Male pregnancy and biparental immune priming

American Naturalist

Volumn 180, Issue 6, 2012, Pages 802-814

  Roth, Olivia ^a   Klein, Verena ^a   Beemelmanns, Anne ^a   Scharsack, Jörn P ^b   Reusch, Thorsten B H ^a  

^a GEOMAR HELMHOLTZ CENTRE FOR OCEAN RESEARCH KIEL   (Germany)

^b UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Host parasite interaction; Immune defense; Parental effects; Pipefish; Placenta; Vibrio

Indexed keywords

MESSENGER RNA;

GENE EXPRESSION; HOST-PARASITE INTERACTION; IMMUNITY; LIFE HISTORY TRAIT; MALE BEHAVIOR; PARENT-OFFSPRING INTERACTION; PARENTAL CARE; PREGNANCY; TELEOST;

ANIMAL; ANIMAL EMBRYO; ARTICLE; EMBRYO DEVELOPMENT; FEMALE; GENE EXPRESSION REGULATION; GENETICS; IMMUNITY; IMMUNOLOGY; MALE; PATERNAL BEHAVIOR; PHYSIOLOGY; PRENATAL DEVELOPMENT; REAL TIME POLYMERASE CHAIN REACTION; SMEGMAMORPHA; UPREGULATION; VIBRIO;

ANIMALS; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNITY; MALE; PATERNAL BEHAVIOR; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; SMEGMAMORPHA; UP-REGULATION; VIBRIO;

BACTERIA (MICROORGANISMS); HIPPOCAMPINAE; SYNGNATHIDAE; TELEOSTEI; VERTEBRATA; VIBRIO;

EID: 84869171950     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/668081     Document Type: Article

References (56)

1. Adamo, S. A. 1999. Evidence for adaptive changes in egg laying in crickets exposed to bacteria and parasites. Animal Behavior 57: 117-124.
2. Altizer, S., D. Harvell, and E. Friedle. 2003. Rapid evolutionary dynamics and disease threats to biodiversity. Trends in Ecology & Evolution 18:589-596.
3. Arnqvist, G., and L. Rowe. 2005. Sexual conflict. Princeton University Press, Princeton, NJ.
4. Bateman, A. J. 1948. Intra-sexual selection in Drosophila. Heredity 2:349-368.
5. Belkin, S., and R. R. Colwell. 2006. Oceans and health: pathogens in the marine environment. Springer, Berlin.
6. Birrer, S. C., T. B. H. Reusch, and O. Roth. 2012. Salinity change impairs pipefish immune defense. Fish and Shellfish Immunololgy 32:1238-1248. doi:10.1016/j.fsi.2012.08.028.
7. Bly, J. E., A. S. Grimm, and I. G. Morris. 1986. Transfer of passive immunity from mother to young in a teleost fish: haemagglutinating activity in the serum and eggs of plaice Pleuronectes platessa L. Comparative Biochemistry Physiology A 84:309-313.
8. Bonneaud, C., J. Mazuc, O. Chastel, H. Westerdahl, and G. Sorci. 2004. Terminal investment induced by immune challenge and fitness traits associated with major histocompatibility complex in the hourse sparrow. Evolution 58:2823-2830.
9. Boots, M., and R. G. Bowers. 2004. The role of ecological feedbacks in the evolution of host defence: what does theory tell us? Philosophical Transactions of the Royal Society B: Biological Sciences 364:27-36.
10. Boulinier, T., and V. Staszweski. 2008. Maternal transfer of antibodies: raising immuno-ecology issues. Trends in Ecology & Evolution 23: 282-288.
11. Clutton-Brock, T. H. 1984. Reproductive effort and terminal investment in iteroparous animals. American Naturalist 123:212-229.
12. Dzyuba, B., K. J. W. Van Look, A. Cliffe, H. J. Koldewey, and W. V. Holt. 2006. Effect of parental age and associated size on fecundity, growth and survival in the yellow seahorse Hippocampous kuda. Journal of Experimental Biology 209:3055-3061.
13. Eizaguirre, C., T. L. Lenz, M. Kalbe, and M. Milinski. 2012. Rapid and adaptive evolution of MHC genes under parasite selection in experimental vertebrate populations. Nature Communications 3: 621. doi:10.1038/ncomms1632.
14. Ellingsen, T., C. Strand, E. Monsen, J. Bogwald, and R. A. Dalmo. 2005. The ontogeny of the comlement component C3 in the spotted wolffish (Anarhichas minor Olafsen). Fish and Shellfish Immunology 18:351-358.
15. Fuda, H., A. Hara, F. Yamazaki, and K. Kobayashi. 1992. A peculiar immunoglobulin M (IgM) identified in eggs of chum salmon (Oncorhynchus keta). Developmental and Comparative Immunology 1993:241-248.
16. Gasparini, J., K. D. McCoy, T. Tveraa, and T. Boulinier. 2002. Related concentrations of specific immunoglobulins against the Lyme disease agent Borrelia burgdorferi sensu lato in eggs, young and adults of the kittiwake (Rissa tridactyla). Ecology Letters 5:519-524.
17. Glezen, P. 2003. Effect of maternal antibodies on the infant immune response. Vaccine 21:3389-3392.
18. Grindstaff, J. L., E. D. Brodie III, and E. D. Ketterson. 2003. Immune function accross generations: integrating mechanism and evolutionary process in maternal antibody transmission. Proceedings of the Royal Society B: Biological Sciences 270:2309-2319.
19. Haig, D. 2000. The kinship theory of genomic imprinting. Annual Review of Ecology and Systematics 31:9-32.
20. Hamilton, W. D. 1980. Sex versus non-sex versus parasite. Oikos 35: 282-290.
21. Hamilton, W. D., R. Axelrod, and R. Tanese. 1990. Sexual reproduction as an adaptation to resist parasites (a review). Proceedings of the National Academy of Sciences of the USA 87:3566-3573.
22. Hanif, A., V. Bakopoulos, and G. J. Dimitriadis. 2004. Maternal transfer of humoral specific and non-specific immune parameters to sea bream (Sparus aurata) larvae. Fish Shellfish Immunol 17:411-435.
23. Hanssen, S. A. 2006. Costs of an immune challenge and terminal investment in a long-lived bird. Ecology 87:2440-2446.
24. Harlin-Cognato, A., E. A. Hoffman, and A. G. Jones. 2006. Gene cooption without duplication during the evolution of a male-pregnancy gene in pipefish. Proceedings of the National Academy of Sciences of the USA 103:19407-19412.
25. Hasselquist, D., and J.-A. Nilsson. 2009. Maternal transfer of antibodies in vertebrates: trans-generational effects on offspring immunity. Philosophical Transactions of the Royal Society B: Biological Sciences 364:51-60.
26. Jones, A. G., G. Rosenqvist, A. Berglund, S. J. Arnold, and J. C. Avise. 2000. The Bateman gradient and the cause of sexual selection in a sex-role-reversed pipefish. Proceedings of the Royal Society B: Biological Sciences 267:677-680.
27. Jones, A. G., G. Rosenqvist, A. Berglund, and J. C. Avise. 2005. The measurement of sexual selection using Bateman's principles: an experimental test in the sex-role-reversed pipefish Syngnathus typhle. Integrative Comparative Biology 45:874-884.
28. Landis, S. H., M. Kalbe, T. B. H. Reusch, and O. Roth. 2012. Consistent pattern of local adaptation during an experimental heat wave in a pipefish-trematode host-parasite system. PLoS ONE 7: e30658.
29. Lemke, H., A. Coutinho, and H. Lange. 2004. Lamarckian inheritance by somatically acquired maternal IgG phenotypes. Trends in Immunology 25:180-186.
30. Magnadottir, B., S. Lange, S. Gudmundsdottir, J. Bogwald, and R. A. Dalmo. 2005. Ontogeny of humoral immune parameters in fish. Fish and Shellfish Immunology 19:773-783.
31. Matsunaga, T., and A. Rahman. 1998. What brought the adaptive immune system to vertebrates? the jaw hypothesis and the seahorse. Immunology Review 166:177-186.
32. Moret, Y. 2006. "Trans-generational immune priming": specific enhancement of the antimicrobial immune response in the mealworm beetle, Tenebrio molitor. Proceedings of the Royal Society B: Biological Sciences 273:1399-1405.
33. Mousseau, T. A., and C. W. Fox. 1998. The adaptive significance of maternal effects. Trends in Ecology & Evolution 13:403-407.
34. Mulero, I., A. Garcia-Ayala, J. Meseguer, and V. Mulero. 2007. Maternal transfer of immunity and ontogeny of autologous immunocompetence of fish: a minireview. Aquaculture 268:244-250.
35. Paczolt, K. A., and A. G. Jones. 2010. Post-copulatory sexual selection and sexual conflict in the evolution of male pregnancy. Nature 464:401-404.
36. Picchietti, S., G. Scapigliati, M. Fanelli, F. Barbato, S. Canese, L. Mastrolia, M. Mazzini, et al. 2001. Sex-related variations of serum immunoglobulins during reproduction in gilthead sea bream and evidence for a transfer from the female to the eggs. Journal of Fish Biology 59:1503-1511.
37. Poulin, R., and F. Thomas. 2008. Epigenetic effects of infection on the phenotype of host offspring: parasites reaching across host generations. Oikos 117:331-335.
38. Råberg, L., J.-A. Nilsson, P. Ilmonen, M. Stjernmann, and D. Hasselquist. 2000. The cost of an immune response: vaccination reduces parental effort. Ecology Letters 3:382-386.
39. Råberg, L., M. Vestberg, D. Hasselquist, R. Holmdahl, E. Svensson, and J.-A. Nilsson. 2002. Basal metabolic rate and the evolution of the adaptive immune system. Proceedings of the Royal Society B: Biological Sciences 269:818-821.
40. Reaney, L. T., and R. J. Knell. 2010. Immune activation but not male quality affects female current reproductive investment in a dung beetle. Behavioral Ecology 21:1367-1372.
41. Reid, J. M., P. Arcese, L. F. Keller, and D. Hasselquist. 2006. Longterm maternal effects on offspring immune response in song sparrows Melospiza melodia. Biology Letters 2:573-576.
42. Ripley, J. L., and C. M. Foran. 2009. Direct evidence for embryonic uptake of paternally-derived nutrients in two pipefishes (Syngnathidae: Syngnathus spp.). Journal of Comparative Physiology B 179:325-333.
43. Roth, O., G. Joop, H. Eggert, J. Hilbert, J. Daniel, P. Schmid-Hempel, and J. Kurtz. 2010. Paternally derived immune priming for offspring in the red flour beetle, Tribolium castaneum. Journal of Animal Ecology 79:403-413.
44. Roth, O., I. Keller, S. H. Landis, W. Salzburger, and T. B. H. Reusch. 2012. Hosts are ahead in a marine host-parasite coevolutionary arms race: innate immune system adaptation in pipefish Syngnathus typhle against Vibrio phylotypes. Evolution 66:2528-2539.
45. Roth, O., J. P. Scharsack, I. Keller, and T. B. H. Reusch. 2011. Batemańs principle and immunity in a sex-role reversed pipefish. Journal of Evolutionary Biology 24:1410-1420.
46. Rozen, S., and H. Skaletzky. 1997. PRIMER3. http://www.genome.wi.mit.edu/genome/other/primer3.html.
47. Sadd, B. M., L. Holman, S. A. O. Armitage, F. Lock, R. Marland, and M. T. Siva-Jothy. 2006. Modulation of sexual signalling by immune challenged male mealworm beetles (Tenebrio molitor, L.): evidence for terminal investment and dishonesty. Journal of Evolutionary Biology 19:321-325.
48. Sadd, B. M., Y. Kleinlogel, R. Schmid-Hempel, and P. Schmid-Hempel. 2005. Trans-generational immune priming in a social insect. Biology Letters 1:386-388.
49. Sadd, B. M., and P. Schmid-Hempel. 2007. Facultative but persistent transgenerational immunity via the mother's eggs in bumblebees. Current Biology 17:R1046-R1047.
50. Sheldon, B. C., and S. Verhulst. 1996. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology & Evolution 11:317-321.
51. Shoemaker, K. L., N. M. Parsons, and S. A. Adamo. 2006. Egg-laying behaviour following infection in the cricket Gryllus texensis. Canadian Journal of Zoology 84:412-418.
52. Stölting, K. K., and A. B. Wilson. 2007. Male pregnancy in seahorses and pipefish: beyond the mammalian model. Bioessays 29:884-896.
53. Van Valen, L. 1973. A new evolutionary law. Evolutionary Theory 1: 1-30.
54. Wassarmann, P. M., L. Jovine, and E. S. Litscher. 2001. A profile of fertilization in mammals. Nature Cell Biology 3:E59-E64.
55. Wilson, A., A. Vincent, I. Ahnjesjö, and A. Meyer. 2001. Male pregnancy in seahorses and pipefishes (Family Syngnathidae): rapid diversification of paternal brood pouch morphology inferred from a molecular phylogeny. Journal of Heredity 92:159-166.
56. Zanchi, C., J.-P. Troussard, G. Martinaud, J. Moreau, and Y. Moret. 2011. Differential expression and costs between maternally and paternally derived immune priming for offspring in an insect. Journal of Animal Ecology 80:1174-1183.