Recombination does not generate pinworm susceptibility during experimental crosses between two mouse subspecies

Abstract

The susceptibility to Aspiculuris tetraptera of European Mus musculus hybrids is thought to reflect the disruption of genomic co-adaptation through recombination of the parental genomes. Here, we compared the susceptibility to this parasite between parents and experimental hybrids (intersubspecific until F4, intrasubspecific F1, F2) to clarify the contributions of heterosis and subspecies incompatibility. F1 showed hybrid vigor. Unlike intrasubspecific F2, intersubspecific F2 were less resistant than F1, but revealed no increased susceptibility relative to the parents. Intersubspecific F3 and F4 showed the same hybrid vigor as F1. Heterosis contributed most to the resistance, but the differences between intra- and intersubspecific F2 suggested genomic incompatibilities between subspecies. However, the susceptibility did not increase through the recombination process, showing that disruption of co-adaptation does not directly affect resistance. Even if previous studies still support the selective role of parasites in the current hybrid zone, an alternative hypothesis on the origin of hybrid susceptibility is warranted.

Where Are the Wormy Mice? A Reexamination of Hybrid Parasitism in the European House Mouse Hybrid Zone

“…In all cases, we find significant taxon differences. Our results are consistent with experimental infection of domesticus and musculus mouse strains and their hybrids (from F1 to F4) in controlled conditions with the pinworm A. tetraptera (Derothe et al 2004), which showed either significantly reduced load (F1, F3, F4) or no significant effect (F2).…”

“…Returning to the first of these three issues: we have suggested coadaption among immune genes is unlikely if they are using recombination to run a Red Queen race against parasites. Even if recombination is not breaking up coadapted gene complexes (Derothe et al 2004), there is still reason to expect hybridization to produce suboptimal genotypes. This is because hybridization involves admixture of alleles that have never coexisted in the same population.…”

“…Subsequent to the 1986 and 1991 studies, experimental infections of individuals from the original taxa and crosses (from F1 to F4) were carried out with the pinworm Aspiculuris tetraptera. These failed to reproduce high worm loads in the hybrids, in fact showing reduced hybrid load (Derothe et al 2004). Finally, it should be noted that the definition of a hybrid varies across these studies.…”

The Variable Genomic Architecture of Isolation Between Hybridizing Species of House Mice

“…Our results illustrate the importance of using a combination of studies of natural populations and laboratory studies in constructing a model of speciation. More detailed studies of the hybrid genomes, including denser sampling of the genome in a greater number of hybrid mice, will help illuminate the specific mode of selection acting to create isolation between these taxa and complementary studies on fitness and behavior of mice from the hybrid zone, such as studies of hybrid sterility (Forejt and Ivanyi 1975; Storchova et al 2004; Britton‐Davidian et al 2005; Vyskocilova et al 2005; Good et al 2008a,b), mate choice preference (Laukaitis et al 1997; Talley et al 2001; Smadja and Ganem 2002; Smadja et al 2004; Bimova et al 2005), and susceptibility to parasites (Sage et al 1986a; Moulia et al 1993; Derothe et al 2001; Derothe et al 2004), may help link specific phenotypes to the patterns of introgression documented here.…”

Intensity of infection with intracellular Eimeria spp. and pinworms is reduced in hybrid mice compared to parental subspecies

“…Infection experiments using the protozoan Sarcocystis muris led to a similar conclusion (Derothe, Le Brun, Loubes, Perriat‐Sanguinet, & Moulia, ). Other laboratory experiments, however, showed either no effect in inter‐subspecies F1s on helminth load or even reduced load in inter‐subspecies F1s compared to pure mouse strains (Derothe, Porcherie, Perriat‐Sanguinet, Loubès, & Moulia, ; Moulia, Le Brun, Loubes, Marin, & Renaud, ). In 2012, more than two decades after the original field studies (Moulia et al, ; Sage et al, ), Baird et al found (with much larger sample size, clearer sampling design and more up to date inference) reduced helminth loads in hybrid mice (Baird et al, ), especially for the pinworms Aspiculuris tetraptera and Syphacia obvelata and the whipworm Trichuris muris .…”