SYMBIOCONTROL

SEVENTH FRAMEWORK PROGRAMME

Marie Curie Actions – People – Marie Curie International Outgoing Fellowship
Full Title: The role of the bacterial symbiont Cardinum in shaping the ecology and evolution of an insect parasitoid wasp: fundamental studies and implications for biological control of plant pests.
Acronym: SYMBIOCONTROL
Grant Agreement Number: PIOF-GA-2012-327425
Duration of the project: 36 months
Beneficiary CONSIGLIO NAZIONALE DELLE RICERCHE
Name of Researcher: Dr. Marco GEBIOLA
Nationality of the Researcher: Italy
Scientist in Charge (Return phase): Dr. Massimo GIORGINI
Scientist in Charge (Outgoing phase): Prof. Martha S. HUNTER

Summary: Arthropods can be infected by facultative symbionts with diverse effects on host reproduction and fitness. Cytoplasmic reproductive incompatibility (CI) appears to be the most prevalent effect, and is caused by two unrelated bacteria: Wolbachia and the recently discovered Cardinium. Bacteria-induced CI is of special interest as it may play a role in reproductive isolation and speciation of insect hosts. Reproductive barriers can arise also by incompatibility due to hybridization (HI). Cardinium-induced CI occurs in the parasitoid wasp Encarsia pergandiella, a natural enemy of agricultural pests, and may have important implications for its use in biological control. Indeed, CI may lead to a suppression of population growth when populations with a different infection status interact. Nevertheless, understanding the role of heritable bacterial symbionts in the biology of natural enemies has not yet been widely recognized as a key research objective of biocontrol programs. The project aims to: 1) evaluate the role of CI-inducing Cardinium in reproductive isolation and competitive interactions of E. pergandiella populations; 2) evaluate the potentially disruptive effects of an introduction of a biological control agent that is partially reproductively isolated (via CI or HI) on biological control provided by an established, conspecific parasitoid population. The project will provide the first study of the cytological mechanisms of Cardinium-induced CI, and will use fundamental studies of CI and HI to develop quantitative models of population interactions, and then test model predictions in population cage and greenhouse studies. The data collected will be used to develop a conceptual model for biocontrol agents with different geographical ranges and reproductive incompatibilities in order to understand the consequences for biological control.

PUBLISHED RESULTS

We first focused on E. inaron, a parasitoid wasp that harbours both Wolbachia and Cardinium. Known then as E. partenopea, E. inaron was introduced to the USA in the late 1980s from populations collected in Italy and Israel for the biological control of an ornamental tree pest, the ash whitefly Siphoninus phillyreae. We studied natural populations from the USA, the Mediterranean and the Middle East, and from a Cardinium-infected laboratory culture established from Italy, with the aims of characterizing these populations genetically, testing reproductive isolation, determining infection status and symbiont role in their native and introduced range. We showed that the two Encarsia populations introduced to the USA are genetically distinct, reproductively isolated, have different symbionts and different host–symbiont interactions, and can be considered distinct biological species. One (E. inaron) is doubly infected by Wolbachia and Cardinium, while only Cardinium is present in the other (E. partenopea). Cardinium strains in the two species are distinct, although closely related, and crossing tests indicate that the Cardinium infecting E. partenopea induces CI. These results led to a retelling of a successful biological control story, and serves as a cautionary tale for future introductions of natural enemies for classical biocontrol projects. The study has been published on Biological Journal of the Linnean Society and is available at http://onlinelibrary.wiley.com/doi/10.1111/bij.12648/abstract.

We have solved the taxonomy of the Encarsia pergandiella species complex, the first fundamental step for the success of the SYMBIOCONTROL project. We integrated molecular and morphometric analyses, and compared laboratory cultures and field collected specimens with available type material. We showed that neither of the two focal species of the project, both commonly referred to as E. pergandiella, a species from Texas that is infected by a Cytoplasmic Incompatibility-inducing strain of the bacterial symbiont Cardinium, and a species from California (later introduced to Europe and the Middle East as biocontrol agent) uninfected by symbionts, correspond to E. pergandiella. The two species resulted to be new to science and we have described them as Encarsia suzannae (Cardinium-infected) and Encarsia gennaroi (uninfected). We also showed that a third species from Brazil infected by a parthenogenesis-inducing strain of Cardinium corresponds to Encarsia tabacivora. The revision has been published on Systematic Entomology and is available at: http://onlinelibrary.wiley.com/doi/10.1111/syen.12187/full.

We have added a contribution to the longstanding debate on the role that bacterial symbionts able to manipulate the reproduction of their hosts play in driving or accelerating speciation, by means of bidirectional or unidirectional Cytoplasmic Incompatibility (CI). Thus far the only experimental evidences were from the symbiont Wolbachia infecting the model insects Drosophila and Nasonia. We have studied reproductive isolation between two sibling species of parasitic wasps, Encarsia suzannae, which is infected by a strain of the symbiont Cardinium that induces CI, and the uninfected Encarsia gennaroi. We have shown that pre-zygotic isolation is still incipient, but post-zygotic isolation is complete. Hybrid offspring is greatly reduced in the interspecific CI cross and by hybrid inviability due to genetic incompatibilities in the reciprocal cross. F1 hybrids are almost completely sterile in both crosses. Therefore, CI and asymmetrical hybrid incompatibilities act as complementary isolating mechanisms. We propose a model in which CI reduces gene flow in one direction, and a symbiont sweep results in accelerated mitochondrial evolution, negative interactions and hybrid incompatibilities. The study has been published on Evolution and is available here: http://onlinelibrary.wiley.com/doi/10.1111/evo.13037/full. Additional information on this study is presented at https://www.researchgate.net/publication/306255052 where videos are available showing the mating behavior in crosses between the two sibling species in no-choice, female choice, male choice, and multiple choice crossing tests.


Research staff

Research activity

  • Green technologies