2010.01170.xDOI Listing
March 2011
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