Salivary androgen-binding protein (ABP) mediates sexual isolation in Mus musculus.
The M. musculus complex has been described in detail in a recent review (Boursot et al. 1993; but we note that there have been different taxonomic descriptions of these groups [e.g., Marshall and Sage 1981; Berry and Bronson 1992; Sage et al. 1993] and we invite the reader's attention to Corbet's  evaluation of the taxonomy). Currently, M. m. domesticus occupies western Europe, the Mediterranean basin, and Africa; M. m. musculus is distributed from central Europe eastward through northern China and Mongolia; and M. m. castaneus occupies Southeast Asia, Malaysia, and southern China. The definition of the three subspecies has been based primarily on combinations of allelic frequencies of many structural loci (Boursot et al. 1993). No single character made possible the partition of these populations until the Abpa alleles [Abpa.sup.a] and [Abpa.sup.b] were shown to be essentially monomorphic in at least two of the three subspecies (see above and Karn and Dlouhy 1991). Although the subspecies make contact along extensive boundaries in Europe and Asia, they maintain their identities.
Bonhomme and his colleagues have recently proposed that M. musculus is a ring species with a double Rassenkreis (Din et al. 1996). Three chains of radiation of the species from its origin in the north of the Indian subcontinent (Boursot et al. 1996; Din et al. 1996) were envisioned, one branch spreading westward to eventually become the domesticus subspecies, one flowing northward and that eventually became the musculus subspecies, and one migrating southeastward to become the castaneus subspecies. The domesticus and musculus subspecies made secondary contact in Europe where they established a relatively narrow hybrid zone, and the musculus and castaneus subspecies made a broad secondary contact in China. Apparently Abpa underwent microevolution in the course of radiation of these three branches, resulting in the distinct intersubspecies variation (Karn and Dlouhy 1991; Hwang et al. 1997).
It has recently been shown that the Alpha subunit of ABP has significant structural identity with chain 1 of the major feline allergen, Fel dI (Karn 1994). Since others have observed that cats contaminate their environments heavily with Fel dI (Morgenstern et al. 1991), Hwang et al. (1997) extended the assortative mate selection hypothesis of ABP function to suggest that mice mark their environment in part by depositing ABP and that this influences mate choice. In this study, we made direct tests of the hypothesis that mouse salivary ABP mediates mate choice behavior in female mice. Our results show that M. m. domesticus and M. m. musculus female mice recognize and discriminate between the territories of male mice, which differ solely in their ABP genotype and that, when the males are present, the female prefers to mate with the one of her own ABP type. We also provide the first direct evidence that males mark their territories with salivary androgen-binding protein.
MATERIALS AND METHODS
C3H/HeJ, DBA/2J (referred to hereinafter as C3H and DBA, respectively, which represent the M. m. domesticus subspecies) and CZECH II mice, which represent the M. m. musculus subspecies, were obtained as previously described (Karn and Dlouhy 1991).
Detecting ABP on Mouse Pelts and in Housing Litter
Dust was vacuumed from litter that had been occupied for two weeks by C3H male mice and the dust was extracted as described by Morgenstern et al. (1991). The ventral pelts of two male C3H mice were rinsed with distilled water in the area of the scrotum and hind legs and the volume of the rinse water was reduced 100 fold. The proteins in both samples were analyzed by electrophoresis followed by electroblotting and immunostaining (Karn and Dlouhy 1991). The immunostained filter was scanned into the Adobe Photoshop 3.0 program and printed on a Shinko dye-sublimation printer.
Producing the b-Congenic Strain for Behavioral Testing
All of the mate preference tests were designed to take advantage of the power of congenic strains: essentially the only genetic difference between males that marked the territories and, in some versions participated directly in the test, was [Abpa.sup.a] and [Abpa.sup.b]. To produce the b-congenic strain, the DBA strain (ABP b) was crossed with the C3H strain (ABP a) and the [F.sub.1] backcrossed to the C3H strain. Backcrossing for 16 generations, followed by intercrossing, and selecting the [Abpa.sup.b] homozygotes, produced [Abpa.sup.b] congenic in the C3H strain "b-congenic".
The b allele of Abpa was maintained in the line during backcrossing by typing ABP (Karn and Dlouhy 1991) in offspring and selecting heterozygotes as parents for the next backcross generation. Estimates have been made of how much heterozygosity remains in congenic strains, depending on the number of backcrosses used to produce them. Naveira and Barbadilla (1992) derived plots of expected combined lengths of heterozygous chromosome segments flanking a selected locus and of the standard deviation. Those plots show that a locus such as Abpa, which has been selected for 16 generations, is expected to have an average combined distance of 12 map units around it, with a standard deviation of eight map units, that is still heterozygous. Thus, while producing the b-congenic line eliminated most of the DBA parental genes, it cannot be said to have eliminated all but the b allele of Abpa. Nonetheless, the exact derivation of Naveira and Barbadilla (1992) yields an asymptotic curve and further backcrossing does not much improve the situation.
The origin of the classical inbred strains of mice is essentially the domesticus subspecies (Bonhomme et al. 1987) and we therefore used C3H females (ABP a) as test subjects to represent that subspecies. CZECH II, an inbred strain derived by Jackson Laboratory from mice trapped in Central Europe, was used as a source of musculus females (ABP b) for test subjects. In addition, b-congenic females were subjects in the tests of choice for male-marked territory. Initial tests of females, while at the same time monitoring their estrus cycles, showed that estrus stage has apparently little or no influence on the female's choice. Therefore tests were conducted on a daily basis.
The test chamber, used in several different ways in the tests described below, is shown in Figure 1. In all the various tests described below, two male mice that were genetically identical except for their Abpa genotypes were allowed to condition the two sides of the chamber for five days. A central barrier divided both the inner and outer chambers. Otherwise the inner chamber was left open (no gates or lid) so that the males were free to each mark their side of that chamber as well as the outer chamber. All tests were conducted under red light (effective darkness to mice) during the middle of their 10-h dark cycle.
Female Mate Choice
Preference for Male-Conditioned Territory. - Two versions of this test were used in which males were removed prior to introducing the female into the test chamber. In the irrevocable-choice version of this test, a female was introduced into the inner chamber, the lid placed on it, and a modified central barrier that divided the outer chamber but not the inner chamber was put in place to hold the lid on the inner chamber. The female was free to explore the entire inner chamber, however, once she exited through one or the other gate, her choice was irrevocable since the gates allow egress but preclude reentry. Her choice was scored as "a" or "b", depending on which male's territory she chose. The null hypothesis, that ABP type does not affect the female's preference, predicts equal numbers of a and b choices.
In the free-roaming version of this test, a female was introduced into a small box in the center of the chamber, but the lid and the one-way gates were not placed on the inner chamber. The female subject was free to roam from one side to the other and her behavior was recorded on videotape for 30 minutes and later analyzed for first choice and for total time spent on each side of the chamber.
Preference for Tethered Males. - This test used the same chamber as described above except that the males were left in the chamber for testing, tethered to their respective sides by a 22.5-cm tether (steel fishing leader with swivels on each end, one end connected to a plastic collar around the male's neck and the other end anchored to an eye screw in the side of the chamber). There was no central divider in the outer chamber, but the one-way gates were in place on the inner chamber and a piece of plate glass was placed as a top on the inner chamber after introducing the female for the test. Her behavior and that of the tethered males was recorded under red light for two hours and the tape was later analyzed for mounting by the male, followed by lordosis (penile thrusting), which was scored as mating behavior.
Analysis of Reproduction. - This was the simplest design of all the tests. The test chamber was the same size as those described previously but did not have an inner chamber. The males conditioned their respective sides as described above but were not tethered during the test. The test consisted of introducing a C3H female into the center of the chamber just after the dark cycle began and removing her the next morning after the lights had come on. Females that became pregnant delivered their pups, which were then typed for ABP. Their type unequivocally indicated the male with which the female had mated (mating with the C3H male produced only a/a pups, while mating with the b-congenic male produced only [TABULAR DATA FOR TABLE 1 OMITTED] a/b pups). We note that it is possible that multiple paternity could produce both types and also realize that sperm competition could influence the ratio of offspring genotypes in the case of multiple paternity. This was addressed, at least in part, however, by observing mating behavior in the tethered-male version of these tests (see above).
Chi-square tests were done on female mate choice behavior as determined by territory exploration, mating behavior or actual reproduction with a male. Since this was a test of our ABP-assortative mate selection hypothesis wherein we predicted a direction of departure from the null hypothesis, we halved the P-values derived from the chi-square test, consistent with a one-tailed test.
Female Mate Choice
Preference for Male-Conditioned Territory. - The first set of behavioral studies tested the female's preference for territory previously occupied by [Abpa.sup.a]/[Abpa.sup.a] and [Abpa.sup.b]/[Abpa.sup.b] males. Table 1 shows that, in the irrevocable-choice test, domesticus females chose the ABP a males' (same type) territory significantly more often than predicted by the null hypothesis (P [less than] 0.001) and that musculus females preferred the territory of their ABP same-type male (P = 0.004). The b-congenic female response was in the opposite direction of the prediction, given their ABP type; they chose the a male's territory more frequently than the b male's territory (P = 0.06).
The free-roaming version of this test was designed to see whether the irrevocable-choice version described above reflected a false choice by the subjects, that is, they would have preferred the side they did not choose first but could not change their choice once they had passed through the gate. Here, the female could pass partially through the aperature (without the gate there) and sniff the area immediately outside the inner chamber. A choice was only recorded when her entire body, not including the tail, passed through the aperature. However, this version of the test was only significant for the female's first choice (Table 2) since the total time spent on each of the two sides did not differ significantly (not shown). As in the irrevocable-choice version, the domesticus females chose the ABP a males' (same type) territory significantly more often than predicted by the null hypothesis (P = 0.007). The b-congenic female gave a null hypothesis result (P = 0.4). The M. m. musculus females only showed escape behavior, running in any direction and/or jumping over the side of the inner chamber without any initial exploration, in this version of the test, probably because there were no gates or top to slow their exit from the smaller chamber into the larger one.
TABLE 2. Results of testing females representing two combinations of ABP type and subspecies background for first choice of male-conditioned territories in a free-roaming configuration. Female choice for male-conditioned territories Abpa Subspecies Inbred strain type background a b P-value(*) C3H/HeJ a/a domesticus 23 8 0.007 b-congenic b/b domesticus 7 8 0.4 * Because our hypothesis predicts female choice in the direction of her own ABP type, the chi-square test is treated as one tailed, that is, P-values were halved.
Preference for Tethered Males. - Both the domesticus and musculus females were tested in the tethered-male system, but mating was only seen in the case of the domesticus females. The skittish behavior of the musculus females caused them to avoid the tethered males except for very brief nose-to-nose contact. This and the observation that the calmer domesticus females were able to escape easily from the males to the center of the cage when they wished to do so, suggests that the mating behavior we observed was voluntary submission rather than forced mating. Table 3 shows that the domesticus females chose to mate with the ABP a male significantly more often than with the ABP b male (P = 0.017). Furthermore, this test allowed us to observe the details of this behavior. In nearly all cases, the female and the male made extensive face-to-face contact, followed by the male sniffing the genital area of the female. During this process, she lay still and let him mount her.
Analysis of Reproduction. - Females that became pregnant in this version were allowed to deliver their pups, which were then typed for salivary ABP. Mate choice in this case was confirmed by reproduction, and Table 3 shows that domesticus females chose to mate with the ABP a male significantly more often than with the ABP b male (P = 0.017), a result that strongly reinforces the results with tethered males.
Detection of ABP on Mouse Pelts and Deposited on the Environment
Figure 2 shows that immunostaining with an antibody specific for ABP (Dlouhy et al. 1986) detects ABP cross-reactive material (ABP-CRM) on mouse pelts and in the dust of litter in which the mice were housed. Immunostains of very concentrated litter extracts initially stained dark brown but faded substantially before the filter had dried enough to be scanned. It appears that, following staining, something in the extract competed for binding of the electrons that were initially transferred to the diaminobenzidene stain. Control immunostain reactions in which either rabbit preimmune serum or goat control serum was substituted for the anti-ABP antibody were always negative. Thus staining is specific for ABP-CRM and not due to nonspecific binding of the rabbit IgG to material transferred to the filter. The ABP-CRM bands in the pelt rinse migrated as a distinct band, but the litter dust always produced a smear. Apparently ABP adheres to something in the environment that causes the smearing. Sonicating the extract or treating it with detergents did not alleviate the smearing problem.
TABLE 3. Results of testing females for choice of male as a mating partner. Female choice of male Target type a b P-value(*) Free-roaming female, tethered males 9 2 0.017 Female exposed to both males, reproduced 7 1 0.017 * Because our hypothesis predicts female choice in the direction of her own ABP type, the chi-square test is treated as one tailed, that is, P-values were halved.
Several unusual features of Abpa polymorphism have been cited to support the idea that its microevolution is related to assortative mate selection in M. musculus subspecies (Hwang et al. 1997). The first of these was the observation that each subspecies apparently has its own allele (Karn and Dlouhy 1991). The second was the finding of a 25-fold excess of nonsynonymous base substitutions over synonymous ones compared to an average protein under purifying selection, which led Hwang et al. (1997) to argue that positive Darwinian selection rather than genetic drift drove the microevolution of Abpa. We have tested the hypothesis (Karn and Dlouhy 1991; Karn and Russell 1993; Hwang et al. 1997) that ABP functions in some form of assortative mate selection behavior and our behavioral studies support the idea. Females show a strong preference ([greater than] 2:1) to associate with, mate with, and reproduce with males of their own Abpa type.
It is especially interesting to note that a female mouse can recognize the difference between two territories marked by male mice that essentially should differ solely in their Abpa genotypes (but see the reservations noted in the Materials and Methods section concerning production of b-congenics). This, in itself, does not directly imply a function for ABP, but does attribute a recognition characteristic to the protein. Combining this recognition with preference of females for the territories of males of their own ABP type, however, suggests that salivary ABP is important in mouse social interaction.
Others have noted that oral scents may be important in mediating social behavior in voles (Ferkin and Johnston 1995) and gerbils (Block et al. 1981). Furthermore, the observation that females can differentiate between the territories of the two males when those mice were absent suggests that the males have marked their territories with ABP. In this study, we detected ABP deposited in the environment by the males. Also finding it on their pelts is consistent with the idea that the animals apply the protein to their pelts by licking and that it is then deposited in their surroundings. Such a suggestion has been made for how cat Fel dI, a protein very similar to ABP (Karn 1994), comes to contaminate the cat's environment (Morgenstern et al. 1991).
In light of the recent observation that ABP and Fel dI are members of a family of proteins, many of which, including these two, apparently share the characteristic of coating surfaces (Dominguez 1995), we recognize the possibility that ABP's original function may have more to do with conditioning the mouse's pelt in some way. Contamination of the environment and, subsequently, detection by other mice might have been secondary to that function. In other words, ABP may have been preadapted to serve a pheromonal role in mice. It is interesting to compare this possibility to the observation that long-chain hydrocarbons that protect the cuticle of Drosophila against dessication have also been shown to act as pheromones involved in sexual isolation (Coyne and Charlesworth 1997).
It is evident from our results of testing b-congenic female behavior that the ABP-based recognition system we propose must be a complex one. It appears that the female's ability to recognize her own type in a male or male-produced target must require an interaction between her Abpa genotype and other genes in her subspecies background, perhaps similar to MHC-based kin recognition by phenotype matching (Manning et al. 1992). It is likely that the system relies on her ABP type as a self-recognition index with which to compare the male's ABP type, the target. We probably compromised that system in producing b-congenic females since their subspecies background genes would predispose them to prefer the ABP a target but their self-recognition index has been changed to ABP b. In any event, the normal combination of subspecies domesticus genes and [Abpa.sup.a]/[Abpa.sup.a] (e.g., in the C3H female) or, alternatively, subspecies musculus genes with [Abpa.sup.b]/[Abpa.sup.b], does not lead to absolute assortative mate selection in our test system and certainly not in the wild or the hybrid zone would not exist.
Previous reports presented the hypothesis that detection of ABP takes place in the vomeronasal organ (VNO; Karn and Russell 1993; Hwang et al. 1997). The VNO is well developed in rodents and ungulates and there is abundant evidence that the VNO is associated with mating behavior in rodents (Estes 1972; Wysocki 1989; Johnston 1992). Verification of a role for the VNO in ABP detection must await behavioral tests of female mice that have had their VNO ablated, as has been done in other studies (Wysocki 1989).
In light of the data presented here, it is reasonable to ask whether the ABP-assortative mate selection behavior we have observed in the laboratory is a factor contributing to the restriction of gene flow across the hybrid zone between the domesticus and musculus subspecies in Europe. It has long been recognized that the disruption of coadapted gene clusters is probably the primary mechanism reducing gene flow by causing hybrids to be less fit than the parental subspecies. Reduced resistance to parasite infections has been offered as an explanation of this reduced fitness and it has been shown to have a genetic basis (Sage et al. 1986a; Moulia et al. 1991, 1993). Barton and others (reviewed in Barton and Hewitt 1985) described a "hybrid sink effect" where genes flow into a hybrid zone and are eliminated by counterselection on hybrids at or near the center. Sage et al. (1986b) have characterized the M. musculus hybrid zone in Europe as such a "genetic sink." We suggest that ABP-assortative mate selection might reduce the loss of genes into the sink.
While the postzygotic isolation mechanisms supposed to be primarily responsible for limiting introgression of genes across the hybrid zone have been reasonably well examined, the interactions mediated by ABP recognition could prove a useful and needed model for studying how prezygotic mechanisms of reproductive isolation help to shape a hybrid zone. Barton and Hewitt (1985) discussed "a male character subject to both natural and sexual selection, the latter resulting from female preferences that evolve through their correlation with the male character." ABP-assortative mate selection appears to fit this description since it is evident that its microevolution was driven by natural selection (Hwang et al. 1997), although it is not yet clear how that happened. Nonetheless, our data suggest that it has become involved, perhaps secondarily, in female preference for the male's ABP type when it matches her own. Lande (1982) has shown that a cline maintained by natural selection will be steepened by sexual selection. It is possible then that the house mouse hybrid zone in Europe may be maintained and modeled both by counterselection on hybrid genomes and by ABP-assortative mate selection. If this is true, however, we suspect that the mate selection behavior is restricted to the edges of the zone where the parental subspecies populations make contact with the transition of hybrid genomes crossing the zone. That is because hybrid indices for introgressed genes do not show depressed frequencies of heterozygotes (underdominance) as would be predicted otherwise (e.g., see Hunt and Selander 1973). Orr (1996) has reported evidence, depending on the method he used to measure mate discrimination, for such a differential mate selection behavior pattern in the tails of a cline across a grasshopper hybrid zone in the Sierra Nevada.
We wish to thank J. Coyne, R. Lewontin, and S. Perrill for reviewing early drafts of the work; L. Getz and S. Perrill for advice about the testing designs; and F. Bonhomme and P. Boursot for helpful comments in the revision stage. Partial support for this work was provided by the Holcomb Research Institute of Butler University and that support is gratefully acknowledged.
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|Author:||Laukaitis, Christina M.; Critser, Elizabeth S.; Karn, Robert C.|
|Date:||Dec 1, 1997|
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