Revisiting density-dependent fecundity in schistosomes using sibship reconstruction

PLoS Negl Trop Dis. 2021 May 13;15(5):e0009396. doi: 10.1371/journal.pntd.0009396. eCollection 2021 May.

Abstract

The stability of parasite populations is regulated by density-dependent processes occurring at different stages of their life cycle. In dioecious helminth infections, density-dependent fecundity is one such regulatory process that describes the reduction in egg production by female worms in high worm burden within-host environments. In human schistosomiasis, the operation of density-dependent fecundity is equivocal and investigation is hampered by the inaccessibility of adult worms that are located intravascularly. Current understanding is almost exclusively limited to data collected from two human autopsy studies conducted over 40 years ago, with subsequent analyses having reached conflicting conclusions. Whether egg production is regulated in a density-dependent manner is key to predicting the effectiveness of interventions targeting the elimination of schistosomiasis and to the interpretation of parasitological data collected during monitoring and evaluation activities. Here, we revisit density-dependent fecundity in the two most globally important human Schistosoma spp. using a statistical modelling approach that combines molecular inference on the number of parents/adult worms in individual human hosts with parasitological egg count data from mainland Tanzania and Zanzibar. We find a non-proportional relationship between S. haematobium egg counts and inferred numbers of female worms, providing the first clear evidence of density-dependent fecundity in this schistosome species. We do not find robust evidence for density-dependent fecundity in S. mansoni because of high sensitivity to some modelling assumptions and the lower statistical power of the available data. We discuss the strengths and limitations of our model-based analytical approach and its potential for improving our understanding of density dependence in schistosomiasis and other human helminthiases earmarked for elimination.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Female
  • Fertility*
  • Humans
  • Male
  • Models, Statistical
  • Parasite Egg Count
  • Schistosoma haematobium / genetics
  • Schistosoma haematobium / physiology*
  • Schistosoma mansoni / genetics
  • Schistosoma mansoni / physiology*
  • Schistosomiasis haematobia / parasitology*
  • Schistosomiasis mansoni / parasitology*
  • Tanzania

Grants and funding

This article is to be published and paid by Chronos under the Gates Foundation Open Access Policy under OPP 50816 Schistosomiasis Consortium for Operational Research and Evaluation (SCORE). MIN acknowledges funding from a Royal Veterinary College, University of London PhD Studentship. CMG acknowledges funding from a Royal Society Dorothy Hodgkin Clore Fellowship. Collection and primary analyses of the mainland Tanzania dataset was funded by The Royal Society and The Bill and Melinda Gates Foundation (BMGF) via the Schistosomiasis Control Initiative (PI: JPW) and of the Zanzibar dataset, by the BMGF via University of Georgia Research Foundation, Inc (UGARF) for the Schistosomiasis Consortium for Operational Research and Evaluation (SCORE) project (Population Genetics Grant Refs RR374-053/5054146 & RR374-053/4785426 PI: JPW). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.