Phenotypic effects of the Y chromosome are variable and structured in hybrids among house mouse recombinant lines

Abstract

Hybrid zones between divergent populations sieve genomes into blocks that introgress across the zone, and blocks that do not, depending on selection between interacting genes. Consistent with Haldane's rule, the Y chromosome has been considered counterselected and hence not to introgress across the European house mouse hybrid zone. However, recent studies detected massive invasion of M. m. musculus Y chromosomes into M. m. domesticus territory. To understand mechanisms facilitating Y spread, we created 31 recombinant lines from eight wild‐derived strains representing four localities within the two mouse subspecies. These lines were reciprocally crossed and resulting F1 hybrid males scored for five phenotypic traits associated with male fitness. Molecular analyses of 51 Y‐linked SNPs attributed ~50% of genetic variation to differences between the subspecies and 8% to differentiation within both taxa. A striking proportion, 21% (frequencies of sperm head abnormalities) and 42% (frequencies of sperm tail dissociations), of phenotypic variation was explained by geographic Y chromosome variants. Our crossing design allowed this explanatory power to be examined across a hierarchical scale from subspecific to local intrastrain effects. We found that divergence and variation were expressed diversely in different phenotypic traits and varied across the whole hierarchical scale. This finding adds another dimension of complexity to studies of Y introgression not only across the house mouse hybrid zone but potentially also in other contact zones.

Sperm quality parameters are increased and asymmetric in house mouse hybrids

“…We replicated the Martincová et al (2019) results for subspecies-specific effects of hybridization on frequency of DSH, where 8 wild-derived strains showed significantly increased frequency of DSH in musculus × domesticus F1 hybrids in comparison with domesticus × musculus F1s. Our extension of DSH data to 29 strains strongly supports that this asymmetric effect is replicable among subspecific crosses.…”

“…Neither of DSH and ASH were distributed normally in F1 hybrids (Shapiro-Wilk normality test, P = 4.38×10 −10 and P < 2.20×10 −16 , respectively). To improve the fit of DSH and ASH to normality we examined two transformations suggested in the literature for sperm head abnormalities: the arcsine square-root transformation (Kawai et al 2006, White et al 2011) and the Box-Cox power transformation utilized by Martincová et al (2019).…”

“…In this paper we explore the replicability and generality of the sperm quality observations for 8 Y haplotypes reported by (Martincová et al 2019). Increasing sample size such that representative genetic variation is captured within each of the subspecies and inter- and intrasubspecific F1 hybrid comparisons we address two questions: (1) Are the proportions of deformed sperm in intersubspecific hybrids different in comparison with intrasubspecific F1 hybrids?…”

“…To explore the conditions of this Y chromosome spread in a wider context we earlier derived 31 recombinant lines from eight wild-derived strains representing four localities within the two mouse subspecies (Martincová et al 2019). These strains were first crossed within either subspecies and subsequently reciprocally crossed to raise intersubspecific hybrids.…”

“…Hierarchical analysis of reproductive traits in F1 hybrids with recombined intrasubspecific genomes revealed that body and testis weights and sperm count differed on local scales (i.e. between localities and strains within subspecies) but not at the intersubspecific level (Martincová et al 2019). On the other hand, two sperm quality traits (frequency of abnormal sperm heads (ASH) and frequency of dissociated sperm heads from tail (DSH)) displayed Y-associated differentiation at the intersubspecific level.…”