Genotype-by-Environment Interactions and Adaptation to Local Temperature Affect Immunity and Fecundity in Drosophila melanogaster

Natural populations of most organisms harbor substantial genetic variation for resistance to infection. The continued existence of such variation is unexpected under simple evolutionary models that either posit direct and continuous natural selection on the immune system or an evolved life history “balance” between immunity and other fitness traits in a constant environment. However, both local adaptation to heterogeneous environments and genotype-by-environment interactions can maintain genetic variation in a species. In this study, we test Drosophila melanogaster genotypes sampled from tropical Africa, temperate northeastern North America, and semi-tropical southeastern North America for resistance to bacterial infection and fecundity at three different environmental temperatures. Environmental temperature had absolute effects on all traits, but there were also marked genotype-by-environment interactions that may limit the global efficiency of natural selection on both traits. African flies performed more poorly than North American flies in both immunity and fecundity at the lowest temperature, but not at the higher temperatures, suggesting that the African population is maladapted to low temperature. In contrast, there was no evidence for clinal variation driven by thermal adaptation within North America for either trait. Resistance to infection and reproductive success were generally uncorrelated across genotypes, so this study finds no evidence for a fitness tradeoff between immunity and fecundity under the conditions tested. Both local adaptation to geographically heterogeneous environments and genotype-by-environment interactions may explain the persistence of genetic variation for resistance to infection in natural populations.

[1]  A. Clark,et al.  The evolutionary costs of immunological maintenance and deployment , 2008, BMC Evolutionary Biology.

[2]  D. Promislow,et al.  The effects of temperature on host-pathogen interactions in D. melanogaster: who benefits? , 2008, Journal of insect physiology.

[3]  David S Schneider,et al.  Bacterial infection of fly ovaries reduces egg production and induces local hemocyte activation. , 2007, Developmental and comparative immunology.

[4]  Timothy B Sackton,et al.  Genetic Variation in Drosophila melanogaster Resistance to Infection: A Comparison Across Bacteria , 2006, Genetics.

[5]  J. David,et al.  Thermal plasticity in Drosophila melanogaster: A comparison of geographic populations , 2006, BMC Evolutionary Biology.

[6]  F. Jiggins,et al.  Genetic variation in Drosophila melanogaster pathogen susceptibility , 2006, Parasitology.

[7]  Annalise B. Paaby,et al.  GENETIC VARIANCE FOR DIAPAUSE EXPRESSION AND ASSOCIATED LIFE HISTORIES IN DROSOPHILA MELANOGASTER , 2005, Evolution; international journal of organic evolution.

[8]  L. Matzkin,et al.  GEOGRAPHIC VARIATION IN DIAPAUSE INCIDENCE, LIFE‐HISTORY TRAITS, AND CLIMATIC ADAPTATION IN DROSOPHILA MELANOGASTER , 2005, Evolution; international journal of organic evolution.

[9]  K. McKean,et al.  BATEMAN'S PRINCIPLE AND IMMUNITY: PHENOTYPICALLY PLASTIC REPRODUCTIVE STRATEGIES PREDICT CHANGES IN IMMUNOLOGICAL SEX DIFFERENCES , 2005, Evolution; international journal of organic evolution.

[10]  Marc Tatar,et al.  Aging of the innate immune response in Drosophila melanogaster , 2005, Aging cell.

[11]  A. Read,et al.  HOST‐PARASITE AND GENOTYPE‐BY‐ENVIRONMENT INTERACTIONS: TEMPERATURE MODIFIES POTENTIAL FOR SELECTION BY A STERILIZING PATHOGEN , 2005, Evolution; international journal of organic evolution.

[12]  A. Read,et al.  HOST-PARASITE AND GENOTYPE-BY-ENVIRONMENT INTERACTIONS: TEMPERATURE MODIFIES POTENTIAL FOR SELECTION BY A STERILIZING PATHOGEN , 2005 .

[13]  David S Schneider,et al.  Secreted Bacterial Effectors and Host-Produced Eiger/TNF Drive Death in a Salmonella-Infected Fruit Fly , 2004, PLoS biology.

[14]  L. Matzkin,et al.  Single-Locus Latitudinal Clines and Their Relationship to Temperate Adaptation in Metabolic Genes and Derived Alleles in Drosophila melanogaster , 2004, Genetics.

[15]  A. Clark,et al.  Genetic Basis of Natural Variation in D. melanogaster Antibacterial Immunity , 2004, Science.

[16]  Z. Bochdanovits,et al.  Temperature dependent larval resource allocation shaping adult body size in Drosophila melanogaster , 2003, Journal of evolutionary biology.

[17]  Z. Bochdanovits Some like it hot... : the evolution and genetics of temperature dependent body size in Drosophila melanogaster , 2003 .

[18]  S. Armitage,et al.  Examining costs of induced and constitutive immune investment in Tenebrio molitor , 2003, Journal of evolutionary biology.

[19]  M. Thomas,et al.  Thermal biology in insect-parasite interactions , 2003 .

[20]  B. Lazzaro A population and quantitative genetic analysis of the Drosophila melanogaster antibacterial immune response , 2002 .

[21]  M. Thomas,et al.  Host–pathogen interactions in a varying environment: temperature, behavioural fever and fitness , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[22]  J. Rolff,et al.  Copulation corrupts immunity: A mechanism for a cost of mating in insects , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[23]  K. McKean,et al.  Increased sexual activity reduces male immune function in Drosophila melanogaster , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[24]  D. Reznick,et al.  Big houses, big cars, superfleas and the costs of reproduction. , 2000, Trends in ecology & evolution.

[25]  H. Godfray,et al.  CROSS‐RESISTANCE FOLLOWING ARTIFICIAL SELECTION FOR INCREASED DEFENSE AGAINST PARASITOIDS IN DROSOPHILA MELANOGASTER , 1999, Evolution; international journal of organic evolution.

[26]  H. Godfray,et al.  Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster , 1997, Nature.

[27]  A. C. James,et al.  Genetic and environmental responses to temperature of Drosophila melanogaster from a latitudinal cline. , 1997, Genetics.

[28]  A. C. James,et al.  Cellular basis and developmental timing in a size cline of Drosophila melanogaster. , 1995, Genetics.

[29]  P. Schmid-Hempel,et al.  Foraging activity and immunocompetence in workers of the bumble bee, Bombus terrestris L , 1995, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[30]  V. French,et al.  EVOLUTION AND DEVELOPMENT OF BODY SIZE AND CELL SIZE IN DROSOPHILA MELANOGASTER IN RESPONSE TO TEMPERATURE , 1994, Evolution; international journal of organic evolution.

[31]  M. Kreitman,et al.  Molecular analysis of an allozyme cline: alcohol dehydrogenase in Drosophila melanogaster on the east coast of North America. , 1993, Genetics.

[32]  P. Schmid-Hempel,et al.  Exploitation of cold temperature as defence against parasitoids in bumblebees , 1993, Nature.