TY - JOUR A1 - Käch, Heidi A1 - Mathe-Hubert, Hugo A1 - Dennis, Alice B. A1 - Vorburger, Christoph T1 - Rapid evolution of symbiont-mediated resistance compromises biological control of aphids by parasitoids JF - Evolutionary applications N2 - There is growing interest in biological control as a sustainable and environmentally friendly way to control pest insects. Aphids are among the most detrimental agricultural pests worldwide, and parasitoid wasps are frequently employed for their control. The use of asexual parasitoids may improve the effectiveness of biological control because only females kill hosts and because asexual populations have a higher growth rate than sexuals. However, asexuals may have a reduced capacity to track evolutionary change in their host populations. We used a factorial experiment to compare the ability of sexual and asexual populations of the parasitoid Lysiphlebus fabarum to control caged populations of black bean aphids (Aphis fabae) of high and low clonal diversity. The aphids came from a natural population, and one-third of the aphid clones harbored Hamiltonella defensa, a heritable bacterial endosymbiont that increases resistance to parasitoids. We followed aphid and parasitoid population dynamics for 3months but found no evidence that the reproductive mode of parasitoids affected their effectiveness as biocontrol agents, independent of host clonal diversity. Parasitoids failed to control aphids in most cases, because their introduction resulted in strong selection for clones protected by H.defensa. The increasingly resistant aphid populations escaped control by parasitoids, and we even observed parasitoid extinctions in many cages. The rapid evolution of symbiont-conferred resistance in turn imposed selection on parasitoids. In cages where asexual parasitoids persisted until the end of the experiment, they became dominated by a single genotype able to overcome the protection provided by H.defensa. Thus, there was evidence for parasitoid counteradaptation, but it was generally too slow for parasitoids to regain control over aphid populations. It appears that when pest aphids possess defensive symbionts, the presence of parasitoid genotypes able to overcome symbiont-conferred resistance is more important for biocontrol success than their reproductive mode. KW - aphids KW - Aphis fabae KW - biological control KW - defensive symbiosis KW - Hamiltonella defensa KW - Lysiphlebus fabarum KW - parasitoid KW - resistance Y1 - 2018 U6 - https://doi.org/10.1111/eva.12532 SN - 1752-4571 VL - 11 IS - 2 SP - 220 EP - 230 PB - Wiley CY - Hoboken ER - TY - JOUR A1 - Matthey-Doret, Cyril A1 - van der Kooi, Casper J. A1 - Jeffries, Daniel L. A1 - Bast, Jens A1 - Dennis, Alice B. A1 - Vorburger, Christoph A1 - Schwander, Tanja T1 - Mapping of Multiple Complementary Sex Determination Loci in a Parasitoid Wasp JF - Genome biology and evolution N2 - Sex determination has evolved in a variety of ways and can depend on environmental and genetic signals. A widespread form of genetic sex determination is haplodiploidy, where unfertilized, haploid eggs develop into males and fertilized diploid eggs into females. One of the molecular mechanisms underlying haplodiploidy in Hymenoptera, the large insect order comprising ants, bees, and wasps, is complementary sex determination (CSD). In species with CSD, heterozygosity at one or several loci induces female development. Here, we identify the genomic regions putatively underlying multilocus CSD in the parasitoid wasp Lysiphlebus fabarum using restriction -site associated DNA sequencing. By analyzing segregation patterns at polymorphic sites among 331 diploid males and females, we identify up to four CSD candidate regions, all on different chromosomes. None of the candidate regions feature evidence for homology with the csd gene from the honey bee, the only species in which CSD has been characterized, suggesting that CSD in L. fabarum is regulated via a novel molecular mechanism. Moreover, no homology is shared between the candidate loci, in contrast to the idea that multilocus CSD should emerge from duplications of an ancestral single -locus system. Taken together, our results suggest that the molecular mechanisms underlying CSD in Hymenoptera are not conserved between species, raising the question as to whether CSD may have evolved multiple times independently in the group. KW - hymenoptera KW - sex determination KW - Lysiphlebus fabarum KW - CSD Y1 - 2019 U6 - https://doi.org/10.1093/gbe/evz219 SN - 1759-6653 VL - 11 IS - 10 SP - 2954 EP - 2962 PB - Oxford Univ. Press CY - Oxford ER - TY - GEN A1 - Dennis, Alice B. A1 - Ballesteros, Gabriel I. A1 - Robin, Stéphanie A1 - Schrader, Lukas A1 - Bast, Jens A1 - Berghöfer, Jan A1 - Beukeboom, Leo W. A1 - Belghazi, Maya A1 - Bretaudeau, Anthony A1 - Buellesbach, Jan A1 - Cash, Elizabeth A1 - Colinet, Dominique A1 - Dumas, Zoé A1 - Errbii, Mohammed A1 - Falabella, Patrizia A1 - Gatti, Jean-Luc A1 - Geuverink, Elzemiek A1 - Gibson, Joshua D. A1 - Hertaeg, Corinne A1 - Hartmann, Stefanie A1 - Jacquin-Joly, Emmanuelle A1 - Lammers, Mark A1 - Lavandero, Blas I. A1 - Lindenbaum, Ina A1 - Massardier-Galata, Lauriane A1 - Meslin, Camille A1 - Montagné, Nicolas A1 - Pak, Nina A1 - Poirié, Marylène A1 - Salvia, Rosanna A1 - Smith, Chris R. A1 - Tagu, Denis A1 - Tares, Sophie A1 - Vogel, Heiko A1 - Schwander, Tanja A1 - Simon, Jean-Christophe A1 - Figueroa, Christian C. A1 - Vorburger, Christoph A1 - Legeai, Fabrice A1 - Gadau, Jürgen T1 - Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum T2 - Postprints der Universität Potsdam : Mathematisch-Naturwissenschaftliche Reihe N2 - 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. T3 - Zweitveröffentlichungen der Universität Potsdam : Mathematisch-Naturwissenschaftliche Reihe - 989 KW - Parasitoid wasp KW - Aphid host KW - Aphidius ervi KW - GC content KW - de novo genome assembly KW - DNA methylation loss KW - Chemosensory genes KW - Toll and Imd pathways KW - Venom proteins KW - Lysiphlebus fabarum Y1 - 2020 U6 - http://nbn-resolving.de/urn/resolver.pl?urn:nbn:de:kobv:517-opus4-476129 SN - 1866-8372 IS - 989 ER - TY - JOUR A1 - Dennis, Alice B. A1 - Ballesteros, Gabriel I. A1 - Robin, Stéphanie A1 - Schrader, Lukas A1 - Bast, Jens A1 - Berghöfer, Jan A1 - Beukeboom, Leo W. A1 - Belghazi, Maya A1 - Bretaudeau, Anthony A1 - Buellesbach, Jan A1 - Cash, Elizabeth A1 - Colinet, Dominique A1 - Dumas, Zoé A1 - Errbii, Mohammed A1 - Falabella, Patrizia A1 - Gatti, Jean-Luc A1 - Geuverink, Elzemiek A1 - Gibson, Joshua D. A1 - Hertaeg, Corinne A1 - Hartmann, Stefanie A1 - Jacquin-Joly, Emmanuelle A1 - Lammers, Mark A1 - Lavandero, Blas I. A1 - Lindenbaum, Ina A1 - Massardier-Galata, Lauriane A1 - Meslin, Camille A1 - Montagné, Nicolas A1 - Pak, Nina A1 - Poirié, Marylène A1 - Salvia, Rosanna A1 - Smith, Chris R. A1 - Tagu, Denis A1 - Tares, Sophie A1 - Vogel, Heiko A1 - Schwander, Tanja A1 - Simon, Jean-Christophe A1 - Figueroa, Christian C. A1 - Vorburger, Christoph A1 - Legeai, Fabrice A1 - Gadau, Jürgen T1 - Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum JF - BMC Genomics N2 - 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. KW - Parasitoid wasp KW - Aphid host KW - Aphidius ervi KW - Lysiphlebus fabarum KW - de novo genome assembly KW - DNA methylation loss KW - Chemosensory genes KW - Venom proteins KW - GC content KW - Toll and Imd pathways Y1 - 2020 U6 - https://doi.org/10.1186/s12864-020-6764-0 SN - 1471-2164 VL - 21 PB - BioMed Central CY - London ER - TY - JOUR A1 - Dennis, Alice B. A1 - Patel, Vilas A1 - Oliver, Kerry M. A1 - Vorburger, Christoph T1 - Parasitoid gene expression changes after adaptation to symbiont-protected hosts JF - Evolution N2 - Reciprocal selection between aphids, their protective endosymbionts, and the parasitoid wasps that prey upon them offers an opportunity to study the basis of their coevolution. We investigated adaptation to symbiont‐conferred defense by rearing the parasitoid wasp Lysiphlebus fabarum on aphids (Aphis fabae) possessing different defensive symbiont strains (Hamiltonella defensa). After ten generations of experimental evolution, wasps showed increased abilities to parasitize aphids possessing the H. defensa strain they evolved with, but not aphids possessing the other strain. We show that the two symbiont strains encode different toxins, potentially creating different targets for counter‐adaptation. Phenotypic and behavioral comparisons suggest that neither life‐history traits nor oviposition behavior differed among evolved parasitoid lineages. In contrast, comparative transcriptomics of adult female wasps identified a suite of differentially expressed genes among lineages, even when reared in a common, symbiont‐free, aphid host. In concurrence with the specificity of each parasitoid lineages’ infectivity, most differentially expressed parasitoid transcripts were also lineage‐specific. These transcripts are enriched with putative venom toxins and contain highly expressed, potentially defensive viral particles. Together, these results suggest that wild populations of L. fabarum employ a complicated offensive arsenal with sufficient genetic variation for wasps to adapt rapidly and specifically to their hosts’ microbial defenses. KW - Adaptation KW - experimental evolution KW - gene expression KW - Lysiphlebus fabarum KW - parasitoid KW - venom Y1 - 2017 U6 - https://doi.org/10.1111/evo.13333 SN - 0014-3820 SN - 1558-5646 VL - 71 SP - 2599 EP - 2617 PB - Wiley CY - Hoboken ER - TY - GEN A1 - Käch, Heidi A1 - Mathé-Hubert, Hugo A1 - Dennis, Alice B. A1 - Vorburger, Christoph T1 - Rapid evolution of symbiont-­mediated resistance compromises biological control of aphids by parasitoids T2 - Postprints der Universität Potsdam : Mathematisch-Naturwissenschaftliche Reihe N2 - There is growing interest in biological control as a sustainable and environmentally friendly way to control pest insects. Aphids are among the most detrimental agricultural pests worldwide, and parasitoid wasps are frequently employed for their control. The use of asexual parasitoids may improve the effectiveness of biological control because only females kill hosts and because asexual populations have a higher growth rate than sexuals. However, asexuals may have a reduced capacity to track evolutionary change in their host populations. We used a factorial experiment to compare the ability of sexual and asexual populations of the parasitoid Lysiphlebus fabarum to control caged populations of black bean aphids (Aphis fabae) of high and low clonal diversity. The aphids came from a natural population, and one-­third of the aphid clones harbored Hamiltonella defensa, a heritable bacterial endosymbiont that increases resistance to parasitoids. We followed aphid and parasitoid population dynamics for 3 months but found no evidence that the reproductive mode of parasitoids affected their effectiveness as biocontrol agents, independent of host clonal diversity. Parasitoids failed to control aphids in most cases, because their introduction resulted in strong selection for clones protected by H. defensa. The increasingly resistant aphid populations escaped control by parasitoids, and we even observed parasitoid extinctions in many cages. The rapid evolution of symbiont-­conferred resistance in turn imposed selection on parasitoids. In cages where asexual parasitoids persisted until the end of the experiment, they became dominated by a single genotype able to overcome the protection provided by H. defensa. Thus, there was evidence for parasitoid counteradaptation, but it was generally too slow for parasitoids to regain control over aphid populations. It appears that when pest aphids possess defensive symbionts, the presence of parasitoid genotypes able to overcome symbiont-­conferred resistance is more important for biocontrol success than their reproductive mode. T3 - Zweitveröffentlichungen der Universität Potsdam : Mathematisch-Naturwissenschaftliche Reihe - 620 KW - aphids KW - Aphis fabae KW - biological control KW - defensive symbiosis KW - Hamiltonella defensa KW - Lysiphlebus fabarum KW - parasitoid KW - resistance Y1 - 2019 U6 - http://nbn-resolving.de/urn/resolver.pl?urn:nbn:de:kobv:517-opus4-423542 SN - 1866-8372 IS - 620 ER -