Barbora Vošlajerová Bímová

GENETIC ANALYSIS OF AUTOSOMAL AND X‐LINKED MARKERS ACROSS A MOUSE HYBRID ZONE

Abstract In this paper, we present results of the first comprehensive study of the introgression of both autosomal and sex-chromosome markers across the central European portion of the hybrid zone between two house mouse subspecies, Mus musculus musculus and M. m. domesticus. More than 1800 individuals sampled from 105 sites were analyzed with a set of allozyme loci (hopefully representing neutral or nearly neutral markers) and X-linked loci (which are assumed to be under selection). The zone center is best modeled as a single straight line independent of fine-scale local geographic or climatic conditions, being maintained by a balance between dispersal and selection against hybrids. The width (w) of the multilocus autosomal cline was estimated as 9.6 km whereas the estimate for the compound X-chromosome cline was about 4.6 km only. As the former estimate is comparable to that of the Danish portion of the zone (assumed to be much younger than the central European one), zone width does not appear to be related to its age. The strength (B) of the central barrier was estimated as about 20 km; with dispersal (σ) of about 1 km/gen1/2, this means effective selection (s*) is approximately 0.06–0.09 for autosomal loci and about 0.25 for X-linked loci. The number of loci under selection was estimated as N = 56–99 for autosomes and about 380 for X-linked loci. Finally, we highlight some potential pitfalls in hybrid zone analyses and in comparisons of different transects. We suggest that conclusions about parts of the mouse genome involved in reproductive isolation and speciation should be drawn with caution and that analytical approaches always providing some estimates should not be used without due care regarding the support or confidence of such estimates, especially if conclusions are based on the difference between these estimates. Finally, we recommend that analysis in two-dimensional space, dense sampling, and rigorous treatment of data, including inspection of likelihood profiles, are essential for hybrid zone studies.

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.

Genetic conflict outweighs heterogametic incompatibility in the mouse hybrid zone

BackgroundThe Mus musculus musculus/M. m. domesticus contact zone in Europe is characterised by sharp frequency discontinuities for sex chromosome markers at the centre of wider clines in allozyme frequencies.ResultsWe identify a triangular area (approximately 330 km2) where the musculus Y chromosome introgresses across this front for up to 22 km into domesticus territory. Introgression of the Y chromosome is accompanied by a perturbation of the census sex ratio: the sex ratio is significantly female biased in musculus localities and domesticus localities lacking Y chromosome introgression. In contrast, where the musculus Y is detected in domesticus localities, the sex ratio is close to parity, and significantly different from both classes of female biased localities. The geographic position of an abrupt cline in an X chromosome marker, and autosomal clines centred on the same position, seem unaffected by the musculus Y introgression.ConclusionWe conclude that sex ratio distortion is playing a role in the geographic separation of speciation genes in this section of the mouse hybrid zone. We suggest that clines for genes involved in sex-ratio distortion have escaped from the centre of the mouse hybrid zone, causing a decay in the barrier to gene flow between the two house mouse taxa.

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. Bartons 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. Bartons 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.

Signalling components of the house mouse mate recognition system

Subspecies-specific mate recognition may represent significant barrier to gene flow between diverged genomes potentially leading to speciation. In the house mouse, assortative mating involves the coevolution of several signals and receptors. We compared signalling ability of bedding material, faeces, urine, saliva, salivary androgen binding proteins (ABP) and combinations of urine with saliva and urine with ABP in mate choice in two wild-derived inbred strains (one of Mus musculus musculus and one of Mus musculus domesticus origin). We observed high levels of variation in assortative preferences between the two strains and sexes. The strongest preferences were observed in M. m. musculus-derived individuals in tests where urine was present either alone or as part of a composite signal target. M. m. domesticus-derived mice displayed strain-specific preferences for faeces. Saliva was the least preferred stimulus in both strains and sexes. No effect of two-compound cues was detected. We conclude that there is divergence across both the stimulus and preference parts of the recognition system for both house mouse strains. Of the tested stimuli, those that have the capacity to carry a signal for extended periods under natural conditions (such as urine and faeces) seem to be the most important substances in strain-specific recognition.

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.

Is water really a barrier for the house mouse? A comparative study of two mouse subspecies

Abstract. House mice are believed to be, unlike rats, only reluctant swimmers. If water is a barrier to mouse dispersal water bodies and streams can have a substantial impact on the genetic structure of populations. Previous studies revealed influence of rivers on the position and structure of the European hybrid zone between two house mouse subspecies, Mus musculus musculus and M. m. domesticus. In this study, we used a simple motivation experiment to test the disposition of both wild and inbred mice representing the subspecies to overcome a water barrier. As the more dispersing sex, males were chosen for the experiment. Mice were tested under two air/water temperature regimes, 20 °C and 10 °C. Contrary to a common belief tested animals entered water rather easily, often even engaging in repeated swimming. We found significant differences in scored behavioural parameters between the subspecies. Under the 20 °C regime, both wild and inbred domesticus males entered and crossed the water earlier and more often swam even when satiated. Strikingly, under the 10 °C regime, the results were rather equivocal but with the opposite tendencies, with musculus males being more willing to swim. We discuss implications of these findings for the hybrid zone dynamics.