Parallel and costly changes to cellular immunity underlie the evolution of parasitoid resistance in three Drosophila species

被引:24
作者
McGonigle, John E. [1 ]
Leitao, Alexandre B. [1 ]
Ommeslag, Sarah [1 ,2 ]
Smith, Sophie [1 ]
Day, Jonathan P. [1 ]
Jiggins, Francis M. [1 ]
机构
[1] Univ Cambridge, Dept Genet, Cambridge, England
[2] Hogesch Gent, Fac Mens & Welzijn, Ghent, Belgium
基金
英国自然环境研究理事会; 英国生物技术与生命科学研究理事会; 欧洲研究理事会;
关键词
ASOBARA-TABIDA; LEPTOPILINA-HETEROTOMA; ENCAPSULATION ABILITY; COMPETITIVE ABILITY; MELANOGASTER LARVAE; NATURAL-POPULATION; GENETIC CHANGE; TRADE-OFF; SELECTION; COEVOLUTION;
D O I
10.1371/journal.ppat.1006683
中图分类号
Q93 [微生物学];
学科分类号
071005 ; 100705 ;
摘要
A priority for biomedical research is to understand the causes of variation in susceptibility to infection. To investigate genetic variation in a model system, we used flies collected from single populations of three different species of Drosophila and artificially selected them for resistance to the parasitoid wasp Leptopilina boulardi, and found that survival rates increased 3 to 30 fold within 6 generations. Resistance in all three species involves a large increase in the number of the circulating hemocytes that kill parasitoids. However, the different species achieve this in different ways, with D. melanogaster moving sessile hemocytes into circulation while the other species simply produce more cells. Therefore, the convergent evolution of the immune phenotype has different developmental bases. These changes are costly, as resistant populations of all three species had greatly reduced larval survival. In all three species resistance is only costly when food is in short supply, and resistance was rapidly lost from D. melanogaster populations when food is restricted. Furthermore, evolving resistance to L. boulardi resulted in cross-resistance against other parasitoids. Therefore, whether a population evolves resistance will depend on ecological conditions including food availability and the presence of different parasite species.
引用
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页数:20
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共 74 条
[1]   Phylogeny of six African Leptopilina species (Hymenoptera: Cynipoidea, Figitidae), parasitoids of Drosophila, with description of three new species [J].
Allemand, R ;
Lemaître, C ;
Frey, F ;
Boulétreau, M ;
Vavre, F ;
Nordlander, G ;
van Alphen, J ;
Carton, Y .
ANNALES DE LA SOCIETE ENTOMOLOGIQUE DE FRANCE, 2002, 38 (04) :319-332
[2]   Population genomics:: Whole-genome analysis of polymorphism and divergence in Drosophila simulans [J].
Begun, David J. ;
Holloway, Alisha K. ;
Stevens, Kristian ;
Hillier, LaDeana W. ;
Poh, Yu-Ping ;
Hahn, Matthew W. ;
Nista, Phillip M. ;
Jones, Corbin D. ;
Kern, Andrew D. ;
Dewey, Colin N. ;
Pachter, Lior ;
Myers, Eugene ;
Langley, Charles H. .
PLOS BIOLOGY, 2007, 5 (11) :2534-2559
[3]   The Evolution of Resistance to a Parasite Is Determined by Resources [J].
Boots, Mike .
AMERICAN NATURALIST, 2011, 178 (02) :214-220
[4]   OVARIAN ACTIVITY AND REPRODUCTIVE POTENTIAL IN A NATURAL-POPULATION OF DROSOPHILA-MELANOGASTER [J].
BOULETREAU, J .
OECOLOGIA, 1978, 35 (03) :319-342
[5]   Drosophila cellular immunity against parasitoids [J].
Carton, Y ;
Nappi, AJ .
PARASITOLOGY TODAY, 1997, 13 (06) :218-227
[6]   Genetics of anti-parasite resistance in invertebrates [J].
Carton, Y ;
Nappi, AJ ;
Poirie, M .
DEVELOPMENTAL AND COMPARATIVE IMMUNOLOGY, 2005, 29 (01) :9-32
[7]   GENETIC-VARIABILITY OF HOST-PARASITE RELATIONSHIP TRAITS - UTILIZATION OF ISOFEMALE LINES IN A DROSOPHILA-SIMULANS PARASITIC WASP [J].
CARTON, Y ;
CAPY, P ;
NAPPI, AJ .
GENETICS SELECTION EVOLUTION, 1989, 21 (04) :437-446
[8]   Insect immune resistance to parasitoids [J].
Carton, Yves ;
Poirie, Marylene ;
Nappi, Anthony J. .
INSECT SCIENCE, 2008, 15 (01) :67-87
[9]   Ability of European parasitoids (Hymenoptera) to control a new invasive Asiatic pest, Drosophila suzukii [J].
Chabert, Stan ;
Allemand, Roland ;
Poyet, Mathilde ;
Eslin, Patrice ;
Gibert, Patricia .
BIOLOGICAL CONTROL, 2012, 63 (01) :40-47
[10]   Variability of venom components in immune suppressive parasitoid wasps: From a phylogenetic to a population approach [J].
Colinet, Dominique ;
Mathe-Hubert, Hugo ;
Allemand, Roland ;
Gatti, Jean-Luc ;
Poirie, Marylene .
JOURNAL OF INSECT PHYSIOLOGY, 2013, 59 (02) :205-212