Paternally derived immune priming for offspring in the red flour beetle, Tribolium castaneum.

1. Parasitized females in mammals, fish and birds can enhance the immune defence of their offspring by transferring specific antibodies for the embryo. Likewise, social insect mothers transfer immunity despite the fact that invertebrates lack antibodies. 2. Female trans-generational immune priming is consistent with parental investment theory, because mothers invest more into rearing their offspring than fathers. However, when immune priming is not directly linked to parental care, as is often the case in insects that abandon their eggs after oviposition, both sexes might benefit from protecting their offspring. 3. Using the red flour beetle, Tribolium castaneum, we show that after parental exposure to heat-killed bacteria, trans-generational immune priming occurs through fathers as well as mothers. 4. This novel finding challenges the traditional view that males provide only genes to their offspring in species without paternal care, and raises the possibility of a division of tasks with respect to immune protection between parents.

[1]  P. Schmid-Hempel,et al.  A distinct infection cost associated with trans-generational priming of antibacterial immunity in bumble-bees , 2009, Biology Letters.

[2]  J. Kurtz,et al.  Phagocytosis mediates specificity in the immune defence of an invertebrate, the woodlouse Porcellio scaber (Crustacea: Isopoda). , 2009, Developmental and comparative immunology.

[3]  D. Heckel,et al.  Dietary-dependent trans-generational immune priming in an insect herbivore , 2009, Proceedings of the Royal Society B: Biological Sciences.

[4]  D. Promislow,et al.  Cross-generational fitness effects of infection in Drosophila melanogaster , 2009, Fly.

[5]  P. Schmid-Hempel,et al.  Strain-specific priming of resistance in the red flour beetle, Tribolium castaneum , 2009, Proceedings of the Royal Society B: Biological Sciences.

[6]  J. Kurtz,et al.  The stimulation of immune defence accelerates development in the red flour beetle (Tribolium castaneum) , 2008, Journal of evolutionary biology.

[7]  K. Gallizzi,et al.  Maternally transmitted parasite defence can be beneficial in the absence of parasites , 2008 .

[8]  P. Schmid-Hempel,et al.  Facultative but persistent trans-generational immunity via the mother's eggs in bumblebees , 2007, Current Biology.

[9]  Lars Råberg,et al.  Disentangling Genetic Variation for Resistance and Tolerance to Infectious Diseases in Animals , 2007, Science.

[10]  R. Martienssen,et al.  Transposable elements and the epigenetic regulation of the genome , 2007, Nature Reviews Genetics.

[11]  P. Schmid-Hempel,et al.  Insect Immunity Shows Specificity in Protection upon Secondary Pathogen Exposure , 2006, Current Biology.

[12]  Y. Moret.  ‘Trans-generational immune priming’: specific enhancement of the antimicrobial immune response in the mealworm beetle, Tenebrio molitor , 2006, Proceedings of the Royal Society B: Biological Sciences.

[13]  P. Gounon,et al.  RNA-mediated non-mendelian inheritance of an epigenetic change in the mouse , 2006, Nature.

[14]  Susan J. Brown,et al.  Genetic Linkage Maps of the Red Flour Beetle, Tribolium castaneum, Based on Bacterial Artificial Chromosomes and Expressed Sequence Tags , 2005, Genetics.

[15]  Peter Gluckman,et al.  Developmental plasticity and human health , 2004, Nature.

[16]  E. Brodie,et al.  Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transmission , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[17]  J. Kurtz,et al.  Innate defence: Evidence for memory in invertebrate immunity , 2003, Nature.

[18]  P. Schmid-Hempel,et al.  Entomology: Immune defence in bumble-bee offspring , 2001, Nature.

[19]  P. Schmid-Hempel,et al.  Survival for immunity: the price of immune system activation for bumblebee workers. , 2000, Science.

[20]  D. Haig.  The Kinship Theory of Genomic Imprinting , 2000 .

[21]  K. P. Sauer,et al.  The immunocompetence handicap hypothesis: testing the genetic predictions , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[22]  Read,et al.  A pluralist approach to sex and recombination , 1999 .

[23]  N. White,et al.  EFFECT OF BACILLUS THURINGIENSIS ON FEEDING AND ENERGY USE BY PLODIA INTERPUNCTELLA (LEPIDOPTERA: PYRALIDAE) AND TRIBOLIUM CASTANEUM (COLEOPTERA: TENEBRIONIDAE) , 1999, The Canadian Entomologist.

[24]  S. Bensch,et al.  Good genes, oxidative stress and condition–dependent sexual signals , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[25]  C. Fox,et al.  The adaptive significance of maternal effects. , 1998, Trends in ecology & evolution.

[26]  A. J. Moore,et al.  Evolutionary consequences of indirect genetic effects. , 1998, Trends in ecology & evolution.

[27]  L. Cerenius,et al.  Role of the prophenoloxidase-activating system in invertebrate immunity. , 1998, Current opinion in immunology.

[28]  M. Rossiter,et al.  INCIDENCE AND CONSEQUENCES OF INHERITED ENVIRONMENTAL EFFECTS , 1996 .

[29]  J. Bernardo.  MATERNAL EFFECTS IN ANIMAL ECOLOGY , 1996 .

[30]  Y. Carlier,et al.  Influence of maternal infection on offspring resistance towards parasites. , 1995, Parasitology today.

[31]  W. Hamilton,et al.  Sexual reproduction as an adaptation to resist parasites (a review). , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[32]  M. Kirkpatrick,et al.  THE EVOLUTION OF MATERNAL CHARACTERS , 1989, Evolution; international journal of organic evolution.

[33]  E. Whitelaw,et al.  Another role for RNA: a messenger across generations. , 2007, Trends in genetics : TIG.

[34]  A. Sokoloff.  The biology of Tribolium, with special emphasis on genetic aspects. , 1974 .