Partnerwahl und Reproduktionsstrategien von differenzierten Populationen der Hausmaus (Mus musculus domesticus)

Population divergence is an important process in the evolution of lineages and can occur rapidly through the interaction of random genetic drift with natural and sexual selection. While natural selection operates on differences in fitness with respect to the local environment, sexual selection acts through pre- and postcopulatory mate choice on the reproductive success of individuals. Recently separated populations of the Western European house mouse Mus musculus domesticus were investigated for mating preferences. The study system consisted of two populations, one sampled in the Cologne/Bonn region, referred to as the “German population” and one from the Massif Central, termed here the “French population”. These populations have been separated for at most 3,000 years. Although this time span is short in evolutionary terms, they already show genetic differentiation. To test whether population divergence is reflected in mate choice, I carried out four replicates of a long-term experiment, in which individually tagged mice of both populations were held for 6 month in a semi-natural enclosure. As controls, I conducted cage experiments, where females could choose between males of both populations during a 6 day period. Paternities in the enclosure populations were determined by microsatellite typing of all individuals and they were used as measures for mate choice and reproductive success. The frequent monitoring of the populations during which animals were examined individually allowed the assessment of their physical condition. Furthermore, I examined the influence of a selfish genetic element, the t haplotype, on pre- or postcopulatory mate choice for the different population backgrounds. Finally, I analyzed whether the population divergence is also reflected in relative frequencies of female strategies such as polyandry and communal breeding. Founder animals of the long-term experiment did not follow a consistent mate choice pattern, while individuals born in the enclosures showed a significant preference for partners who had a father from the same population as themselves. In the controlled cage experiment, there was no consistent preference pattern regarding population background. However, female littermates that grew up in the same cage chose males coming from one population, indicating an environmental influence. These findings are discussed in the context of behavioral and genomic imprinting. German and French founder animals differed slightly in reproductive success. Among the F1 individuals, the comparison of reproductive success between individuals with a mixed population background (i.e. with parents from different populations) versus animals with a pure background (i.e. with parents from the same population) revealed no significant differences. Nevertheless, when looking at the combination of measures for reproductive success, such as offspring number, number of mating events, and offspring per mating, in 5 out of 6 parameters “pure” individuals outperformed the “mixed” individuals, which might indicate a slight decrease in hybrid fitness. No different influences were detected between German, French and hybrid animals regarding the t haplotype or different frequencies of female multiple mating and communal breeding. Influences of the t haplotype were restricted to a slight decrease in offspring number in successful mating events between t/wt animals for all combinations of population backgrounds. Contrary to theoretical assumptions and other experiments, no evidence for an increased multiple mating frequency or avoidance of partners with t/wt was found. Polyandry and communal breeding seemed to be general strategies in females of pure as well as mixed population backgrounds, and both strategies increased in frequency with an increasing population density. Females displaying these strategies had a slightly higher reproductive success in semi-natural conditions: Mothers with litters sired by several males had a higher reproductive success than mothers with only single paternity litters. A higher reproductive success was also detected for females which grew up in communally reared litters. Summarizing the outcome of the study, the recently diverged populations do not vary in partner choice: no differences in mate choice or reproductive strategies were observed. However, females preferred mates that had fathers from the same population as themselves, a pattern which I will call the “father related assortative mating pattern”. This suggests the presence of cues which enable the differentiation between “one’s own population” and “the other population”. In addition, the results gave insights into the benefits of costly female reproductive strategies.Populationsdivergenz ist ein wichtiger evolutionärer Prozess und kann schnell durch das Zusammenwirken von genetischer Drift, natürlicher und sexueller Selektion eintreten. Natürliche Selektion wirkt über unterschiedliche Anpassung an lokale Umweltbedingungen und sexuelle Selektion über Partnerwahl auf den Fortpflanzungserfolg von Individuen. Für die vorliegende Studie habe ich die Partnerwahl in divergierenden Populationen der Westeuropäischen Hausmaus Mus musculus domesticus aus der Köln-Bonner Region (die „deutsche Population") und aus dem Zentralmassiv (die "französische Population") untersucht. Die Populationen sind seit höchstens 3.000 Jahren getrennt. Obwohl eine solche Zeitspanne evolutionär kurz ist, zeigt sich bereits genetische Differenzierung. Ob eine Differenzierung der Populationen auch bei der Partnerwahl zu beobachten ist, habe ich in Langzeitexperimenten untersucht. Dazu habe ich individuell markierte Mäuse beider Populationen für 6 Monate in einem weitestgehend natürlichen Gehege gehalten. Für Kontrollexperimente habe ich ein Käfigsystem genutzt, bei dem Weibchen Kontakt zu Männchen beider Populationen hatten. Die Weibchen konnten über sechs Tage zwischen Männchen beider Populationen wählen; die Männchen hatten keinen Kontakt untereinander. Die Vaterschaften aller Individuen in den Langzeitexperimenten wurden durch Mikrosatelliten-Typisierung als Maß für die Partnerwahl und den Fortpflanzungserfolg bestimmt. Die individuelle Überwachung der Tiere ermöglichte die Aufnahme ihres physischen Zustandes. Untersucht habe ich auch wie eine egoistische Genvariante, der t-Haplotyp auf die Partnerwahl in beiden Populationen wirkt. Schließlich habe ich geprüft, ob sich die Populationsdivergenz auch in relativen Häufigkeiten weiblicher Reproduktionsstrategien wie Polyandrie und gemeinsamer Jungenaufzucht widerspiegelt. Die Gründerindividuen in den Langzeitexperimenten folgten keinem einheitlichen Muster bei der Partnerwahl. Mäuse die in den Gehegen geboren und aufgewachsen waren zeigten dagegen eine signifikante Präferenz für Partner, deren Väter aus derselben Population wie der eigene Vater stammte. Das Experiment im Käfigsystem lieferte keine einheitlichen Präferenzen in Bezug auf Populationszugehörigkeit. Bemerkenswert jedoch ist, dass Schwestern, die gemeinsam in einem Käfig aufgewachsen waren Männchen aus derselben Population bevorzugten. Diese Ergebnisse werden im Kontext von ethologischer und genetischer Prägung diskutiert. Einzelne Parameter zum Fortpflanzungserfolg (z.B. Anzahl der Nachkommen, Anzahl der erfolgreichen Verpaarungen, Nachkommen pro Verpaarung) unterschieden sich nicht signifikant im Vergleich von Tieren mit Eltern aus den verschieden Populationen („Hybride“) und Tieren mit Eltern aus der jeweils gleichen Population. Die Kombination der Parameter jedoch zeigte, dass in 5 von 6 Fällen die Nachkommen von Eltern aus der gleichen Population die Hybriden übertrafen. Dies weist auf eine leichte Abnahme der Hybrid-Fitness hin. Ein unterschiedlicher Einfluss des t-Haplotypen auf Partnerwahl oder Verpaarungsverhalten von Weibchen wurde zwischen deutschen und französischen Mäusen und Hybriden nicht gefunden. Der einzig beobachtbare und statistisch signifikante Einfluss dieser egoistischen Genvariante besteht in einem leichten Rückgang der Nachkommenanzahl in erfolgreichen Verpaarungen zwischen Tieren die heterozygot für den t-Haplotypen waren. Im Gegensatz zu theoretischen Annahmen und Experimenten anderer Wissenschaftler habe ich keine Hinweise auf erhöhte Polyandrie oder die Vermeidung von Partnern mit t/wt gefunden. Polyandrie und gemeinsame Weibchenaufzucht scheinen allgemeine Strategien von Weibchen zu sein. Beides trat vermehrt mit zunehmender Bevölkerungsdichte auf. Beide Strategien erhöhten leicht den individuellen Fortpflanzungserfolg im Langzeitexperiment: Weibchen, die Würfe von gleichzeitig mehreren Männchen hatten, zeigten einen höheren Reproduktionserfolg als Weibchen die nur Würfe hatten, die von jeweils einem Männchen gezeugt wurden. Ein höherer Fortpflanzungserfolg wurde auch bei Weibchen gefunden, die aus gemeinschaftlich aufgezogegnen Würfen stammten. Zusammenfassend lässt sich feststellen, dass zwischen den untersuchten Populationen keine Unterschiede in Partnerwahl und Fortpflanzungsstrategien beobachtet wurden. Weibchen präferieren jedoch Männchen, deren Väter von der gleichen Population kommen wie ihr eigener Vater, ein Phänomen, das ich als „vaterbezogene assortative Präferenz“ bezeichne. Dies deutet auf die Existenz von Merkmalen hin, die ein Unterscheiden zwischen "eigener Population" und "anderer Population" möglich machen. Darüber hinaus gaben die Ergebnisse Einblicke in Vorteile durch kostspielige weibliche Reproduktionsstrategien

Genomic resources for wild populations of the house mouse, Mus musculus and its close relative Mus spretus

WOS: 000390231600001PubMed ID: 27622383Wild populations of the house mouse (Mus musculus) represent the raw genetic material for the classical inbred strains in biomedical research and are a major model system for evolutionary biology. We provide whole genome sequencing data of individuals representing natural populations of M. m. domesticus (24 individuals from 3 populations), M. m. helgolandicus (3 individuals), M. m. musculus (22 individuals from 3 populations) and M. spretus (8 individuals from one population). We use a single pipeline to map and call variants for these individuals and also include 10 additional individuals of M. m. castaneus for which genomic data are publically available. In addition, RNAseq data were obtained from 10 tissues of up to eight adult individuals from each of the three M. m. domesticus populations for which genomic data were collected. Data and analyses are presented via tracks viewable in the UCSC or IGV genome browsers. We also provide information on available outbred stocks and instructions on how to keep them in the laboratory.Max-Planck Society; DFG [HA 3139/4-1]; ERC [322564]; contract-research-project for the Bundeswehr Medical Service [M/SABX/005]This work was mostly financed by institutional resources of the Max-Planck Society, a DFG grant to B.H. and M.T. (HA 3139/4-1) and an ERC grant to D.T. (NewGenes, 322564). We thank Sonja Ihle, Susanne Krochter, Ruth Rottscheidt for contributing to collecting animals in the wild and our animal care takers for active involvement of optimizing the scheme for wild mouse keeping. The initial analysis of mice from Afghanistan was funded by contract-research-project for the Bundeswehr Medical Service M/SABX/005. We thank Bastian Pfeifer for help with software package PopGenome, Leslie Turner for discussion and Daniel M. Hooper and Trevor Price for helpful comments on the manuscript. D.T. had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis

Genomic resources for wild populations of the house mouse, Mus musculus and its close relative Mus spretus

Belgium Herbarium image of Meise Botanic Garden

Data from: Paternal Imprinting of Mating Preferences Between Natural Populations of House Mice (Mus musculus domesticus)

The evolutionary divergence of cues for mate recognition can contribute to early stages of population separation. We compare here two allopatric populations of house mice (Mus musculus domesticus) that have become separated about 3000 years ago. We have used paternity assignments in semi-natural environments to study the degree of mutual mate recognition according to population origin under conditions of free choice and overlapping generations. Our results provide insights into the divergence of mating cues, but also for the mating system of house mice. We find frequent multiple mating, occurrence of inbreeding and formation of extended family groups. In addition, many animals show strong mate fidelity, that is, frequent choice of the same mating partners in successive breeding cycles, indicating a role for familiarity in mating preference. With respect to population divergence, we find evidence for assortative mating, but only under conditions where the animals had time to familiarize themselves with mating partners from their own population. Most interestingly, the first-generation offspring born in the enclosure showed a specific mating pattern. Although matings between animals of hybrid population origin with animals of pure population origin should have occurred with equal frequency with respect to matching the paternal or maternal origin, paternal matching with mates from their own populations occurred much more often. Our findings suggest that paternally imprinted cues play a role in mate recognition between mice and that the cues evolve fast, such that animals of populations that are separated since not more than 3000 years can differentially recognize them

datatables

Excel file with three tables; the first table lists details for all matings evaluated, including all mating partner IDs and associated information from the monitoring surveys. The second table is a subset of the first table restricted to all matings among F1 animals that were born in the enclosure. The third table is a subset of the second table, restricted to all first matings only

all mice in experiment

List of all mice that were collected and genotyped. Only animals with clear assignments were used for generating the mating data presented in the file "datatables.xls

Meta-populational demes constitute a reservoir for large MHC allele diversity in wild house mice (Mus musculus)

Abstract Background The MHC class I and II loci mediate the adaptive immune response and belong to the most polymorphic loci in vertebrate genomes. In fact, the number of different alleles in a given species is often so large that it remains a challenge to provide an evolutionary model that can fully account for this. Results We provide here a general survey of MHC allele numbers in house mouse populations and two sub-species (M. m. domesticus and M. m. musculus) for H2 class I D and K, as well as class II A and E loci. Between 50 and 90% of the detected different sequences constitute new alleles, confirming that the discovery of new alleles is indeed far from complete. House mice live in separate demes with small effective population sizes, factors that were proposed to reduce, rather than enhance the possibility for the maintenance of many different alleles. To specifically investigate the occurrence of alleles within demes, we focused on the class II H2-Aa and H2-Eb exon 2 alleles in nine demes of M. m. domesticus from two different geographic regions. We find on the one hand a group of alleles that occur in different sampling regions and three quarters of these are also found in both sub-species. On the other hand, the larger group of different alleles (56%) occurs only in one of the regions and most of these (89%) only in single demes. We show that most of these region-specific alleles have apparently arisen through recombination and/or partial gene conversion from already existing alleles. Conclusions Demes can act as sources of alleles that outnumber the set of alleles that are shared across the species range. These findings support the reservoir model proposed for human MHC diversity, which states that large pools of rare MHC allele variants are continuously generated by neutral mutational mechanisms. Given that these can become important in the defense against newly emerging pathogens, the reservoir model complements the selection based models for MHC diversity and explains why the exceptional diversity exists

Genetic differentiation of hypothalamus parentally biased transcripts in populations of the house mouse implicate the prader-willi syndrome imprinted region as a possible source of behavioral divergence

Parentally biased expression of transcripts (genomic imprinting) in adult tissues, including the brain, can influence and possibly drive the evolution of behavioral traits. We have previously found that paternally determined cues are involved in population-specific mate choice decisions between two populations of the Western house mouse (Mus musculus domesticus). Here, we ask whether this could be mediated by genomically imprinted transcripts that are subject to fast differentiation between these populations. We focus on three organs that are of special relevance for mate choice and behavior: The vomeronasal organ (VNO), the hypothalamus, and the liver. To first identify candidate transcripts at a genome-wide scale, we used reciprocal crosses between M. m. domesticus and M. m. musculus inbred strains and RNA sequencing of the respective tissues. Using a false discovery cutoff derived from mock reciprocal cross comparisons, we find a total of 66 imprinted transcripts, 13 of which have previously not been described as imprinted. The largest number of imprinted transcripts were found in the hypothalamus; fewer were found in the VNO, and the least were found in the liver. To assess molecular differentiation and imprinting in the wild-derived M. m. domesticus populations, we sequenced the RNA of the hypothalamus from individuals of these populations. This confirmed the presence of the above identified transcripts also in wild populations and allowed us to search for those that show a high genetic differentiation between these populations. Our results identify the Ube3a-Snrpn imprinted region on chromosome 7 as a region that encompasses the largest number of previously not described transcripts with paternal expression bias, several of which are at the same time highly differentiated. For four of these, we confirmed their imprinting status via single nucleotide polymorphism-specific pyrosequencing assays with RNA from reciprocal crosses. In addition, we find the paternally expressed Peg13 transcript within the Trappc9 gene region on chromosome 15 to be highly differentiated. Interestingly, both regions have been implicated in Prader-Willi nervous system disorder phenotypes in humans. We suggest that these genomically imprinted regions are candidates for influencing the population-specific mate-choice in mice