Log in

Inbreeding in stochastic subdivided mating systems: the genetic consequences of host spatial structure, aggregated transmission dynamics and life history characteristics in parasite populations

  • RESEARCH ARTICLE
  • Published:
Journal of Genetics Aims and scope Submit manuscript

Abstract

Inbreeding in parasite populations can have important epidemiological and evolutionary implications. However, theoretical models have predominantly focussed on the evolution of parasite populations under strong selection or in epidemic situations, and our understanding of neutral gene dynamics in parasite populations at equilibrium has been limited to verbal arguments or conceptual models. This study focusses on how host–parasite population dynamics affects observed levels of inbreeding in a random sample of parasites from an infinite population of hosts by bridging traditional genetic and parasitological processes utilizing a backward–forward branching Markov process embedded within a flexible statistical framework, the logarithmic-poisson mixture model. My results indicate that levels of inbreeding in parasites are impacted by demographic and/or transmission dynamics (subdivided mating, aggregated transmission dynamics and host spatial structure), and that this inbreeding is poorly estimated by ‘equilibrium’ levels of inbreeding calculated assuming regular systems of mating. Specifically, the model reveals that at low levels of inbreeding (F≤ 0.1), equilibrium levels of inbreeding are lower than those observed, while at high levels of inbreeding the opposite pattern occurs. The model also indicates that inbreeding could have important epidemiological implications (e.g., the spread of recessive drug resistance genes) by directly impacting the observed frequency of rare homozygotes in parasite populations. My results indicate that frequencies of rare homozygotes are affected by aggregated transmission dynamics and host spatial structure, and also that an increase in the frequency of rare homozygotes can be caused by a decrease in effective population size solely due to the presence of a subdivided breeding system.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  • Anderson R. M., May R. M. and Gupta S. 1989 Non-linear phenomena in host-parasite interactions. Parasitology 99, S59– S79.

    Article  PubMed  Google Scholar 

  • Anderson T. J. C., Romeroabal M. E. and Jaenike J. 1995 Mitochondrial DNA and Ascaris microepidemiology - the composition of parasite populations from individual hosts, families and villages. Parasitology 110, 221–229.

    Article  PubMed  Google Scholar 

  • Ascunce M. S., Toups M. A., Kassu G., Fane J., Scholl K. and Reed D. L. 2013 Nuclear genetic diversity in human lice (Pediculus humanus) reveals continental differences and high inbreeding among worldwide populations. PLoS One 8, e57619.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Blouin M. S., Yowell C. A., Courtney C. H. and Dame J. B. 1995 Host movement and the genetic structure of populations of parasitic nematodes. Genetics 141, 1007–1014.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Brown A. H. D. 1979 Enzyme polymorphism in plant-populations. Theor. Pop. Biol. 15, 1–42.

    Article  Google Scholar 

  • Bush A. O., Lafferty K. D., Lotz J. M. and Shostak A. W. 1997 Parasitology meets ecology on its own terms: Margolis et al. revisited. J. Parasitol. 83, 575–583.

    Article  CAS  PubMed  Google Scholar 

  • Caillaud D., Prugnolle F., Durand P., Theron A. and de Meeus T. 2006 Host sex and parasite genetic diversity. Microb. Infect. 8, 2477–2483.

    Article  CAS  Google Scholar 

  • Charlesworth D. and Willis J. H. 2009 Fundamental concepts in genetics: the genetics of inbreeding depression. Nat. Rev. Genet. 10, 783–796.

    Article  CAS  PubMed  Google Scholar 

  • Chevillon C., Koffi B. B., Barre N., Durand P., Arnathau C. and de Meeus T. 2007 Direct and indirect inferences on parasite mating and gene transmission patterns - pangamy in the cattle tick Rhipicephalus (Boophilus) microplus. Infect. Genet. Evol. 7, 298–304.

    Article  CAS  PubMed  Google Scholar 

  • Churcher T. S., Schwab A. E., Prichard R. K. and Basanez M. G. 2008 An analysis of genetic diversity and inbreeding in Wuchereria bancrofti: implications for the spread and detection of drug resistance. PLoS Negl. Trop. Dis. 2, e211.

    Article  PubMed Central  PubMed  Google Scholar 

  • Cornell S. 2005 Modelling nematode populations: 20 years of progress. Trends Parasitol 21, 542–545.

    Article  PubMed  Google Scholar 

  • Cornell S. J., Isham V. S. and Grenfell B. T. 2000 Drug-resistant parasites and aggregated infection - early-season dynamics. J. Math. Biol. 41, 341–360.

    Article  CAS  PubMed  Google Scholar 

  • Cornell S. J., Isham V. S., Smith G. and Grenfell B. T. 2003 Spatial parasite transmission, drug resistance, and the spread of rare genes. Proc. Nat. Acad. Sci. USA 100, 7401–7405.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Criscione C. D. 2008 Parasite co-structure: Broad and local scale approaches. Parasite 15, 439–443.

    Article  CAS  PubMed  Google Scholar 

  • Criscione C. D. and Blouin M. S. 2005 Effective sizes of macroparasite populations: a conceptual model. Trends Parasitol. 21, 212–217.

    Article  PubMed  Google Scholar 

  • Criscione C. D., Poulin R. and Blouin M. S. 2005 Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Mol. Ecol. 14, 2247–2257.

    Article  CAS  PubMed  Google Scholar 

  • Cutulle C., Jonsson N. N. and Seddon J. M. 2010 Multiple paternity in Rhipicephalus (Boophilus) microplus confirmed by microsatellite analysis. Exp. Appl. Acarol. 50, 51–58.

    Article  CAS  PubMed  Google Scholar 

  • de Meeus T., Humair P. F., Grunau C., Delaye C. and Renaud F. 2004 Non-Mendelian transmission of alleles at microsatellite loci: an example in Ixodes ricinus, the vector of Lyme disease. Int. J. Parasitol. 34, 943–950.

    Article  CAS  PubMed  Google Scholar 

  • Desloire S., Moro C. V., Chauve C. and Zenner L. 2006 Comparison of four methods of extracting DNA from D. gallinae (Acari: Dermanyssidae). Vet. Res. 37, 725–732.

    Article  CAS  PubMed  Google Scholar 

  • Dharmarajan G. 2008 Of genes and ticks: the population genetics of Dermacentor variabilis and Ixodes texanus infecting a wildlife host. Doctoral dissertation submitted to Purdue University, West Lafayette, USA.

  • Dharmarajan G. and Rhodes Jr O. E. 2011 Evaluating levels of PCR efficiency and genoty** error in DNA extracted from engorged and non-engorged female Dermacentor variabilis ticks. Med. Vet. Entomol. 25, 109–112.

    Article  CAS  PubMed  Google Scholar 

  • Dharmarajan G., Beasely J. C. and Rhodes J. O. E. 2010 Spatial and temporal factors affecting parasite genotypes encountered by hosts: empirical data from American dog ticks (Dermacentor variabilis) parasitizing raccoons (Procyon lotor). Int. J. Parasitol. 7, 787–795.

    Article  Google Scholar 

  • Dharmarajan G., Beasley J. C. and Rhodes J. O. E. 2011 Heterozygote deficiencies in parasite populations: An evaluation of interrelated hypotheses in the raccoon tick, Ixodes texanus. Heredity 106, 253–260.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dybdahl M. F. and Storfer A. 2003 Parasite local adaptation: red queen versus suicide king. Trends Ecol. Evol. 18, 523–530.

    Article  Google Scholar 

  • Dye 1994 Models for investigating genetic exchange in protozoan populations. In Modelling vector-borne and other parasitic diseases (ed. B. D. Perry and J. W. Hansen), pp. 165–176. ILRAD, Nairobi, Kenya.

  • Guzinski J., Bull C. M., Donnellan S. C. and Gardner M. G. 2009 Molecular genetic data provide support for a model of transmission dynamics in an Australian reptile tick, Bothriocroton hydrosauri. Mol. Ecol. 18, 227–234.

    Article  PubMed  Google Scholar 

  • Hartl D. L. and Clark A. G. 1989 Principles of population genetics. 2nd edition. Sinauer Associates, Sunderland.

  • Hasle G., Roed K. H. and Leinaas H. P. 2008 Multiple paternity in Ixodes ricinus (Acari: Ixodidae), assessed by microsatellite markers. J. Parasitol. 94, 345–347.

    Article  PubMed  Google Scholar 

  • Hedrick P. W. and Cockerham C. C. 1986 Partial inbreeding-equilibrium heterozygosity and the heterozygosity paradox. Evolution 40, 856–861.

    Article  Google Scholar 

  • Keeney D. B., Waters J. M. and Poulin R. 2007 Clonal diversity of the marine trematode Maritrema novaezealandensis within intermediate hosts: the molecular ecology of parasite life cycles. Mol. Ecol. 16, 431–439.

    Article  CAS  PubMed  Google Scholar 

  • Keller L. F. and Waller D. M. 2002 Inbreeding effects in wild populations. Trends Ecol. Evol. 17, 230–241.

    Article  Google Scholar 

  • Lafferty K. D. and Kuris A. M. 2002 Trophic strategies, animal diversity and body size. Trends Ecol. Evol. 17, 507–513.

    Article  Google Scholar 

  • Levins R. 1966 Strategy of model building in population biology. Am. Sci. 54, 421–431.

    Google Scholar 

  • Luo H. Y., Nie P., Zhang Y. A., Yao W. J. and Wang G. T. 2003 Genetic differentiation in populations of the cestode Bothriocephalus acheilognathi (Cestoda, Pseudophyllidea) as revealed by eight microsatellite markers. Parasitology 126, 493– 501.

    Article  CAS  PubMed  Google Scholar 

  • Lymbery A. J. and Thompson R. C. A. 2012 The molecular epidemiology of parasite infections; Tools and applications. Mol. Biochem. Parasitol. 181, 102–116.

    Article  CAS  PubMed  Google Scholar 

  • Mackinnon M. J. and Hastings I. M. 1998 The evolution of multiple drug resistance in malaria parasites. Trans. Roy. Soc. Trop. Med. Hyg. 92, 188–195.

    Article  CAS  PubMed  Google Scholar 

  • Malécot G. 1969. The mathematics of heredity (translated by D. M. Yermanos). Freeman, San Fransico, California.

  • May R. M. 2001 Stability and complexity in model ecosystems. Princeton University Press, Princeton, New Jersey, USA.

    Google Scholar 

  • McCoy K. D., Boulinier T. and Tirard C. 2005 Comparative host-parasite population structures: disentangling prospecting and dispersal in the black-legged kittiwake Rissa tridactyla. Mol. Ecol. 14, 2825–2838.

    Article  CAS  PubMed  Google Scholar 

  • McCoy K. D., Boulinier T., Tirard C. and Michalakis Y. 2003 Host-dependent genetic structure of parasite populations: Differential dispersal of seabird tick host races. Evolution 57, 288–296.

    Article  PubMed  Google Scholar 

  • Mharakurwa S. 2004 Plasmodium falciparum transmission rate and selection for drug resistance: a vexed association or a key to successful control? Int. J. Parasitol. 34, 1483–1487.

    Article  CAS  PubMed  Google Scholar 

  • Nadler S. A. 1995 Microevolution and the genetic structure of parasite populations. J. Parasitol. 81, 395–403.

    Article  CAS  PubMed  Google Scholar 

  • Nadler S. A., Hafner M. S., Hafner J. C. and Hafner D. J. 1990 Genetic differentiation among chewing louse populations (Mallophaga, Trichodectidae) in a pocket gopher contact zone (Rodentia, Geomyidae). Evolution 44, 942–951.

    Article  Google Scholar 

  • Nee S., West S. A. and Read A. F. 2002 Inbreeding and parasite sex ratios. Proc. R. Soc. London., B Biol. 269, 755–760.

    Article  Google Scholar 

  • Nei M. 1975 Molecular population genetics and evolution. North-Holland, Amsterdam.

    Google Scholar 

  • Paul R. E. L., Packer M. J., Walmsley M., Lagog M., Ranfordcartwright L. C., Paru R. and Day K. P. 1995 Mating patterns in malaria parasite populations of Papua New Guinea. Science 269, 1709–1711.

    Article  CAS  PubMed  Google Scholar 

  • Picard D., Scurrah M. and Mugniery D. 2004 Inbreeding and population structure of the potato cyst nematode (Globodera pallida) in its native area (Peru). Mol. Ecol. 13, 2899–2908.

    Article  CAS  PubMed  Google Scholar 

  • Pielou E. C. 1976 Mathematical ecology. Wiley, New York, USA.

    Google Scholar 

  • Plantard O., Picard D., Valette S., Scurrah M., Grenier E. and Mugniery D. 2008 Origin and genetic diversity of Western European populations of the potato cyst nematode (Globodera pallida) inferred from mitochondrial sequences and microsatellite loci. Mol. Ecol. 17, 2208–2218.

    Article  CAS  PubMed  Google Scholar 

  • Price P. W. 1980 Evolutionary biology of parasites. Princeton University Press, Princeton, USA.

    Google Scholar 

  • Rauch G., Kalbe M. and Reusch T. B. H. 2005 How a complex life cycle can improve a parasite’s sex life. J. Evol. Biol. 18, 1069–1075.

    Article  CAS  PubMed  Google Scholar 

  • Redman E., Grillo V., Saunders G., Packard E., Jackson F., Berriman M. and Gilleard J. S. 2008 Genetics of mating and sex determination in the parasitic nematode Haemonchus contortus. Genetics 180, 1877–1887.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rostron J. 1978 Computation of inbreeding coefficients. Ann. Hum. Genet. 41, 469–475.

    Article  CAS  PubMed  Google Scholar 

  • Ruiz-Lopez M. J., Chaskelson S., Gompper M. E. and Eggert L. S. 2012 Multiple paternity in the american dog tick Dermacentor variabilis (acari: Ixodidae). J. Parasitol. 98, 498–501.

    Article  PubMed  Google Scholar 

  • Ryman N. 1994 Supportive breeding and effective population size - differences between inbreeding and variance effective numbers. Conserv. Biol. 8, 888–890.

    Article  Google Scholar 

  • Saleem M. and Gliddon C. J. 1986 Effect of breeding system on the genotypic structure in trifolium species. Pakistan J. Bot. 18, 183–188.

    Google Scholar 

  • Saul A. 1995 Computer-model of the maintenance and selection of genetic-heterogeneity in polygamous helminths. Parasitology 111, 531–536.

    Article  PubMed  Google Scholar 

  • Schmidt K. F. 1995 Malaria research - inbred parasites may spur resistance. Science 269, 1670.

    Article  CAS  PubMed  Google Scholar 

  • Schwab A. E., Churcher T. S., Schwab A. J., Basanez M. G. and Prichard R. K. 2007 An analysis of the population genetics of potential multi-drug resistance in Wuchereria bancrofti due to combination chemotherapy. Parasitology 134, 1025– 1040.

    Article  CAS  PubMed  Google Scholar 

  • Shaw D. J. and Dobson A. P. 1995 Patterns of macroparasite abundance and aggregation in wildlife populations: A quantitative review. Parasitology 111, S111–S133.

    Article  PubMed  Google Scholar 

  • Shaw D. J., Grenfell B. T. and Dobson A. P. 1998 Patterns of macroparasite aggregation in wildlife host populations. Parasitology 117, 597–610.

    Article  PubMed  Google Scholar 

  • Shields M. W. 1982 Philopatry, inbreeding, and the evolution of sex. State University of New York Press, Albany, New York, USA.

    Google Scholar 

  • Sirea C., Durand P., Pointier J. and Theron A. 2001 Genetic diversity of Schistosoma mansoni within and among individual hosts (Rattus rattus): infrapopulation differentiation at microspatial scale. Int. J. Parasitol. 31, 1609–1616.

    Article  Google Scholar 

  • Smith G., Grenfell B. T., Isham V. and Cornell S. 1999 Anthelmintic resistance revisited: under-dosing, chemoprophylactic strategies, and mating probabilities. Int. J. Parasitol 29, 77–91.

    Article  CAS  PubMed  Google Scholar 

  • Sonenshine D. E. 1991 Biology of ticks, Vol. 1. Oxford University Press, New York, USA.

  • Sonenshine D. E. 1993 Biology of ticks, Vol. 2. Oxford University Press, New York, USA.

  • Templeton A. R. 1986 Coadaptation and outbreeding depression. In Conservation biology: the science of scarcity and diversity (ed. M. E. Soule), pp. 105–116. Sinauer Associates, Sunderland, USA.

  • Thiele E. A., Sorensen R. E., Gazzinelli A. and Minchella D. J. 2008 Genetic diversity and population structuring of Schistosoma mansoni in a Brazilian village. Int. J. Parasitol. 38, 389–399.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vilas R., Vazquez-Prieto S. and Paniagua E. 2012 Contrasting patterns of population genetic structure of Fasciola hepatica from cattle and sheep: Implications for the evolution of anthelmintic resistance. Infect. Genet. Evol. 12, 45– 52.

    Article  PubMed  Google Scholar 

  • Waser N. M. and Price M. V. 1989 Optimal outcrossing in Ipomopsis aggregata - seed set and offspring fitness. Evolution 43, 1097–1109.

    Article  Google Scholar 

  • Weisberg M. 2006 Forty years of ‘The strategy’: Levins on model building and idealization. Biol. Philos. 21, 623–645.

    Article  Google Scholar 

  • Wielgoss S., Taraschewski H., Meyer A. and Wirth T. 2008 Population structure of the parasitic nematode Anguillicola crassus, an invader of declining North Atlantic eel stocks. Mol. Ecol. 17, 3478–3495.

    Article  CAS  PubMed  Google Scholar 

  • Zhou C. H., Yuan K., Tang X. L., Hu N. Y. and Peng W. D. 2011 Molecular genetic evidence for polyandry in Ascaris suum. Parasitol. Res. 108, 703–708.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

I thank Gene Rhodes and Saptarshi Guha for early discussions on the model. I also thank the Department of Science and Technology, Government of India for financial support through a Ramanujan Fellowship Grant.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to GUHA DHARMARAJAN.

Additional information

[Dharmarajan G. 2015 Inbreeding in stochastic subdivided mating systems: the genetic consequences of host spatial structure, aggregated transmission dynamics and life history characteristics in parasite populations. J. Genet. 94, xx–xx]

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

DHARMARAJAN, G. Inbreeding in stochastic subdivided mating systems: the genetic consequences of host spatial structure, aggregated transmission dynamics and life history characteristics in parasite populations. J Genet 94, 43–53 (2015). https://doi.org/10.1007/s12041-015-0488-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12041-015-0488-y

Keywords

Navigation