Skip to main content
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2003 Jul 22;270(1523):1535–1540. doi: 10.1098/rspb.2003.2402

Variable male potential rate of reproduction: high male mating capacity as an adaptation to parasite-induced excess of females?

Jérôme Moreau 1, Thierry Rigaud 1
PMCID: PMC1691398  PMID: 12965021

Abstract

Numerous animals are known to harbour intracytoplasmic symbionts that gain transmission to a new host generation via female eggs and not male sperm. Bacteria of the genus Wolbachia are a typical example. They infect a large range of arthropod species and manipulate host reproduction in several ways. In terrestrial isopods (woodlice), Wolbachia are responsible for converting males into females (feminization (F)) in some species, or for infertility in certain host crosses in other species (cytoplasmic incompatibility (CI)). Wolbachia with the F phenotype impose a strong excess of females on their host populations, while Wolbachia expressing CI do not. Here, we test the possibility that male mating capacity (MC) is correlated with Wolbachia-induced phenotype. We show that males of isopod hosts harbouring F Wolbachia possess a strong MC (i.e. are able to mate with several females in a short time), while those of species harbouring CI Wolbachia possess a weaker MC. This pattern may be explained either by the selection of high MC following the increase in female-biased sex ratios, or because the F phenotype would lead to population extinction in species where MC is not sufficiently high. This last hypotheses is nevertheless more constrained by population structure.

Full Text

The Full Text of this article is available as a PDF (112.5 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Altizer SM, Oberhauser KS. Effects of the protozoan parasite ophryocystis elektroscirrha on the fitness of monarch butterflies (Danaus plexippus) . J Invertebr Pathol. 1999 Jul;74(1):76–88. doi: 10.1006/jipa.1999.4853. [DOI] [PubMed] [Google Scholar]
  2. Bandi C., Anderson T. J., Genchi C., Blaxter M. L. Phylogeny of Wolbachia in filarial nematodes. Proc Biol Sci. 1998 Dec 22;265(1413):2407–2413. doi: 10.1098/rspb.1998.0591. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bilton DT, Goode D, Mallet J. Genetic differentiation and natural hybridization between two morphological forms of the common woodlouse, oniscus asellus linnaeus 1758 . Heredity (Edinb) 1999 Apr;82(Pt 4):462–469. doi: 10.1038/sj.hdy.6885170. [DOI] [PubMed] [Google Scholar]
  4. Bollache L., Rigaud T., Cézilly F. Effects of two acanthocephalan parasites on the fecundity and pairing status of female Gammarus pulex (Crustacea: Amphipoda). J Invertebr Pathol. 2002 Feb;79(2):102–110. doi: 10.1016/s0022-2011(02)00027-7. [DOI] [PubMed] [Google Scholar]
  5. Bouchon D., Rigaud T., Juchault P. Evidence for widespread Wolbachia infection in isopod crustaceans: molecular identification and host feminization. Proc Biol Sci. 1998 Jun 22;265(1401):1081–1090. doi: 10.1098/rspb.1998.0402. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dedeine F., Vavre F., Fleury F., Loppin B., Hochberg M. E., Bouletreau M. Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proc Natl Acad Sci U S A. 2001 May 15;98(11):6247–6252. doi: 10.1073/pnas.101304298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hatcher M. J., Taneyhill D. E., Dunn A. M., Tofts C. Population dynamics under parasitic sex ratio distortion. Theor Popul Biol. 1999 Aug;56(1):11–28. doi: 10.1006/tpbi.1998.1410. [DOI] [PubMed] [Google Scholar]
  8. Hatcher MJ. Persistence of selfish genetic elements: population structure and conflict. Trends Ecol Evol. 2000 Jul;15(7):271–277. doi: 10.1016/s0169-5347(00)01875-9. [DOI] [PubMed] [Google Scholar]
  9. Hurd H. Host fecundity reduction: a strategy for damage limitation? Trends Parasitol. 2001 Aug;17(8):363–368. doi: 10.1016/s1471-4922(01)01927-4. [DOI] [PubMed] [Google Scholar]
  10. Jiggins F. M., Hurst G. D., Majerus M. E. Sex-ratio-distorting Wolbachia causes sex-role reversal in its butterfly host. Proc Biol Sci. 2000 Jan 7;267(1438):69–73. doi: 10.1098/rspb.2000.0968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Legrand J. J., Martin G., Artault J. C. Corrélation entre la présence d'un symbionte bactérien dans les ovocytes de Porcellio dilatatus petiti, et la stérilité du croisement: P.d. petiti male x P.d. dilatatus female. Arch Inst Pasteur Tunis. 1978 Dec;55(4):507–514. [PubMed] [Google Scholar]
  12. Michel-Salzat A., Bouchon D. Phylogenetic analysis of mitochondrial LSU rRNA in oniscids. C R Acad Sci III. 2000 Sep;323(9):827–837. doi: 10.1016/s0764-4469(00)01221-x. [DOI] [PubMed] [Google Scholar]
  13. Moret Y., Juchault P., Rigaud T. Wolbachia endosymbiont responsible for cytoplasmic incompatibility in a terrestrial crustacean: effects in natural and foreign hosts. Heredity (Edinb) 2001 Mar;86(Pt 3):325–332. doi: 10.1046/j.1365-2540.2001.00831.x. [DOI] [PubMed] [Google Scholar]
  14. Pagel M. D., Harvey P. H. Recent developments in the analysis of comparative data. Q Rev Biol. 1988 Dec;63(4):413–440. doi: 10.1086/416027. [DOI] [PubMed] [Google Scholar]
  15. Polak M., Starmer W. T. Parasite-induced risk of mortality elevates reproductive effort in male Drosophila. Proc Biol Sci. 1998 Nov 22;265(1411):2197–2201. doi: 10.1098/rspb.1998.0559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Purvis A., Rambaut A. Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analysing comparative data. Comput Appl Biosci. 1995 Jun;11(3):247–251. doi: 10.1093/bioinformatics/11.3.247. [DOI] [PubMed] [Google Scholar]
  17. Rigaud T., Bouchon D., Souty-Grosset C., Raimond R. Mitochondrial DNA polymorphism, sex ratio distorters and population genetics in the isopod Armadillidium vulgare. Genetics. 1999 Aug;152(4):1669–1677. doi: 10.1093/genetics/152.4.1669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Rigaud T., Pennings P. S., Juchault P. Wolbachia bacteria effects after experimental interspecific transfers in terrestrial isopods. J Invertebr Pathol. 2001 May;77(4):251–257. doi: 10.1006/jipa.2001.5026. [DOI] [PubMed] [Google Scholar]
  19. Rigaud T, Moreau J, Juchault P. Wolbachia infection in the terrestrial isopod oniscus asellus: sex ratio distortion and effect on fecundity. Heredity (Edinb) 1999 Oct;83(#):469–475. doi: 10.1038/sj.hdy.6885990. [DOI] [PubMed] [Google Scholar]
  20. Rousset F., Bouchon D., Pintureau B., Juchault P., Solignac M. Wolbachia endosymbionts responsible for various alterations of sexuality in arthropods. Proc Biol Sci. 1992 Nov 23;250(1328):91–98. doi: 10.1098/rspb.1992.0135. [DOI] [PubMed] [Google Scholar]
  21. Stouthamer R., Breeuwer J. A., Hurst G. D. Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol. 1999;53:71–102. doi: 10.1146/annurev.micro.53.1.71. [DOI] [PubMed] [Google Scholar]
  22. Wade M. J., Chang N. W. Increased male fertility in Tribolium confusum beetles after infection with the intracellular parasite Wolbachia. Nature. 1995 Jan 5;373(6509):72–74. doi: 10.1038/373072a0. [DOI] [PubMed] [Google Scholar]
  23. Werren J. H., Zhang W., Guo L. R. Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proc Biol Sci. 1995 Jul 22;261(1360):55–63. doi: 10.1098/rspb.1995.0117. [DOI] [PubMed] [Google Scholar]
  24. Worden BD, Parker PG, Pappas PW. Parasites reduce attractiveness and reproductive success in male grain beetles. Anim Behav. 2000 Mar;59(3):543–550. doi: 10.1006/anbe.1999.1368. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES