Abstract

Host‐parasite interaction studies across hybrid zones often focus on host genetic variation, treating parasites as homogeneous. ‘Intimately’ associated hosts and parasites might be expected to show similar patterns of genetic structure. In the literature, factors such as no intermediate host and no free‐living stage have been proposed as ‘intimacy’ factors likely constraining parasites to closely follow the evolutionary history of their hosts. To test whether the whipworm, Trichuris muris, is intimately associated with its house mouse host, we studied its population genetics across the European house mouse hybrid zone (HMHZ) which has a strong central barrier to gene flow between mouse taxa. T. muris has a direct life cycle and nonmobile free stage: if these traits constrain the parasite to an intimate association with its host we expect a geographic break in the parasite genetic structure across the HMHZ. We genotyped 205 worms from 56 localities across the HMHZ and additionally T. muris collected from sympatric woodmice (Apodemus spp.) and allopatric murine species, using mt‐COX1, ITS1‐5.8S‐ITS2 rDNA and 10 microsatellites. We show four haplogroups of mt‐COX1 and three clear ITS1‐5.8S‐ITS2 clades in the HMHZ suggesting a complex demographic/phylogeographic history. Microsatellites show strong structure between groups of localities. However, no marker type shows a break across the HMHZ. Whipworms from Apodemus in the HMHZ cluster, and share mitochondrial haplotypes, with those from house mice. We conclude Trichuris should not be regarded as an ‘intimate’ parasite of the house mouse: while its life history might suggest intimacy, passage through alternate hosts is sufficiently common to erase signal of genetic structure associated with any particular host taxon.

Highlights

  • It has been suggested that the short generation time, and potential for rapid divergence, of parasites relative to their hosts means the genetic structure of ‘intimate’ parasites can be used to resolve recent divisions in host populations

  • We addressed the following questions: (1) Is there a break in the population genetic structure of T. muris across the house mouse hybrid zone (HMHZ)? (2) Do the ITS1-5.8S-ITS2 rDNA lineages found in the HMHZ correspond to the western and eastern clades previously suggested across Europe; (3) Does T. muris show population structure at the murine species/locality level? (4) What is the inferred role of other sympatric murine host species in the transmission of T. muris across the HMHZ?

  • Intermediate host, a nonmobile free-living phase) are predictive of the parasite’s genetic structure across the European house mouse hybrid zone, or if, in contrast; (2) the frequency of T. muris passage through alternative hosts is sufficient to break any potential signal of intimate association with the house mouse host

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Summary

Introduction

It has been suggested that the short generation time, and potential for rapid divergence, of parasites relative to their hosts means the genetic structure of ‘intimate’ parasites can be used to resolve recent divisions in host populations (review in Whiteman and Parker 2005; Nieberding and Olivieri 2007). No intermediate host and a lack of free-living stage are suggested as ‘intimacy’ factors likely to constrain parasites to closely follow the demo- and phylo-geographic history of their hosts (Nieberding and Olivieri 2007). Using parasites to resolve host divisions requires an understanding of the balance between these opposing forces: barriers to the passage of parasites between host taxa versus mechanisms allowing such passage.

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