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

Abstract

Genetic diversity in animal immune systems is usually beneficial. In hybrid recombinants, this is less clear, as the immune system could also be impacted by genetic conflicts. In the European house mouse hybrid zone, the long‐standing impression that hybrid mice are more highly parasitized and less fit than parentals persists despite the findings of recent studies. Working across a novel transect, we assessed infections by intracellular protozoans, Eimeria spp., and infections by extracellular macroparasites, pinworms. For Eimeria, we found lower intensities in hybrid hosts than in parental mice but no evidence of lowered probability of infection or increased mortality in the centre of the hybrid zone. This means ecological factors are very unlikely to be responsible for the reduced load of infected hybrids. Focusing on parasite intensity (load in infected hosts), we also corroborated reduced pinworm loads reported for hybrid mice in previous studies. We conclude that intensity of diverse parasites, including the previously unstudied Eimeria, is reduced in hybrid mice compared to parental subspecies. We suggest caution in extrapolating this to differences in hybrid host fitness in the absence of, for example, evidence for a link between parasitemia and health.

Coupling between tolerance and resistance for two related Eimeria parasite species

“…we found in the present study, resistance and tolerance are decoupled, this can be misleading. In our host system, the house mice, for example, it has been shown that hybrids between M. m. domesticus and M. m. musculus are more resistant to parasites (Baird et al, 2012;Balard et al, 2020), including Eimeria, but tolerance could not be measured under natural conditions (Balard et al, 2020). The effect of parasites on host fitness in the evolution of the house mouse hybrid zone is thus still rather ambiguous (Baird & Goüy de Bellocq, 2019).…”

Coupling between tolerance and resistance for two related Eimeria parasite species

“…If, as we found in the present study, resistance and tolerance are decoupled this can be misleading. In our host system, the house mice, for example, it has been shown that hybrids between M. m. domesticus and M. m. musculus are more resistant to parasites (Baird et al 2012; Balard et al 2020), including Eimeria , but tolerance could not be measured under natural conditions (Balard et al 2020). The effect of parasites on host fitness in the evolution of the house mouse hybrid zone is thus still rather ambiguous (Baird and Goüy de Bellocq 2019).…”

“…The parasite isolates belong to both the most prevalent Eimeria species in this area, namely E. ferrisi (isolate Brandenburg64) and E. falciformis (isolate Brandenburg88)(Jarquín-Díaz et al 2019). Isolate Brandenburg64 was isolated in a 92% M. m. domesticus individual (hybrid index (HI) = 0.08: Proportion of M. m. musculus alleles in a set of 14 diagnostic markers, see Balard et al (2020)) and isolate Brandenburg88 in a 80% M. m. domesticus (HI=0.2). Pre-patency and the peak day of parasite shedding for these isolates were estimated during infection in NMRI laboratory mice (Al-khlifeh et al 2019) which were also used for serial passaging of the isolates.…”

“…Hybrids between M. m. domesticus and M. m. musculus are used in the present study solely to increase statistical power for comparisons among strains (such as resistance-tolerance correlations). In the future, analyses of a hybrid effect (Balard et al 2020) could investigate tolerance and resistance employing a larger panel of such hybrid strains allowing statistical analysis of an outbreeding effect. Two parental strains represented M. m. domesticus : SCHUNT (Locality: Schweben, Hessen, Germany [N: 5°0 26’, E: 9° 36’] (Martincová et al 2019)) and STRA (Locality: Straas, Bavaria, Germany [N: 50° 11’, E: 11° 46’] (Piálek et al 2008), and two derived from M. m. musculus : BUSNA (Locality: Buškovice, Bohemia, Czech Republic [N: 5°0 14’, E: 1°3 22’] (Piálek et al 2008)) and PWD (Locality: Kunratice, Bohemia, Czech Republic [N: 5°0 01’, E: 14 2°9’] (Gregorová and Forejt 2000)).…”

“…(A) Map showing locations at which mice were collected for breeding of mouse strains and isolation of parasites. The purple line is an estimation of the center of the house mouse hybrid zone between M. m. domesticus and M. m. musculus based on sampling and genotyping of mice in this area (Balard et al 2020; Ďureje et al 2012; Macholán et al 2019). (B) The eight mouse groups (parents and F1s) used in our experimental infections.…”