Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-30T15:24:52.683Z Has data issue: false hasContentIssue false
  • English
  • Français

Sex ratio and morphological polymorphism in an isolated, endemic Teladorsagia circumcincta population

Published online by Cambridge University Press:  18 September 2009

B.H. Craig ,
J.G. Pilkington  and
J.M. Pemberton
B.H. Craig*
Affiliation:
Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, West Mains Road, EdinburghEH9 3JT, UK
J.G. Pilkington
Affiliation:
Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, West Mains Road, EdinburghEH9 3JT, UK
J.M. Pemberton
Affiliation:
Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, West Mains Road, EdinburghEH9 3JT, UK
*
*E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Teladorsagia circumcincta is a polygamous nematode that exhibits morphological polymorphism. Sex ratio is typically female biased and the male nematodes occur in association with the genetically similar, minor morphotypes Teladorsagia davtiani and Teladorsagia trifurcata. In experimental infections, sex ratio (proportion male) and the proportion of minor male morphs observed have been shown to be influenced by both host and nematode-related factors. As similar investigations from natural systems are rare, this study examined whether sex ratio and minor male morph frequency were associated with host age and sex and nematode infra-population size in the isolated Soay sheep population on St Kilda. Count data for Teladorsagia were analysed for sheep of all age classes and both sexes from the winters of three consecutive population crashes (1999, 2002 and 2005). Generally, the intensity of Teladorsagia nematodes increased with host age until the age of 2 years before decreasing. In 2005, abundance of nematodes was generally higher than in the previous crashes, nematode sex ratio was negatively associated with host age and tended to be negatively associated with nematode intensity. Within the male nematode subpopulation, T. circumcincta always predominated, followed by T. davtiani and then T. trifurcata, with little variation in the relative proportions between hosts. The presence of each minor morph was primarily associated with the intensity of male T. circumcincta and, in those hosts where all three male morphs were detected, intensity of each minor morph was most associated with intensity of Teladorsagia females. Therefore, in a year when the nematode was generally more abundant, sex ratio appeared to be influenced by both host and nematode-related factors, whereas in all years examined, the frequency of morphological polymorphism was primarily density dependent.

Type
Research Papers
Information
Journal of Helminthology , Volume 84 , Issue 2 , June 2010 , pp. 208 - 215
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Andrews, R.H. & Beveridge, I. (1990) Apparent absence of genetic differences among species of Teladorsagia (Nematoda: Trichostrongylidae). Journal of Helminthology 64, 290–294.Google Scholar
Becklund, W.W. (1962) Distribution and hosts of the ruminant parasite Teladorsagia davtiani Andreeva and Satubaldin, 1954 (Nematoda: Trichostrongylidae) in the United States. Journal of Parasitology 48, 469.Google Scholar
Becklund, W.W. & Walker, M.L. (1971) Nomenclature and morphology of Ostertagia trifurcata Ransom, 1907, with data on spicule lengths of five stomach worms of ruminants. Journal of Parasitology 57, 508–516.Google Scholar
Cabaret, J. (1984) Seasonal changes in the abomasal nematodes of naturally infected ewes in Moulay-Bouazza (Morocco). Veterinary Parasitology 15, 47–56.Google Scholar
Cabaret, J., Morales, G. & Gruner, L. (1984) Caracterisation de Teladorsagia circumcincta et T. trifurcata. Aspects epidemiologiques et biologiques. Annales de Parasitologie Humaine et Comparee 59, 607–617.Google Scholar
Clutton-Brock, T.H. & Pemberton, J.M. (2004) Soay sheep: dynamics and selection in an island population. Cambridge, Cambridge University Press.Google Scholar
Craig, B.H., Pilkington, J.G. & Pemberton, J.M. (2006) Gastrointestinal nematode species burdens and host mortality in a feral sheep population. Parasitology 133, 485–496.Google Scholar
Crawley, M.J. (2003) Statistical computing: an introduction to data analysis using S-Plus. New York, Wiley.Google Scholar
Drozdz, J. (1995) Polymorphism in the Ostertagiinae Lopez-Neyra, 1947 and comments on the systematics of these nematodes. Systematic Parasitology 32, 91–99.Google Scholar
Fowler, J. & Cohen, L. (1990) Practical statistics for field biology. Chichester, Wiley.Google Scholar
Gaba, S., Gruner, L. & Cabaret, J. (2006) The establishment rate of a sheep nematode: revisiting classics using a meta-analysis of 87 experiments. Veterinary Parasitology 140, 302–311.Google Scholar
Grillo, V., Craig, B.H., Wimmer, B. & Gilleard, J.S. (2008) Microsatellite genotyping supports the hypothesis that Teladorsagia davtiani and Teladorsagia trifurcata are morphotypes of Teladorsagia circumcincta. Molecular and Biochemical Parasitology 159, 59–63.Google Scholar
Haukisalmi, V., Henttonen, H. & Vikman, P. (1996) Variability of sex ratio, mating probability and egg production in an intestinal nematode in its fluctuating host population. International Journal for Parasitology 26, 755–764.Google Scholar
Huettel, R.N. (2004) Reproductive behaviour. pp. 127–149in Gaugler, R. & Bilgrami, A.L. (Eds) Nematode behaviour. Wallingford, CABI Publishing.Google Scholar
Lancaster, M., Hong, C. & Michel, J.F. (1983) Polymorphism in the Trichostrongylidae. pp. 293–302in Stone, A.R., Platt, H.M. & Khalil, L.F. (Eds) Concepts in nematode systematics, Vol. 22. London, Academic Press.Google Scholar
Lee, D.L. & Atkinson, H.J. (1976) Reproductive physiology and hatching. pp. 116–144in Lee, D.L. & Atkinson, H.J. (Eds) Physiology of nematodes. London, Macmillan Press.Google Scholar
Leignel, V. & Cabaret, J (2001a) Are Teladorsagia (Nematoda) morphs equally able to survive under anthelmintic treatment in sheep on pastures? Parasitology Research 87, 687–692.Google Scholar
Leignel, V. & Cabaret, J. (2001b) Massive use of chemotherapy influences life traits of parasitic nematodes in domestic ruminants. Functional Ecology 15, 569–574.Google Scholar
Leignel, V., Cabaret, J. & Humbert, J.F. (2002) New molecular evidence that Teladorsagia circumcincta (Nematoda: Trichostrongylidea) is a species complex. Journal of Parasitology 88, 135–140.Google Scholar
Lichtenfels, J.R. & Hoberg, E.P. (1993) The systematics of nematodes that cause ostertagiasis in domestic and wild ruminants in North America: an update and a key to species. Veterinary Parasitology 46, 33–53.Google Scholar
May, R.M. & Woolhouse, M.E.J. (1993) Biased sex ratios and parasite mating probabilities. Parasitology 107, 287–295.Google Scholar
Poulin, R. (1997) Population abundance and sex ratio in dioecious helminth parasites. Oecologia 111, 375–380.Google Scholar
Poulin, R. (2007) Parasite aggregation: causes and consequences. pp. 134–159in Poulin, R. (Ed.) Evolutionary ecology of parasites. Oxford, Princeton University Press.Google Scholar
Richard, S. & Cabaret, J. (1993) Primary infection of kids with Teladorsagia circumcincta: susceptibility and blood constituents. Veterinary Parasitology 47, 279–287.Google Scholar
Rose, H.J. (1962) Differentiation of the sheep stomach worms Teladorsagia davtiani (Andreeva and Satubaldin, 1954) and Ostertagia trifurcata (Ransom, 1907). Research in Veterinary Science 3, 304–307.Google Scholar
Rowland, J.M. & Emlen, D.J. (2009) Two thresholds, three male forms result in facultative male trimorphism in beetles. Science 323, 773–776.Google Scholar
Stear, M.J., Baiden, K., Bishop, S.C., Buitkamp, J., Duncan, J.L., Gettinby, G., McKellar, Q.A., Park, M., Parkins, J.J., Reid, S.W.J., Strain, S. & Murray, M. (1997) The genetic basis of resistance to Ostertagia circumcincta in lambs. The Veterinary Journal 154, 111–119.Google Scholar
Stear, M.J., Fitton, L., Innocent, G.T., Murphy, L., Rennie, K. & Matthews, L. (2007) The dynamic influence of genetic variation on the susceptibility of sheep to gastrointestinal nematode infection. Journal of the Royal Society Interface 4, 767–776.Google Scholar
Stevenson, L.A., Gasser, R.B. & Chilton, N.B. (1996) The ITS-2 rDNA of Teladorsagia circumcincta, T. trifurcata and T. davtiani (Nematoda: Trichostrongylidae) indicates that these taxa are one species. International Journal for Parasitology 26, 1123–1126.Google Scholar
Suarez, V.H., Cabaret, J. & Gruner, L. (1995) Morphological polymorphism in the nematode Teladorsagia circumcincta in relation to age of larvae, infection mode and lamb characteristics in experimental conditions. International Journal for Parasitology 25, 1173–1177.Google Scholar
Waller, P.J. & Thomas, R.J. (1978) Host-induced effects on the morphology of Ostertagia circumcincta in grazing lambs. International Journal for Parasitology 8, 365–370.Google Scholar
Wilson, K. & Hardy, I.C.W. (2002) Statistical analysis of sex ratios: an introduction. pp. 48–92in Hardy, I.C.W. (Ed.) Sex ratios: concepts and research methods. Cambridge, Cambridge University Press.Google Scholar
Wilson, K., Grenfell, B.T., Pilkington, J.G., Boyd, H.E.G. & Gulland, F.M.D. (2004) Parasites and their impact. pp. 113–165in Clutton-Brock, T.H. & Pemberton, J.M. (Eds) Soay sheep: dynamics and selection in an island population. Cambridge, Cambridge University Press.Google Scholar