Antagonistic coevolution; aphids; Aphis fabae; clones; endosymbionts; experimental evolution; Hamiltonella defensa; local adaptation; Lysiphlebus fabarum; parasitoids; resistance; thelytoky; biological control; coevolution; infection; parthenogenesis; symbiosis
Rothacher Lukas, Ferrer-Suay Mar, Vorburger Christoph (2016), Bacterial endosymbionts protect aphids in the field and alter parasitoid community composition, in ECOLOGY
, 97(7), 1712-1723.
Cayetano Luis, Rothacher Lukas, Simon Jean-Christophe, Vorburger Christoph (2015), Cheaper is not always worse: strongly protective isolates of a defensive symbiont are less costly to the aphid host., in Proceedings. Biological sciences
, 282(1799), 20142333-20142333.
Cayetano Luis, Vorburger Christoph (2015), Symbiont-conferred protection against Hymenopteran parasitoids in aphids: how general is it?, in ECOLOGICAL ENTOMOLOGY
, 40(1), 85-93.
Wilson Alex C. C., Delgado Ryan N., Vorburger Christoph (2014), Biased Transmission of Sex Chromosomes in the Aphid Myzus persicae Is Not Associated with Reproductive Mode, in PLOS ONE
, 9(12), e0118524.
Vorburger Christoph (2014), The evolutionary ecology of symbiont-conferred resistance to parasitoids in aphids., in Insect science
, 21(3), 251-64.
Vorburger C (2014), Thelytoky and sex determination in the hymenoptera: mutual constraints., in Sexual development : genetics, molecular biology, evolution, endocrinology, embryology, and patholog
, 8(1-3), 50-8.
Vorburger Christoph, Ganesanandamoorthy Pravin, Kwiatkowski Marek (2013), Comparing constitutive and induced costs of symbiont-conferred resistance to parasitoids in aphids, in ECOLOGY AND EVOLUTION
, 3(3), 706-713.
Cayetano Luis, Vorburger Christoph (2013), Effects of heat shock on resistance to parasitoids and on life history traits in an aphid/endosymbiont system, in PLoS One
, 8, e75966.
Cayetano L., Vorburger C. (2013), Genotype-by-genotype specificity remains robust to average temperature variation in an aphid/endosymbiont/parasitoid system, in JOURNAL OF EVOLUTIONARY BIOLOGY
, 26(7), 1603-1610.
Schar Sami, Vorburger Christoph (2013), Host specialization of parasitoids and their hyperparasitoids on a pair of syntopic aphid species, in BULLETIN OF ENTOMOLOGICAL RESEARCH
, 103(5), 530-537.
Razmjou J, Vorburger C, Mohammadi M, Hassanpour M (2012), Influence of vermicompost and cucumber cultivar on population growth of Aphis gossypii Glover, in JOURNAL OF APPLIED ENTOMOLOGY
, 136(8), 568-575.
Kwiatkowski M, Vorburger C (2012), Modeling the Ecology of Symbiont-Mediated Protection against Parasites, in AMERICAN NATURALIST
, 179(5), 595-605.
Kwiatkowski M, Engelstadter J, Vorburger C (2012), On Genetic Specificity in Symbiont-Mediated Host-Parasite Coevolution, in PLOS COMPUTATIONAL BIOLOGY
, 8(8), e1002633-e1002633.
Gehrer L, Vorburger C (2012), Parasitoids as vectors of facultative bacterial endosymbionts in aphids, in BIOLOGY LETTERS
, 8(4), 613-615.
Rouchet R., Vorburger C. (2012), Strong specificity in the interaction between parasitoids and symbiont-protected hosts, in JOURNAL OF EVOLUTIONARY BIOLOGY
, 25(11), 2369-2375.
Sandrock C, Razmjou J, Vorburger C (2011), Climate effects on life cycle variation and population genetic architecture of the black bean aphid, Aphis fabae, in Molecular Ecology
, 20(19), 4165-4181.
Engelstädter J, Sandrock C, Vorburger C (2011), Contagious parthenogenesis, automixis, and a sex determination meltdown, in Evolution
, 65(2), 501-511.
Sandrock C, Schirrmeister BE, Vorburger C (2011), Evolution of reproductive mode variation and host associations in a sexual-asexual complex of aphid parasitoids, in BMC EVOLUTIONARY BIOLOGY
, 11, 348-348.
Hansen Allison K, Vorburger Christoph, Moran Nancy A (2011), Genomic basis of endosymbiont-conferred protection against an insect parasitoid., in Genome research
, 22, 106-114.
Vorburger C, Gouskov A (2011), Only helpful when required: A longevity cost of harbouring defensive symbionts, in Journal of Evolutionary Biology
, 24(7), 1611-1617.
Sandrock C, Vorburger C (2011), Single-Locus Recessive Inheritance of Asexual Reproduction in a Parasitoid Wasp, in CURRENT BIOLOGY
, 21(5), 433-437.
Vorburger Christoph (2011), Versteckte Helfer: Symbionten und ihr Einfluss auf Wirt-Parasit-Beziehungen bei Insekten, in Vierteljahresschrift der Naturforschenden Gesellschaft in Zürich
, 156(3/4), 89-97.
Vorburger C, Gehrer L, Rodriguez P (2010), A strain of the bacterial symbiont Regiella insecticola protects aphids against parasitoids, in Biology Letters
, 6(1), 109-111.
Sandrock C, Gouskov A, Vorburger C (2010), Ample genetic variation but no evidence for genotype specificity in an all-parthenogenetic host-parasitoid interaction, in Journal of Evolutionary Biology
, 23(3), 578-585.
Vorburger C, Eugster B, Villiger J, Wimmer C (2010), Host genotype affects the relative success of competing lines of aphid parasitoids under superparasitism, in Ecological Entomology
, 35(1), 77-83.
Razmjou J, Vorburger C, Moharramipour S, Mirhoseini SZ, Fathipour Y (2010), Host-associated differentiation and evidence for sexual reproduction in Iranian populations of the cotton aphid, Aphis gossypii, in ENTOMOLOGIA EXPERIMENTALIS ET APPLICATA
, 134(2), 191-199.
Castañeda LE, Sandrock C, Vorburger C (2010), Variation and covariation of life history traits in aphids are related to infection with the facultative bacterial endosymbiont Hamiltonella defensa, in Biological Journal of the Linnean Society
, 100(1), 237-247.
Bieri APS, HÄrri SA, Vorburger C, MÜller CB (2009), Aphid genotypes vary in their response to the presence of fungal endosymbionts in host plants, in Journal of Evolutionary Biology
, 22(8), 1775-1780.
Vorburger C, Sandrock C, Gouskov A, Castañeda LE, Ferrari J (2009), Genotypic variation and the role of defensive endosymbionts in an all-parthenogenetic host-parasitoid interaction, in Evolution
, 63(6), 1439-1450.
Schmid M, Sieber R, Zimmermann Y-S, Vorburger C, Development, specificity and sublethal effects of symbiont-conferred resistance to parasitoids in aphids, in Functional Ecology
Antagonistic coevolution between hosts and parasites may result in open-ended cycles of adaptation and counter-adaptation. These genetic dynamics have been suggested to be a driving force behind many important evolutionary phenomena, in particular the maintenance of genetic variation, or even sex. Reciprocal selection is particularly strong in insect host-parasitoid systems because these are a matter of life or death. Parasitoids only survive if they can overcome host defences; hosts are invariably killed if their defences fail. It was recently discovered in aphids that some genotypes rely on 'helpers' in the form of facultative endosymbiotic bacteria for defence against their hymenopteran parasitoids. One of these symbionts, aptly named Hamiltonella defensa, can provide very strong protection against parasitoid wasps. Presumably, parasitoids succumb to toxins encoded by a bacteriophage within the H. defensa genome. These are fascinating discoveries and they challenge existing models of host-parasitoid coevolution. While there is a solid theoretical framework of host-parasitoid coevolution between two species based on interaction loci, we lack such a framework for symbiont-mediated coevolution. Empirically, the interaction between aphids and their facultative endosymbionts is currently under intensive investigation, but the role of parasitoids is largely ignored or at best treated as a constant. However, just as parasitoids select for improved defences in hosts, the host's acquisition of defensive endosymbionts selects for counterdefences in parasitoids. Therefore, I propose a project to clear these deficiencies. We will develop models describing the expected dynamics of such symbiont-mediated coevolution and empirically examine this process from the level of individual genotypes up to the level of the biological community, using the black bean aphid, Aphis fabae, and its parasitoid Lysiphlebus fabarum as a study system. The project builds on our ongoing work on this recently established study system, which we chose because uniquely among aphid parasitoids, L. fabarum occurs in arrhenotokous (sexual) as well as thelytokous (parthenogenetic) populations. This offers exciting opportunities for experimentation. Thelytoky allows us to extract individual parasitoid genotypes from the field and faithfully replicate them in the lab, while arrhenotoky makes the system amenable for the powerful approaches of artificial selection and experimental evolution. Our previous work has shown that, just like the pea aphid, in which this association was first described, A. fabae may be infected with H. defensa and thereby enjoy strong protection against L. fabarum. We also found that the rate of infection with H. defensa varies geographically, and that different genotypes of L. fabarum vary in their ability to parasitize H. defensa-bearing aphids. These findings indicate that L. fabarum is under selection and does have the potential to adapt to the presence of H. defensa in its host, yet the process is entirely unstudied so far.The project consists of five parts. In the first part, we will develop new models to derive the expected frequency of defensive symbionts in host populations and to evaluate their effect on reciprocal selection between hosts and parasitoids. In the second part, we will test in the field whether parasitoids are locally adapted to endosymbiont-conferred resistance, and we will use an experimental evolution approach to assess the potential of parasitoids to adapt to defensive symbionts, and analyse correlated responses that might constrain such adaptation. The third and fourth parts are concerned with effects of the biotic and abiotic environment on our host-parasitoid system. We will test if high temperatures might interfere with bacterial protection, and we will assess how the community context, i.e. the availability of alternative hosts or parasitoids, respectively, affects reciprocal selection between A. fabae and L. fabarum. Finally, we will test whether ectoparasitic mites may act as vectors of bacterial endosymbionts in aphids, a yet undescribed route of horizontal transmission. This is important because the ease of horizontal transmission is a key element in this system. It determines whether selection by parasitoids may lead to the rapid spread of endosymbionts among previously uninfected hosts or whether it primarily favours clones already associated with endosymbionts.This project will contribute novel models of host-parasite coevolution that explicitly account for resistance provided by defensive symbionts, and it will be the first to empirically study parasitoid adaptation to defensive symbionts in hosts. It will thus represent an important step towards a better understanding of host-parasite coevolution. I also expect this work to yield applied benefits, because aphid parasitoids are frequently used for biological control of pest aphids. It is now clear that aphid infection with defensive symbionts can seriously compromise the efficiency of biocontrol. This could be avoided if it was possible to improve the parasitoids' counterdefences by artificial selection. The project will show whether this is a viable strategy.