Abstract
The susceptibility to Aspiculuris tetraptera of European Mus musculus hybrids is thought to reflect the disruption of genomic co-adaptation through recombination of the parental genomes. Here, we compared the susceptibility to this parasite between parents and experimental hybrids (intersubspecific until F4, intrasubspecific F1, F2) to clarify the contributions of heterosis and subspecies incompatibility. F1 showed hybrid vigor. Unlike intrasubspecific F2, intersubspecific F2 were less resistant than F1, but revealed no increased susceptibility relative to the parents. Intersubspecific F3 and F4 showed the same hybrid vigor as F1. Heterosis contributed most to the resistance, but the differences between intra- and intersubspecific F2 suggested genomic incompatibilities between subspecies. However, the susceptibility did not increase through the recombination process, showing that disruption of co-adaptation does not directly affect resistance. Even if previous studies still support the selective role of parasites in the current hybrid zone, an alternative hypothesis on the origin of hybrid susceptibility is warranted.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adamson ML (1989) Evolutionary biology of the Oxyurida (Nematoda): biofaces of a haplodiploid taxon. Adv Parasitol 28:175–228
Anya AO (1966) Studies on the biology of some oxyurid nematodes. II. The hatching of eggs and development of Aspiculuris tetraptera Schultz, within the host. J Helminthol 40:261–268
Barton N (2001) The role of hybridization in evolution. Mol Ecol 10:551–568
Barton N, Hewitt G (1985) Analysis of hybrid zones. Annu Rev Ecol Syst 16:113–148
Behnke JM (1975) Aspiculuris tetraptera in wild Mus musculus. The prevalence of infection in male and female mice. J Helminthol 49:85–90
Boissinot S, Boursot P (1997) Discordant phylogeographic patterns between the Y chromosome and the mitochondrial DNA in the house mouse: selection on the Y chromosome? Genetics 146:1019–1034
Boursot P, Auffray JC, Britton-Davidian J, Bonhomme F (1993) The evolution of house mice. Annu Rev Ecol Syst 24:119–152
Burke JM, Arnold ML (2001) Genetics and the fitness of hybrids. Annu Rev Genet 35:31–52
Derothe JM, Loubes C, Orth A, Renaud F, Moulia C (1997) Comparison between patterns of pinworms infection (Aspiculuris tetraptera) in wild and laboratory strains of mice, Mus musculus. Int J Parasitol 27:645–651
Derothe JM, Le Brun N, Loubes C, Perriat-Sanguinet M, Moulia C (1999a) Trypanosoma musculi: compared levels of parasitosis in wild and laboratory strains of Mus musculus mice. Exp Parasitol 91:196–198
Derothe JM, Le Brun N, Loubes C, Perriat-Sanguinet M, Orth A, Moulia C (1999b) Experimental trypanosomiasis of natural hybrids between house mouse subspecies. Int J Parasitol 29:1011–1016
Derothe JM, Le Brun N, Loubes C, Perriat-Sanguinet M, Moulia C (2001) Susceptibility of natural hybrids between house mouse subspecies to Sarcocystis muris. Int J Parasitol 31:15–19
Din W, Anand R, Boursot P, Darviche D, Dod B, Jouvin-Marche E, Orth A, Talwar GP, Cazenave PA, Bonhomme F (1996) Origin and radiation of the house mouse: clues from nuclear genes. J Evol Biol 9:519–539
Edmands S (1999) Heterosis and outbreeding depression in interpopulation crosses spanning a wide range of divergence. Evolution 53:1757–1768
Goncalves L, Pinto Roberto M, Vicente JJ, Noronha D, Gomes Delir C (1998) Helminth parasites of conventionally maintained laboratory mice. II. Inbred strains with an adaptation of the anal swab technique. Mem Inst Oswaldo Cruz 93:121–126
Grant PR, Grant BR (1992) Hybridization of bird species. Science 256:193–197
Hewitt GM (1988) Hybrid zones—natural laboratories for evolutionary studies. Trends Evol Ecol 3:158–167
Hoffman SM, Brown WM (1995) The molecular mechanism underlying the “rare allele phenomenon” in a subspecific hybrid zone of the California field mouse, Peromyscus californicus. J Mol Evol 41:1165–1169
Liersch S, Schimd-Hempel P (1998) Genetic variation within social insect colonies reduces parasite load. Proc R Soc Lond B Biol Sci 265:221–225
Lively CM, Craddock C, Vrijenhoek RC (1990) Red queen hypothesis supported by parasitism in sexual and clonal fish. Nature 344:864–866
Meagher S (1999) Genetic diversity and Capillaria hepatica (Nematoda) prevalence in Michigan deer mouse populations. Evolution 53:1318–1324
Moore WS (1977) An evaluation of narrow hybrid zones in vertebrates. Q Rev Biol 52:263–278
Moore WS, Price JP (1993) Nature of selection in the northern flicker hybrid zone and its implication for speciation theory. In: Harrison RG (ed) Hybrid zones and the evolutionary process. Oxford University Press, Oxford, pp 196–225
Moulia C (1999) Parasitism of plant and animal hybrids—are facts and fates the same? Ecology 80:392–406
Moulia C, Aussel JP, Bonhomme F, Boursot P, Nielsen JT, Renaud F (1991) Wormy mice in a hybrid zone, a genetic control of susceptibility to parasite infection. J Evol Biol 4:679–687
Moulia C, Le Brun N, Dallas J, Orth A, Renaud F (1993) Experimental evidence of genetic determinism in high susceptibility to intestinal pinworm infection in mice: a hybrid zone model. Parasitology 106:387–393
Moulia C, Le Brun N, Loubes C, Marin R, Renaud F (1995) Hybrid vigour against parasites in interspecific crosses between two mice species. Heredity 74:48–52
Moulia C, Le Brun N, Renaud F (1996) Mouse–parasite interactions: from gene to population. Adv Parasitol 38:120–167
Orr HA, Orr LH (1996) Waiting for speciation: the effect of population subdivision on the time of speciation. Evolution 50:1742–1749
Piàlek J, Barton N (1997) The spread of an advantageous allele across a barrier: the effect of random drift and selection against heterozygotes. Genetics 145:493–504
Potts WK, Slev PR (1995) Pathogen-based models favoring MHC genetic diversity. Immunol Rev 143:181–197
Rieseberg LH (1997) Hybrid origins of plant species. Annu Rev Ecol Syst 28:359–389
Rieseberg LH, Archer MA, Wayne RK (1999) Transgressive segregation, adaptation and speciation. Heredity 83:363–372
Sage RD, Heyneman D, Lim KC, Wilson AC (1986) Wormy mice in a hybrid zone. Nature 324:60–63
Sage RD, Atchley WR, Capanna E (1993) House mouse as models in systematic biology. Syst Biol 42:523–561
Schilthuizen M, Hoekstra RF, Gitenberger E (1999) Selective increase of a rare haplotype in a land snail hybrid zone. Proc R Soc Lond B Biol Sci 266:2181–2185
Scott ME, Gibbs HC (1986) Long-term population dynamics of pinworms (Syphacia obvelata and Aspiculuris tetraptera) in mice. J Parasitol 72:652–662
Sherrer B (1984) Biostatistique. Gaetan Morin, Paris
Taffs LF (1976) Pinworm infections in laboratory rodents: a review. Lab Anim 10:1–13
Turelli M, Orr HA (2000) Dominance, epistatis and the genetics of postzygotic isolation. Genetics 154:1663–1679
Zuk M, McKean KA (1996) Sex differences in parasitic infections: patterns and processes. Int J Parasitol 26:1009–1024
Acknowledgements
We especially thank Annie Orth for providing us with wild-derived strains of the Wild Mouse Repository, François Bonhomme for his many suggestions and support throughout the completion of this project and Janice Britton-Davidian and Serge Morand for their helpful comments to improve this manuscript. These experiments comply with the current laws of the France.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Derothe, JM., Porcherie, A., Perriat-Sanguinet, M. et al. Recombination does not generate pinworm susceptibility during experimental crosses between two mouse subspecies. Parasitol Res 93, 356–363 (2004). https://doi.org/10.1007/s00436-004-1145-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-004-1145-1