Sperm quality, aggressiveness and generation turnover may facilitate unidirectional Y chromosome introgression across the European house mouse hybrid zone.

The widespread and locally massive introgression of Y chromosomes of the eastern house mouse (Mus musculus musculus) into the range of the western subspecies (M. m. domesticus) in Central Europe calls for an explanation of its underlying mechanisms. Given the paternal inheritance pattern, obvious candidates for traits mediating the introgression are characters associated with sperm quantity and quality. We can also expect traits such as size, aggression or the length of generation cycles to facilitate the spread. We have created two consomic strains carrying the non-recombining region of the Y chromosome of the opposite subspecies, allowing us to study introgression in both directions, something impossible in nature due to the unidirectionality of introgression. We analyzed several traits potentially related to male fitness. Transmission of the domesticus Y onto the musculus background had negative effects on all studied traits. Likewise, domesticus males possessing the musculus Y had, on average, smaller body and testes and lower sperm count than the parental strain. However, the same consomic males tended to produce less- dissociated sperm heads, to win more dyadic encounters, and to have shorter generation cycles than pure domesticus males. These data suggest that the domesticus Y is disadvantageous on the musculus background, while introgression in the opposite direction can confer a recognizable, though not always significant, selective advantage. Our results are thus congruent with the unidirectional musculus → domesticus Y chromosome introgression in Central Europe. In addition to some previous studies, they show this to be a multifaceted phenomenon demanding a multidisciplinary approach.

The strength of gut microbiota transfer along social networks and genealogical lineages in the house mouse.

The gut microbiota of vertebrates is acquired from the environment and other individuals, including parents and unrelated conspecifics. In the laboratory mouse, a key animal model, inter-individual interactions are severely limited and its gut microbiota is abnormal. Surprisingly, our understanding of how inter-individual transmission impacts house mouse gut microbiota is solely derived from laboratory experiments. We investigated the effects of inter-individual transmission on gut microbiota in two subspecies of house mice (Mus musculus musculus and M. m. domesticus) raised in a semi-natural environment without social or mating restrictions. We assessed the correlation between microbiota composition (16S rRNA profiles), social contact intensity (microtransponder-based social networks), and mouse relatedness (microsatellite-based pedigrees). Inter-individual transmission had a greater impact on the lower gut (colon and cecum) than on the small intestine (ileum). In the lower gut, relatedness and social contact independently influenced microbiota similarity. Despite female-biased parental care, both parents exerted a similar influence on their offspring's microbiota, diminishing with the offspring's age in adulthood. Inter-individual transmission was more pronounced in M. m. domesticus, a subspecies, with a social and reproductive network divided into more closed modules. This suggests that the transmission magnitude depends on the social and genetic structure of the studied population.

Reinforcement selection acting on the European house mouse hybrid zone.

Behavioural isolation may lead to complete speciation when partial postzygotic isolation acts in the presence of divergent-specific mate-recognition systems. These conditions exist where Mus musculus musculus and M. m. domesticus come into contact and hybridize. We studied two mate-recognition signal systems, based on urinary and salivary proteins, across a Central European portion of the mouse hybrid zone. Introgression of the genomic regions responsible for these signals: the major urinary proteins (MUPs) and androgen binding proteins (ABPs), respectively, was compared to introgression at loci assumed to be nearly neutral and those under selection against hybridization. The preference of individuals taken from across the zone regarding these signals was measured in Y mazes, and we develop a model for the analysis of the transition of such traits under reinforcement selection. The strongest assortative preferences were found in males for urine and females for ABP. Clinal analyses confirm nearly neutral introgression of an Abp locus and two loci closely linked to the Abp gene cluster, whereas two markers flanking the Mup gene region reveal unexpected introgression. Geographic change in the preference traits matches our reinforcement selection model significantly better than standard cline models. Our study confirms that behavioural barriers are important components of reproductive isolation between the house mouse subspecies.

No postnatal maternal effect on male aggressiveness in wild-derived strains of house mice.

Male aggressiveness is a complex behavior influenced by a number of genetic and non-genetic factors. Traditionally, the contribution of each of these factors has been established from experiments using artificially selected strains for high/low aggressive phenotypes. However, little is known about the factors underlying aggressive behavior in natural populations. In this study, we assess the influence of genetic background vs. postnatal maternal environment using a set of cross-fostering experiments between two wild-derived inbred strains, displaying high (STRA, derived from Mus musculus domesticus) and low (BUSNA, derived from Mus musculus musculus) levels of aggressiveness. The role of maternal environment was tested in males with the same genetic background (i.e. strain origin) reared under three different conditions: unfostered (weaned by mother), infostered (weaned by an unfamiliar dam from the same strain), and cross-fostered (weaned by a dam from a different strain). All males were tested against non-aggressive opponents from the A/J inbred strain. Resource-holding potential was assessed through body weight gains and territory ownership. The STRA males were shown to be aggressive in both neutral cage and resident-intruder tests. On the contrary, the BUSNA males were less aggressive in all tests. We did not find a significant effect of postnatal maternal environment; however, we detected significant maternal effect on body weight with differences between the strains, fostering type and interactions between these factors. We conclude that the aggressiveness preserved in the two strains has significant genetic component whose genetic basis can be dissected by quantitative trait loci analysis.

Studies of an Androgen-Binding Protein Knockout Corroborate a Role for Salivary ABP in Mouse Communication.

The house mouse Androgen-binding protein (Abp) gene family is comprised of 64 paralogs, 30 Abpa and 34 Abpbg, encoding the alpha (ABPA) and beta-gamma (ABPBG) protein subunits that are disulfide-bridged to form dimers in secretions. Only 14 Abp genes are expressed in distinct patterns in the lacrimal (11) and submandibular glands (3). We created a knockout mouse line lacking two of the three genes expressed in submandibular glands, Abpa27 and Abpbg27, by replacing them with the neomycin resistance gene. The knockout genotype (-/-) showed no Abpa27 or Abpbg27 transcripts in submandibular gland complementary DNA (cDNA) libraries and there was a concomitant lack of protein expression of ABPA27 and ABPBG27 in the -/- genotype saliva, shown by elimination of these two proteins from the saliva proteome and the loss of cross-reactive material in the acinar cells of the submandibular glands. We also observed a decrease in BG26 protein in the -/- animals, suggesting monomer instability. Overall, we observed no major phenotypic changes in the -/- genotype, compared with their +/+ and +/- siblings raised in a laboratory setting, including normal growth curves, tissue histology, fecundity, and longevity. The only difference is that male and female C57BL/6 mice preferred saliva of the opposite sex containing ABP statistically significantly more than saliva of the opposite sex without ABP in a Y-maze test. These results show for the first time that mice can sense the presence of ABP between saliva targets with and without ABPs, and that they spend more time investigating the target containing ABP.

Assessing multilocus introgression patterns: a case study on the mouse X chromosome in central Europe.

Multilocus hybrid zone (HZ) studies predate genomics by decades. The power of early methods is becoming apparent and now large datasets are commonplace. Relating introgression along a chromosome to evolutionary process is challenging: although reduced introgression regions may indicate speciation genes, this pattern may be obscured by asymmetric introgression of linked invasive genes. Further, HZ movement may form salients and leave islands in its wake. Barton's concordance was proposed 24 years ago for assessing introgression where geographic patterns are complex. The geographic axis of introgression is replaced with the hybrid index. We compare this, a recently proposed genomic clines approach, and two-dimensional (2D) geographic analyses, for 24 X chromosome loci of 2873 mice from the central-European house mouse HZ. In 2D, 14 loci show linear contact, seven precisely matching previous studies. Four show introgression islands to the east of the zone, suggesting past westward zone movement, two show westward salients. Barton's concordance both recovers and refines this information. A region of reduced introgression on the central X is supported, despite X centromere-proximal male-biased westward introgression matching a westward 2D geographic salient. Genomic clines results are consistent regarding introgression asymmetries, but otherwise more difficult to interpret. Evidence for genetic conflict is discussed.