Mit der ETH-Medaille zeichnet die ETH Zürich herausragende Master- und Doktorarbeiten aus. Elena Gimmi durfte den Preis am letzten Freitag, 24. Januar 2025 für ihre Dissertation entgegennehmen. Die Auszeichnung würdigt Gimmis Erkenntnisse über den Einfluss bakterieller «Bodyguards» auf die Koevolution der schwarzen Bohnenblattlaus, einem wichtigen Schädling im Lebensmittelanbau, und ihrem natürlichen Feind, der Schlupfwespe.
Als Doktorandin am Wasserforschungsinstitut Eawag nahm Elena Gimmi die Dreiecksbeziehung zwischen schwarzer Bohnenblattlaus (Aphis fabae), der winzigen Schlupfwespe Lysiphlebus fabarum und dem Bakterium Hamiltonella defensa unter die Lupe. Betreut wurde sie von Prof. Christoph Vorburger und Prof. Jukka Jokela. Die Forschungsgruppe von Vorburger verfolgt das Zusammenspiel der drei unterschiedlichen Partner schon seit Jahren. In Laboruntersuchungen zeigte sich, dass das Bakterium H. defensa als Symbiont im Körper der Blattläuse lebt: Es wird von diesen mit «Kost und Logis» versorgt und schützt sie im Gegenzug gegen die parasitischen Schlupfwespen, deren Larven die Läuse auffressen. Vermutlich produzieren die Bakterien Giftstoffe, welche die Eier der Wespen töten.
Umfassende Datenreihe aus dem Feld – Corona zum Trotz
Elena Gimmi hat die Ergebnisse aus der Grundlagenforschung nun erstmals unter natürlichen Bedingungen an wilden Populationen getestet und sich insbesondere angesehen, welche Muster und saisonalen Dynamiken bei der Resistenz der Blattläuse zu Tage treten. «Ich fand es spannend und herausfordernd, bekannte Laborresultate mit Beobachtungen aus der realen Welt zu vergleichen», so die Umweltbiologin.
Das Kernstück von Gimmis Arbeit bildete dabei eine gross angelegte, über zwei Jahre dauernde Feldstudie. In drei verschiedenen Gebieten rund um Zürich hat Gimmi monatlich die Häufigkeit der Bakterien in den Blattläusen verfolgt. Zudem hat sie über die gleiche Zeit untersucht, wie sich das Risiko der Blattläuse, von den Wespen parasitiert zu werden, veränderte. «Beim Start war klar, dass im Grunde sehr vieles dabei schief gehen könnte. Aber dank einer Kombination aus Hartnäckigkeit und Glück gingen die ursprünglichen Pläne für meine Arbeit ziemlich gut auf», blickt Gimmi zurück.
«Der betriebene Aufwand im Feld war enorm. Entsprechend hoch ist die Qualität der gesammelten Daten, aus denen wir viele neue und wichtige Erkenntnisse gewinnen konnten.» Christoph Vorburger
Christoph Vorburger betont: «Der betriebene Aufwand für die Untersuchungen im Feld war enorm. Entsprechend hoch ist die Qualität der gesammelten Daten, aus denen wir viele neue und wichtige Erkenntnisse gewinnen konnten.» Das wichtige zweite Jahr des Feldprojekts war dabei durch die Corona-Pandemie ernsthaft gefährdet. Kurzerhand richtete die Forscherin mit Hilfe ihres Vaters ein kleines Insektenlabor zu Hause ein und engagierte ihren Bruder als Feldassistenten. Die Datenreihe blieb dadurch lückenlos und sieht aus, als hätte nie ein Lockdown stattgefunden. Vorburger: «Das war wirklich eine grosse Leistung, und ich bin auch Elenas Familie sehr dankbar für die Unterstützung.»
Christoph Vorburger und Elena Gimmi (Foto: Eawag).
Überraschender Einfluss der Umgebungstemperatur
Gimmis Daten liefern neues und zum Teil überraschendes Wissen über die Beziehung der drei ungleichen Partner. So konnte die Forscherin unter anderem zeigen, dass die Häufigkeit der Bakterien in den Blattlauspopulationen im Jahresverlauf schwankte – und dass die Umgebungstemperatur einen viel grösseren Einfluss darauf hatte als vermutet. Das heisst: Je wärmer es ist, desto mehr der bakteriellen «Bodyguards» wurden gefunden und desto grösser dürfte auch die Widerstandfähigkeit der Blattläuse sein. Dies könnte darauf hindeuten, dass die Klimaerwärmung den Einsatz parasitischer Wespen in der biologischen Schädlingsbekämpfung beeinträchtigt.
Eine Blattlauswespe attackiert eine Blattlaus. Darunter sieht man Blattläuse, die bereits von den Wespen parasitiert wurden. (Foto: Christoph Vorburger, Eawag).
Forschung wird an der Eawag weitergeführt
Christoph Vorburger engagiert sich über 20 Jahren in der akademischen Lehre. Er bezeichnet die Auszeichnung als sehr verdient: «Wir hatten wirklich grosses Glück, dass wir Elena für dieses Projekt gewinnen konnten. Zu ihrem Talent kommen Gewissenhaftigkeit, Sorgfalt und eine gesunde Portion Ehrgeiz, was ihr half, das ambitionierte Projekt zielstrebig voranzutreiben. Gleichzeitig ist sie eine hervorragende Teamplayerin. Es ist zudem beeindruckend, dass bereits kurz nach ihrer Promotion ausnahmslos alle Kapitel ihrer Arbeit in hochstehenden Originalpublikationen veröffentlicht waren.»
Gimmis Ergebnisse bilden auch die Grundlage für ein Folgeprojekt an der Eawag, das vom Schweizerischen Nationalfonds bis ins Jahr 2027 unterstützt wird.
Titelbild: Elena Gimmi mit ETH Rektor Günther Dissertori (Foto: Alessandro della Bella).
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description => protected'Defensive symbiosis describes the interaction between two species where one species protects the other from dangers, in exchange for another benefit. Pr otagonist of this thesis is <em>Hamiltonella defensa</em>, a vertically tran smitted bacterial endosymbiont of aphids. <em>H. defensa</em> can defend its aphid host against parasitoid wasps and in return profits from nutrients an d shelter inside the aphid body. In wild aphid populations, <em>H. defensa</ em> often occurs at intermediate prevalence, that is, some aphid individuals carry the bacteria, but others do not. This might be explained by balancing selection, as carrying <em>H. defensa</em> has not only benefits but also c osts for the aphid. The tripartite interaction between aphids, <em>H. defens a</em> and aphid parasitoids is considered a model system for symbiont-drive n hostparasite coevolution and has been studied from various angles during t he past twenty years. However, there is still a lack of data on the role of defensive symbiosis in the ecology and evolution of natural communities. Wit h my PhD work, I sought to improve on that by studying patterns and dynamics of <em>H. defensa</em>-conferred resistance in the field. [...]<br /><br /> Symbiose beschreibt das enge Zusammenleben zweier unterschiedlicher Organism en. In sogenannten defensiven Symbiosen bietet eine Art der anderen Schutz o der Resistenz gegen Feinde oder Gefahren. Protagonist der vorliegenden Arbei t ist <em>Hamiltonella defensa</em>, ein endosymbiotisches Bakterium, das im Körper von Blattläusen lebt und von einer zur nächsten Blattlausgenerati on vererbt wird. <em>H. defensa</em> kann Blattläusen Resistenz gegen paras itische Schlupfwespen verleihen, welche wichtige natürliche Feinde der Läu se sind. <em>H. defensa</em> ist also ein defensiver Symbiont von Blattläus en. Im Gegenzug profitiert <em>H. defensa</em> von 'Kost und Logis' im Inner n der Blattlaus. In natürlichen Blattlauspopulationen leben meist einige In dividuen mit, andere ohn...' (2465 chars)
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description => protected'Different host plants represent ecologically dissimilar environments for phy tophagous insects. The resulting divergent selection can promote the evoluti on of specialized host races, provided that gene flow is reduced between pop ulations feeding on different plants. In black bean aphids belonging to the <em>Aphis fabae</em> complex, several morphologically cryptic taxa have been described based on their distinct host plant preferences. However, host cho ice and mate choice are largely decoupled in these insects: they are host-al ternating and migrate between specific summer host plants and shared winter hosts, with mating occurring on the shared hosts. This provides a yearly opp ortunity for gene flow among aphids using different summer hosts, and raises the question if and to what extent the ecologically defined taxa are reprod uctively isolated. Here, we analyzed a geographically and temporally structu red dataset of microsatellite genotypes from <em>A. fabae</em> that were mos tly collected from their main winter host <em>Euonymus europaeus</em>, and a dditionally from another winter host and fourteen summer hosts. The data rev eals multiple, strongly differentiated genetic clusters, which differ in the ir association with different summer and winter hosts. The clusters also dif fer in the frequency of infection with two heritable, facultative endosymbio nts, separately hinting at reproductive isolation and divergent ecological s election. Furthermore, we found evidence for occasional hybridization among genetic clusters, with putative hybrids collected more frequently in spring than in autumn. This suggests that similar to host races in other phytophago us insects, both prezygotic and postzygotic barriers including selection aga inst hybrids maintain genetic differentiation among <em>A. fabae</em> taxa, despite a common mating habitat.' (1856 chars)
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description => protected'Host–parasite coevolution is mediated by genetic interactions between the antagonists and may lead to reciprocal adaptation. In the black bean aphid, <em>Aphis fabae fabae</em>, resistance to parasitoids can be conferred by th e heritable bacterial endosymbiont <em>Hamiltonella defensa</em>. <em>H. def ensa</em> has been shown to be variably protective against different parasit oid species, and different genotypes of the black bean aphid's main parasito id <em>Lysiphlebus fabarum</em>. However, these results were obtained using haphazard combinations of laboratory-reared insect lines with different orig ins, making it unclear how representative they are of natural, locally (co)a dapted communities. We therefore comprehensively sampled the parasitoids of a natural <em>A. f. fabae</em> population and measured the ability of the fi ve most abundant species to parasitize aphids carrying the locally prevalent <em>H. defensa</em> haplotypes. <em>H. defensa</em> provided resistance onl y against the dominant parasitoid <em>L. fabarum</em> (70% of all parasitoid s), but not against less abundant parasitoids, and resistance to <em>L. faba rum</em> acted in a genotype-specific manner (G × G interactions betwee n <em>H. defensa</em> and <em>L. fabarum</em>). These results confirm that s trong species- and genotype-specificity of symbiont-conferred resistance is indeed a hallmark of wild <em>A. f. fabae</em> populations, and they are con sistent with symbiont-mediated adaptation of aphids to the parasitoids posin g the highest risk.' (1539 chars)
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description => protected'Parasite-mediated selection can rapidly drive up resistance levels in host p opulations, but fixation of resistance traits may be prevented by costs of r esistance. Black bean aphids (<em>Aphis fabae</em>) benefit from increased r esistance to parasitoids when carrying the defensive bacterial endosymbiont <em>Hamiltonella defensa</em>. However, due to fitness costs that come with symbiont infection, symbiont-conferred resistance may result in either a net benefit or a net cost to the aphid host, depending on parasitoid presence a s well as on the general ecological context. Balancing selection may therefo re explain why in natural aphid populations, <em>H. defensa</em> is often found at intermediate frequencies. Here we present a 2-year field study wher e we set out to look for signatures of balancing selection in natural aphid populations. We collected temporally well-resolved data on the prevalence of <em>H. defensa</em> in <em>A. f. fabae</em> and estimated the risk im posed by parasitoids using sentinel hosts. Despite a marked and consistent e arly-summer peak in parasitism risk, and significant changes in symbiont pre valence over time, we found just a weak correlation between parasitism risk and <em>H. defensa</em> frequency dynamics. <em>H. defensa</em> prevalen ce in the populations under study was, in fact, better explained by the numb er of heat days that previous aphid generations were exposed to. Our study g rants an unprecedentedly well-resolved insight into the dynamics of endosymb iont and parasitoid communities of <em>A. f. fabae</em> populations, and it adds to a growing body of empirical evidence suggesting that not only pa rasitism risk, but rather multifarious selection is shaping <em>H. defensa </em> prevalence in the wild.' (1777 chars)
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description => protected'The dynamics of coevolution between hosts and parasites are influenced by th eir genetic interactions. Highly specific interactions, where the outcome of an infection depends on the precise combination of host and parasite genoty pes (G × G interactions), have the potential to maintain genetic variatio n by inducing negative frequency-dependent selection. The importance of this effect also rests on whether such interactions are consistent across differ ent environments or modified by environmental variation (G × G × E int eraction). In the black bean aphid, <em>Aphis fabae</em>, resistance to its parasitoid <em>Lysiphlebus fabarum</em> is largely determined by the possess ion of a heritable bacterial endosymbiont, <em>Hamiltonella defensa</em>, wi th strong G × G interactions between <em>H</em>. <em>defensa</em> and <e m>L</em>. <em>fabarum</em>. A key environmental factor in this system is th e host plant on which the aphid feeds. Here, we exposed genetically identica l aphids harbouring three different strains of <em>H</em>. <em>defensa</em> to three asexual genotypes of <em>L</em>. <em>fabarum</em> and measured pa rasitism success on three common host plants of <em>A</em>. <em>fabae</em>, namely <em>Vicia faba</em>, <em>Chenopodium album</em> and <em>Beta vulgari s</em>. As expected, we observed the pervasive G × G interaction between <em>H</em>. <em>defensa</em> and <em>L</em>. <em>fabarum</em>, but despite strong main effects of the host plants on average rates of parasitism, this interaction was not altered significantly by the host plant environment (n o G × G × E interaction). The symbiont-conferred specificity of resist ance is thus likely to mediate the coevolution of <em>A</em>. <em>fabae</em > and <em>L</em>. <em>fabarum</em>, even when played out across diverse hos t plants of the aphid.' (1846 chars)
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Defensive symbiosis in the wild - patterns and dynamics of symbiont-conferred resistance in natural host-parasitoid communities
Defensive symbiosis describes the interaction between two species where one species protects the other from dangers, in exchange for another benefit. Protagonist of this thesis is Hamiltonella defensa, a vertically transmitted bacterial endosymbiont of aphids. H. defensa can defend its aphid host against parasitoid wasps and in return profits from nutrients and shelter inside the aphid body. In wild aphid populations, H. defensa often occurs at intermediate prevalence, that is, some aphid individuals carry the bacteria, but others do not. This might be explained by balancing selection, as carrying H. defensa has not only benefits but also costs for the aphid. The tripartite interaction between aphids, H. defensa and aphid parasitoids is considered a model system for symbiont-driven hostparasite coevolution and has been studied from various angles during the past twenty years. However, there is still a lack of data on the role of defensive symbiosis in the ecology and evolution of natural communities. With my PhD work, I sought to improve on that by studying patterns and dynamics of H. defensa-conferred resistance in the field. [...]
Symbiose beschreibt das enge Zusammenleben zweier unterschiedlicher Organismen. In sogenannten defensiven Symbiosen bietet eine Art der anderen Schutz oder Resistenz gegen Feinde oder Gefahren. Protagonist der vorliegenden Arbeit ist Hamiltonella defensa, ein endosymbiotisches Bakterium, das im Körper von Blattläusen lebt und von einer zur nächsten Blattlausgeneration vererbt wird. H. defensa kann Blattläusen Resistenz gegen parasitische Schlupfwespen verleihen, welche wichtige natürliche Feinde der Läuse sind. H. defensa ist also ein defensiver Symbiont von Blattläusen. Im Gegenzug profitiert H. defensa von 'Kost und Logis' im Innern der Blattlaus. In natürlichen Blattlauspopulationen leben meist einige Individuen mit, andere ohne symbiotische H. defensa. Das wird damit erklärt, dass H. defensa für die Läuse nicht nur Vorteile bringt, sondern auch Kosten. Diese Kosten kommen besonders dann zur Geltung, wenn keine Schlupfwespen die Blattläuse bedrohen, weil die Resistenz gegen solche dann nichts bringt, H. defensa aber weiterhin von den Blattlausressourcen zehrt. Je nach Situation sind also Blattläuse mit oder solche ohne H. defensa fitter. [...]
Gimmi, E. L. (2023) Defensive symbiosis in the wild - patterns and dynamics of symbiont-conferred resistance in natural host-parasitoid communities, 175 p, doi:10.3929/ethz-b-000617575, Institutional Repository
Ecological divergence despite common mating sites: genotypes and symbiotypes shed light on cryptic diversity in the black bean aphid species complex
Different host plants represent ecologically dissimilar environments for phytophagous insects. The resulting divergent selection can promote the evolution of specialized host races, provided that gene flow is reduced between populations feeding on different plants. In black bean aphids belonging to the Aphis fabae complex, several morphologically cryptic taxa have been described based on their distinct host plant preferences. However, host choice and mate choice are largely decoupled in these insects: they are host-alternating and migrate between specific summer host plants and shared winter hosts, with mating occurring on the shared hosts. This provides a yearly opportunity for gene flow among aphids using different summer hosts, and raises the question if and to what extent the ecologically defined taxa are reproductively isolated. Here, we analyzed a geographically and temporally structured dataset of microsatellite genotypes from A. fabae that were mostly collected from their main winter host Euonymus europaeus, and additionally from another winter host and fourteen summer hosts. The data reveals multiple, strongly differentiated genetic clusters, which differ in their association with different summer and winter hosts. The clusters also differ in the frequency of infection with two heritable, facultative endosymbionts, separately hinting at reproductive isolation and divergent ecological selection. Furthermore, we found evidence for occasional hybridization among genetic clusters, with putative hybrids collected more frequently in spring than in autumn. This suggests that similar to host races in other phytophagous insects, both prezygotic and postzygotic barriers including selection against hybrids maintain genetic differentiation among A. fabae taxa, despite a common mating habitat.
Gimmi, E.; Wallisch, J.; Vorburger, C. (2024) Ecological divergence despite common mating sites: genotypes and symbiotypes shed light on cryptic diversity in the black bean aphid species complex, Heredity, 132, 320-330, doi:10.1038/s41437-024-00687-0, Institutional Repository
High specificity of symbiont-conferred resistance in an aphid-parasitoid field community
Host–parasite coevolution is mediated by genetic interactions between the antagonists and may lead to reciprocal adaptation. In the black bean aphid, Aphis fabae fabae, resistance to parasitoids can be conferred by the heritable bacterial endosymbiont Hamiltonella defensa. H. defensa has been shown to be variably protective against different parasitoid species, and different genotypes of the black bean aphid's main parasitoid Lysiphlebus fabarum. However, these results were obtained using haphazard combinations of laboratory-reared insect lines with different origins, making it unclear how representative they are of natural, locally (co)adapted communities. We therefore comprehensively sampled the parasitoids of a natural A. f. fabae population and measured the ability of the five most abundant species to parasitize aphids carrying the locally prevalent H. defensa haplotypes. H. defensa provided resistance only against the dominant parasitoid L. fabarum (70% of all parasitoids), but not against less abundant parasitoids, and resistance to L. fabarum acted in a genotype-specific manner (G × G interactions between H. defensa and L. fabarum). These results confirm that strong species- and genotype-specificity of symbiont-conferred resistance is indeed a hallmark of wild A. f. fabae populations, and they are consistent with symbiont-mediated adaptation of aphids to the parasitoids posing the highest risk.
Gimmi, E.; Vorburger, C. (2024) High specificity of symbiont-conferred resistance in an aphid-parasitoid field community, Journal of Evolutionary Biology, 37(2), 162-170, doi:10.1093/jeb/voad013, Institutional Repository
Defensive symbiosis in the wild: seasonal dynamics of parasitism risk and symbiont‐conferred resistance
Parasite-mediated selection can rapidly drive up resistance levels in host populations, but fixation of resistance traits may be prevented by costs of resistance. Black bean aphids (Aphis fabae) benefit from increased resistance to parasitoids when carrying the defensive bacterial endosymbiont Hamiltonella defensa. However, due to fitness costs that come with symbiont infection, symbiont-conferred resistance may result in either a net benefit or a net cost to the aphid host, depending on parasitoid presence as well as on the general ecological context. Balancing selection may therefore explain why in natural aphid populations, H. defensa is often found at intermediate frequencies. Here we present a 2-year field study where we set out to look for signatures of balancing selection in natural aphid populations. We collected temporally well-resolved data on the prevalence of H. defensa in A. f. fabae and estimated the risk imposed by parasitoids using sentinel hosts. Despite a marked and consistent early-summer peak in parasitism risk, and significant changes in symbiont prevalence over time, we found just a weak correlation between parasitism risk and H. defensa frequency dynamics. H. defensa prevalence in the populations under study was, in fact, better explained by the number of heat days that previous aphid generations were exposed to. Our study grants an unprecedentedly well-resolved insight into the dynamics of endosymbiont and parasitoid communities of A. f. fabae populations, and it adds to a growing body of empirical evidence suggesting that not only parasitism risk, but rather multifarious selection is shaping H. defensa prevalence in the wild.
Gimmi, E.; Wallisch, J.; Vorburger, C. (2023) Defensive symbiosis in the wild: seasonal dynamics of parasitism risk and symbiont‐conferred resistance, Molecular Ecology, 32(14), 4063-4077, doi:10.1111/mec.16976, Institutional Repository
Strong genotype-by-genotype interactions between aphid-defensive symbionts and parasitoids persist across different biotic environments
The dynamics of coevolution between hosts and parasites are influenced by their genetic interactions. Highly specific interactions, where the outcome of an infection depends on the precise combination of host and parasite genotypes (G × G interactions), have the potential to maintain genetic variation by inducing negative frequency-dependent selection. The importance of this effect also rests on whether such interactions are consistent across different environments or modified by environmental variation (G × G × E interaction). In the black bean aphid, Aphis fabae, resistance to its parasitoid Lysiphlebus fabarum is largely determined by the possession of a heritable bacterial endosymbiont, Hamiltonella defensa, with strong G × G interactions between H. defensa and L. fabarum. A key environmental factor in this system is the host plant on which the aphid feeds. Here, we exposed genetically identical aphids harbouring three different strains of H. defensa to three asexual genotypes of L. fabarum and measured parasitism success on three common host plants of A. fabae, namely Vicia faba, Chenopodium album and Beta vulgaris. As expected, we observed the pervasive G × G interaction between H. defensa and L. fabarum, but despite strong main effects of the host plants on average rates of parasitism, this interaction was not altered significantly by the host plant environment (no G × G × E interaction). The symbiont-conferred specificity of resistance is thus likely to mediate the coevolution of A. fabae and L. fabarum, even when played out across diverse host plants of the aphid.
Gimmi, E.; Vorburger, C. (2021) Strong genotype-by-genotype interactions between aphid-defensive symbionts and parasitoids persist across different biotic environments, Journal of Evolutionary Biology, 34(12), 1944-1953, doi:10.1111/jeb.13953, Institutional Repository
