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Frontiers in Zoology volume 14Article : 38 Cite this article. Metrics details. In many animal species, interactions between individuals of different sex often occur in the context of courtship and mating. During these interactions, a specific mating partner can be chosen. By discriminating potential mates according to specific characteristics, individuals can increase their evolutionary fitness in terms of reproduction and offspring survival.
In this study, we monitored the partner preference behaviour of female and male wild house mice Mus musculus domesticus from populations in Germany G and France F in a controlled cage setup for 5 days and six nights. We analysed the effects of individual factors e. Selectivity was stronger in mice with a pure population background than mixed individuals. Furthermore, female mice with a father from the German population had stronger selectivity than other mice.
In all mice, selectivity followed a clear temporal pattern: it was low in the beginning and reached its maximum only after a whole day in the experiment.
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After two days, mice seemed to have chosen their preferred partner, as this choice was stable for the remaining four days in the experiment. Our study supports earlier findings that mate choice behaviour in wild mice can be paternally influenced.
In our study, preference seems to be potentially associated with paternal MHC distance.
Furthermore, our experiments show that preferences can change after the first day of encounter, which implies that extended observation times might be required to obtain that allow a valid ecological interpretation. In social animals, individuals interact with each other in a broad range of different situations. Interactions between individuals of different sex often occur in the context of courtship, pair bonding, and mating.
No speed dating please! patterns of social preference in male and female house mice
A preference for some possible social partners over others can ultimately lead to mate choice. The evolution of mate choice is assumed to be driven by several mechanisms [ 1 ], such as preferences for direct or indirect phenotypic benefits and genetic correlations between mating preferences and preferred traits [ 2 ]. Selective mating is meant to increase the evolutionary fitness of individuals in terms of reproduction and offspring survival [ 13456 ].
Consequently, different mating strategies have evolved. Assortative mating from the reproduction of phenotypically or genotypically matching mates and promotes population differentiation [ 78 ]. In contrast, disassortative mating occurs when individuals prefer dissimilar mates compared to neutral expectations [ 9101112 ]. The latter strategy maintains or even increases genetic variability and counteracts possible disadvantages due to inbreeding depression e.
In mice Mus musculus sp. Chemical als used are volatiles i. Acoustic communication occurs via ultrasonic vocalisation [ 161718 ]. Since Yamazaki and colleagues [ 20 ] detected MHC-related mating preferences in laboratory mice, many studies have reported an influence of MHC loci on mate choice in nearly all classes of vertebrates [ 21 ].
An important pre-requisite for MHC-based mate choice in mice is the ability to identify and discriminate potential partners based on MHC alleles. Several studies have analysed the influence of MHC on partner choice for house mice.
They mostly support the hypothesis of disassortative mating [ 2324 ] and raised evidence for familial imprinting [ 2325 ]. Familial imprinting is the non-genetical transmission i. Wild mice offer a perfect model system to study the behavioural and genetic basis of mate choice, since they are still far more natural than common laboratory mouse strains in both aspects.
Due to the vast amount of studies on lab mice, numerous genetic tools are available and can be also applied for studies in wild mice. Examples of such study populations are two originally wild caught populations of M. This separation is reflected in the divergence of the nuclear genome and gene expression differences [ 272829 ], as well as in ultrasonic vocalisation [ 30 ]. Montero and colleagues [ 31 ] studied the degree of mutual mate recognition according to population origin under semi-natural conditions and identified complex mating patterns in these two populations.
Assortative mating according to population background was only observed when mice of the single populations could get familiar with each other before individuals of both populations had the chance to meet.
Further, the mating patterns observed were based on paternally influenced mate preferences, such that mice with a father from the French population preferred mating with a partner from that population, individuals fathered by a German male preferred mating with an individual from the German population. The authors suggested genomic or familial imprinting as being involved.
The aim of the present study is to reveal possible factors that determine the mating patterns found by Montero et al. We studied the exact two mouse populations mentioned to shed light on the evolution of mate choice in the early phase of population differentiation. By using a controlled cage setup, we were able to follow single focal individuals during their decision making processes and analyse the persistency of their choices.
To offer the same possible mates as in the study by Montero and colleagues [ 31 ], focal mice were allowed to choose between four partners of either the same or different population origins France and Germany or reciprocal crosses of both.
Focal mice were females and males of the same four genotypes. We aimed to confirm the findings of preferences for paternally matching population backgrounds. In order to do so we investigated three different aspects of mouse behaviour in our setup, i general activity of the focal mice, ii their degree of selectivity i. The mice used for this study originate from two M.
At the time of the experiment, mice from the French population were in the 8th, mice from the German population in the 6th and 7th generation. A specific breeding has been set up for this experiment and we obtained experimental mice from 15 breeding pairs.
All mice were kept and raised under standard conditions together with both parents until weaning at the age of four weeks.
Female and male offspring were kept separated after weaning to ensure no sexual experience before the experiment. We had a balanced system of experimental mice: six females and males per genotype GG, FF, GF, FGwhich in a total of 48 mice in the behavioural experiment. For genetic analyses, we additionally included the parents of the focal mice and some siblings that had not been used in the behavioural experiment, resulting in genetic samples from 76 individuals.
All information on mice including population background, sex, microsatellite data and experimental information can be Thomas jager speed dating in Additional file 1 : Table S1. The experimental setup consisted of five standard macrolon cages Techniplast. One central cage Schematic top view of the experimental setup. One central cage is connected via Plexiglas tubes with four satellite cages. Satellite cages are divided by a metal grid dotted lines to prevent mating of the focal mouse with access to the central cage and the smaller inner parts of the satellite cages and the four satellite mice with access only to the larger outer part of their respective satellite cage.
Food, water and shelter were provided for all mice, but are not shown in the figure for clarity. The satellite cages were divided into two parts by a metal grid. In each of the four satellite cages, a so-called satellite mouse was placed in the larger, outer part. The smaller inner part could be accessed by the so-called focal individual from the central cage, in which it was placed at the beginning of the experiment. This setup allowed the focal mouse to move between the central and all outer cages. Through the separation mice could interact i.
Water and food as well as bedding were provided for all mice ad libitum, for the satellite mice in their part of the respective cage, for the focal mouse in the central cage. The order a mouse participated in the experiment first as focal vs. The mice in each quad stayed the same over experiments to ensure a comparable measure of preference across cage systems.
Each quad participated four times as satellite mice, one time for each of the four possible genotypes of focal mice. Each run of the experiment was started by placing the focal and satellite mice in their respective cages and starting the computer program monitoring the RFID antennae.
Each experiment ran over five days and six nights, always starting around h on a Thursday and finishing the following Wednesday around h. The rooms were set with a dark-light cycle of h with lights on at and off at h, both for the breeding before the experiments, as well as during the experiments.
We chose such a comparatively long duration of the experiment as we were interested in the decision making process. Further, in this time frame, each female mouse can be assumed to have concluded at least one full oestrus cycle [ 32 ]. Females also usually enter oestrus synchronised as soon as they perceive certain pheromones of a nearby male [ 33 ], which was the case in our study.
For each focal individual a text-file was generated with time stamps for every antenna read, and the identification of the respective antenna. By this, we could gain information about the of antenna re as a proxy for activity. Using a self-written script in R [ 34 ] we calculated the duration of time spent in the four satellite cages, which served a proxy for preference behaviour of the focal mouse.
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To determine if genetic distance is an important factor of partner preference we chose 13 unlinked microsatellite markers published by Teschke et al. Raw alleles have been called using GeneMapper 4. The proportion of shared alleles [ 35 ] and the pairwise genetic distance Cavalli-Sforza distance; in the present paper referred to as CAS between all individuals were calculated with the program MSA [ 36 ] and visualized using MEGA 6 [ 37 ]. As a paternal influence on partner choice was proposed by Montero and colleagues [ 31 ], we also included the genetic distance from the mother and father of the focal mouse to each of the satellite mice referred to as Thomas jager speed dating or CASpat, respectively.
The phase of diploid sequences was estimated following Stephens and colleagues [ 3940 ], implemented in DNASp [ 41 ]. To assess whether MHC-dissimilarity between two potential mating partners were important, the of amino acid differences per site p-distance between sequences of the focal individual to the four satellite individuals was calculated, as well as the p-distance between the mother and father of the focal individual to each of the satellite mice in this paper referred to as MHC, MHCmat and MHCpat, respectively.
Furthermore, we addressed the question if MHC-diversity of the potential mate is influencing mate choice. Therefore, we again calculated the of amino acid differences per site p-distance between the two haplotypes within each satellite individual.
To estimate the activity patterns of focal mice, we analysed the of antenna re per hour for each focal mouse. We tested for changes in activity over time using a generalised linear model with Poisson error distribution, fitting to our count data with experimental day, genotype and sex as fixed factors, and activity per hour as response variable. For the analysis of temporal behavioural patterns, we had to exclude one of the focal mice, as during the run of one individual a GF male the recording was stopped unintentionally after three days due to power failure.
To analyse the selectivity i. SI was calculated in ten minute intervals for each focal mouse to get measures for the change of selectivity over time, and over the whole period to get a measure of overall selectivity for each individual. To calculate which factors might influence the selectivity, we applied a generalised linear model with the overall SI per focal mouse as response variable. We used the best fitting error distribution, which was a beta-distribution. The tested factors were the sex of the focal individual, its maternal and paternal population background, and whether it is of pure or mixed population background.