Assortative mating in mice. I. Female mating preference - Springer Link

0 downloads 0 Views 714KB Size Report
Assortative Mating in Mice. I, Female Mating Preference. Joseph Yanai 1'2 and Gerald E. McClearn 1. Received 15 July 1971. Females of two inbred strains of ...
Behavior Genetics, Vol.2, No. 2/3, 1972

Assortative Mating in Mice. I, Female Mating Preference Joseph Yanai 1'2 and Gerald E. McClearn 1

Received 15 July 1971 Females of two inbred strains of Mus musculus domesticus, C57BL/Ibg and DBA/Ibg, were allowed to choose between two males, one of each strain, who were restrained within their cages. Females of both strains preferred to spend more time with, and to mate with, the males of the opposite strain rather than with males of their own strain. No major strain difference for the degree of preference wasfound. Preference was also unchanged between trials. There is a general lack of correlation between trials which is explained in terms of the nature of the variance in inbred strains. Female mating preference may have an evolutionary significance in reducing inbreeding. INTRODUCTION Assortative mating is an important mechanism in the determination of the genetic composition of populations, in that it is one of the identified sources of deviation from the Hardy-Weinberg equilibrium. Assortative mating, either positive or negative, gives rise to changes in homozygosity, in total variance, and in the correlation between relatives in the population. Crow and Felsenrein (1968) have recently summarized and reviewed these effects. Departures from random mating have been studied extensively in many animal populations. For example, positive assortative mating and sexual selection for various traits and rare-type mating advantage have been described in Drosophila. Female preference appears to be an important determinant of these mating patterns. A comprehensive review of nonrandom This work was supported by NIGMS Grant GM-14547. 1 Institute for Behavioral Genetics, University of Colorado, Boulder, Colorado. 2 Present address: Department of Biobehavioral Sciences, University of Connecticut, Storrs, Connecticut. 173 9 1972PlenumPublishingCorporation,227West17thStreet,NewYork,N.Y. 10011.

174

Yanai and McClearn

mating in Drosophila has been presented by Parsons (1967). An interesting case of negative assortative mating for body color determined by female preference has also been described in the moth Panaxia dominula (Sheppard, 1952). Work with avian species provides examples of mating preference related to imprinting. Graig (1908) described clear cases of preferential mating of pigeons with mates of a species like their foster parent. Lill and Wood-Gush (1965), in a study on true breeds of the domestic fowl, found a general tendency for homogamy. A detailed analysis of its behavioral basis was provided later (Lill, 1968a,b). Positive assortative mating for color phase of the Arctic skua has been described by O'Donald (1959), and negative assortative mating for plumage color in the whitethroated sparrow was found by Lowther (1961). It has also long been recognized that mating in man is often not at random with respect to many characteristics. In one early study, Pearson and Lee (1903) demonstrated the existence of positive assortative mating for a variety of physical traits, such as stature and forearm length. As early as 1928, strong positive assortative mating was shown to exist in man for behavioral characteristics such as intelligence (Jones, 1928). A comprehensive survey of the many published studies on human assortative mating has been provided by Spuhler (1968), who also provides evidence on the heritability of many of the traits discussed. This is of basic importance because nonrandom mating has population consequences only for heritable traits. In Spuhler's review, all statistically significant instances of assortative mating were positive. There are, however, suggestions that negative assortative mating in humans might be expected to occur through such relationships as the negative correlation between childhood association and sexual attraction (Wolf, 1970). Incest taboos of some cultures might possibly contribute to outbreeding and negative assortative mating (Lindzey, 1967). It would appear particularly important to have information concerning mating preference in Mus musculus domesticus, because that species has been the principal laboratory mammal in behavioral genetics. In spite of this, research on preferential mating in mice has been relatively neglected. Most of the relevant work has been done by Mainardi (1963a,b, 1964) and Mainardi et al. (1965a,b). In one study, females of Mus musculus domesticus had estrus induced by injections of estrogen. During a 24 hr observation period, these females preferred to associate more with males of their own subspecies than with those of another subspecies, Mus musculus bactrianus (Mainardi, 1963a). This preference was presumably due to imprinting or some related process since it only appeared if the father had been present during rearing (Mainardi, 1963b). Within the subspecies Mus musculus domesticus, females of the Swiss and C57BL strains associated more often with males of the opposite strain

Assortative Mating in Mice

175

(Mainardi, 1964). As in the previous case, presence of the father during rearing was necessary for the preference to appear (Mainardi, 1964). Male mice did not show any sexual preference (Mainardi et aL, 1965a). In an initial effort to characterize the behavioral mechanisms of the preference, Mainardi has established the importance of olfactory stimuli (Mainardi et al., 1965b). The present study is the first of a planned series of further experiments on mating preference in Mus museulus domesticus. This experiment used two inbred strains in which the sexual behavior of the males has been shown to differ extensively (Wilson, personal communication). The purpose of the study was to determine the importance of female choice in the mating behavior of these strains. MATERIALS AND METHODS Two inbred strains of Mus musculus domesticus, DBA/Ibg (hereafter designated DBA) and C57BL/Ibg (hereafter designated C57~, were employed. The animals were born and maintained in the laboratory facilities of the Institute for Behavioral Genetics at the University of Colorado, Boulder, Colorado. Animals were reared until weaning by both parents. At weaning, which occurred at 25 days of age, each litter was segregated and placed into two different cages according to sex. Because solitary rearing during this period might influence the behaviors under investigation, animals with no like-sexed sibs were not employed in the experiment. Between 56 and 70 days of age, animals were placed in a room with reversed light cycle, where they remained for the duration of the study. In preparation for the experiment, each male at the age of 70-84 days was housed in an individual cage. Each was then tested for sexual activity. The ability to mate with an outbred-strain female in induced estrus was affirmed by the existence of a vaginal plug. Those demonstrating sexual activity were then collared with fine flexible polyvinyl tubing (1.6 mm in diameter) and restrained in their individual cages with light stainless steel bead chains (bead diameter of 2.3 ram) which were attached to the collars with a small swivel and secured to the cage lid. Testing of the females began at the age of 70-84 days. Preparation of the females was started 9-14 days prior to testing by injecting 0.025-0.050 ml of estrogen (estradiol benzoate 1.0 mg/ml in sesame oil). Two days later, 0.025-0.050 ml of progesterone (25 mg/ml in sesame oil) was injected. Three days before testing, the females were separated and introduced individually for a 24 hr period into an apparatus simulating the testing apparatus so that they might become habituated to it. At the end of this period, the females received their second injection of estrogen and were placed into individual cages. Two days later, the second injection of progesterone was administered,

176

Yanai and McClearn

Fig. 1. The testing unit. A: The males' cages. B: Photocell units. C: The female's cage.

and 5 hr later they were tested. This double injection series has been found to provide more positive assurance of sexual receptivity of the female. This sequence of injections is based on a procedure of Wilson (personal communication). Two testing units were employed, each consisting of a "triad" of standard living cages (23 by 11 by 10 cm high) interconnected by means of a Y-shaped tube. Photocell units with red light sources were installed along two of the tubes (Fig. 1). During testing, the males were restrained in the cages into which these photocell-equipped tubes extended. Wood shavings were placed in the males' cages only. The third cage was the cage into which the female was placed at the beginning of a trial. Rations of water and Allied Mills Lab Blox were available in each cage. Males were used repeatedly throughout the entire experiment. They were given appropriate recovery time after ejaculation before being used again (McGiU and Blight, 1963). Three successive groups of females were employed. Of each group, every female was tested twice with at least 7 days elapsing between trials. A third trial was given to those females who had an invalid trial in either of the first two trials. A valid trial was defined as one during which either ejaculation occurred or the female stayed with one or both males for at least 1200 see and two or more intromissions occurred. A further condition for a valid trial was that both males be sexually active. The male was regarded as nonactive if, during a cumulative period of 1200 sec with the female present in his cage, he failed to mount or intromit. If a mount without intromission occurred

Assortative Mating in Mice

177

during the first 1200 sec, an additional 600 sec period was provided within which he could intromit. Entries by the female into a male's cage actuated the photocell unit, which in turn activated the recording device. A counter, cumulative time meter, and Esterline-Angus event recorder recorded the number of entries and the total amount of time the female spent with each male. The photocell detection system of the apparatus could not record any interference of less than 2 sec, so that entries of less than this duration were ignored. Other data were recorded by direct observation. The whole experiment took place in the reverse-cycle room under night conditions. Darkness prevailed from 0800 to 2000 hr, and testing took place between 1200-1800 hr. One DBA and one C57 male were used in each trial; a female of either strain was introduced into the female cage. The males were randomly placed in the left or right cage. With the males restrained in their respective cages, the female was free to choose between them. The experiment ended with an ejaculation or, in case no ejaculation occurred, after 2 hr. The following data were recorded: time of association with each male, the number of entries into each male cage, the first cage entered, the number of intromissions by each male, the identity of the male that intromitted first, and the identity of the male that ejaculated.

RESULTS Data were collected from 32 C57 and 28 DBA females. Of this number, two C57 and three DBA females had only one valid trial. The remaining animals all had two valid trials. The data have been treated as follows: The time of association with each male during the experiment, the number of erttries into each male cage, and the number of intromissions by each male were converted Table 1. Female Mating Preferences in the First Valid Trial

Strain C57 DBA C57 and DBA combined * t test. b )r test.

Cp