Behavioral Ecology Vol. 13 No. 3: 312-320
© 2002 International Society for Behavioral Ecology
Subspecies recognition in the house mouse: a study of two populations from the border of a hybrid zone
Laboratoire Génétique et Environnement, Institut des Sciences de l'Evolution de Montpellier, UMR 5554, Université Montpellier II, Montpellier, France
Address correspondence to C. Smadja, Laboratoire Génétique et Environnement, Institut des Sciences de l'Evolution, Université Montpellier II, C.C. 065, 34095 Montpellier cedex 5, France. E-mail: smadja{at}isem.univ-montp2.fr .
Received 29 November 2000; revised 15 June 2001; accepted 26 June 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Mate choice is the outcome of sexual preference for partners carrying specific signals. Thus, mating among conspecifics (homogamy) depends on the occurrence of species recognition systems. We asked what happens if populations diverge, and we investigated female sexual preference between two subspecies of the house mouse in populations from the borders of a hybrid zone (Jutland, Denmark). We used choice tests to analyze the occurrence of recognition signals and to locate these signals in soiled bedding and urine. Our results show that populations of the two subspecies can be discriminated on the basis of urinary signals, suggesting that the latter have diverged. Additionally, these signals seem to have similar features in populations of different geographical origins, suggesting that subspecific differentiation occurs. This is the first demonstration that subspecific recognition through urinary signals occurs in the house mouse. However, while Mus musculus domesticus does not display a preference, we show that Mus musculus musculus females tend to mate with males of the same subspecies. We discuss the different factors that could explain these discrepancies between females of the two taxa: differences in signal perception, evolution at a different pace, or evolution under different selective pressures in their area of contact. Further, we propose that the divergence in male signal was at least partly initiated in allopatry and discuss different evolutionary scenario that may explain the patterns observed in Denmark and their relevance to isolation between the two taxa.
Key words: Denmark, female preference, house mouse, mate recognition system, Mus musculus, speciation, urine signals.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Divergence of the mate recognition system (MRS) could limit gene flow between populations and hence play an important role in speciation (Coyne et al., 1994
;
Grant and Grant, 1996;
Hatfield and Schulter, 1996;
Ritchie et al., 1989). Indeed,
individuals of the same species are able to perform the signal-response
sequence necessary to achieve mating, but the sequence will not be completed
successfully in interspecific pairs (Butlin
and Ritchie, 1994). Choice between sexual partners relies on
interindividual recognition, which is performed through a complex
biocommunication system (Alberts,
1992; Littlejohn,
1993; Otte, 1974).
The recognition system comprises two entities: a transmitter (signal) and a
receiver (recognition and preference)
(Butlin and Ritchie, 1994). Due
to the complexity of the recognition process, it is assumed that both entities
need to coevolve for functional coordination to be possible
(Butlin and Ritchie, 1994; but
see Ryan and Rand, 1995).
Different types of recognition systems exist, relying on one or a combination
of visual, tactile, auditory, or olfactory cues
(Butlin and Ritchie, 1991;
Endler and Houde, 1995;
Witte and Curio, 1999).
Within a given species, variation of different components of the MRS is
reported (Butlin, 1994). A
balance between natural and sexual selection could explain such variation
(Butlin and Ritchie, 1991;
Kirkpatrick, 1982; Ryan and
Rand,
1993a,b;
West-Eberhard, 1983).
Moreover, changes in local environmental conditions or drift can lead to
geographical variation (Cotgreave,
1997; Endler and Houde,
1995). Thus, although the concept of species recognition system
(Eldredge, 1994;
Paterson, 1985;
Verrell, 1988) suggests that
homogamy is the result of different individuals of a species sharing a common
mate recognition system, signal-response systems can nonetheless vary within
and between populations of the same species. Depending on the extent to which
populations have diverged, homogamy within a species may be altered, and
reproduction between individuals of different populations may no longer be
possible as the result of assortative mating within these groups
(Littlejohn, 1993).
Divergence of the MRS is generally inferred from the analysis of one of its
associated phenotypes: behavioral discrimination between different types of
mate. A clear directional sexual preference is evidence of discrimination and
hence of divergence of mate recognition signals. Additionally, depending on
its direction, preference indicates whether assortative or disassortative
mating occurs (Butlin, 1994;
Wagner, 1998). In contrast, if
a preference is not observed, physiological discrimination may still occur
(Ganem and Searle, 1996).
Sexual preference measured under laboratory conditions may not accurately
reflect preference in natural conditions; however, so far, the experimental
approach has proved to be the best way to assess the potentialities and
unravel the processes involved in MRS.
The present study deals with mate recognition in the house mouse (Mus
musculus). This species relies on chemical cues to communicate
information on individual, population, and species characteristics
(Boyse et al., 1987;
Eklund et al., 1991;
Hurst and Barnard, 1992;
Lenington and Egid, 1985;
Penn and Potts, 1998;
Yamazaki et al., 1990) and
seems to use this information in mating decisions
(Coopersmith and Lenington,
1992; Wolff,
1985). The house mouse originated in the northern part of the
Indian subcontinent (Boursot et al.,
1993; see also Prager et al.,
1998). From there, the species has radiated into several
subspecies (but see Sage et al.,
1993), two of which occur in Europe and share a hybrid zone.
Available archaeozoological and genetic data suggest that these two subspecies
followed different colonization paths, which led to Mus musculus
domesticus occurring in western Europe and the Mediterranean basin, and
to Mus musculus musculus distributed from central Europe to northern
China (Auffray et al., 1990).
The transition between M. m. musculus and M. m. domesticus
in Europe occurs along a secondary contact believed to have taken place some
6000-2800 years ago (Boursot et al.,
1993). It is a narrow hybrid zone (30-40 km) that extends from
Denmark to the Caspian Sea, where it becomes larger
(Orth et al., 1996). Variation
of allozyme markers traced across the hybrid zone reveals the existence of
recombined hybrids in the center of the zone and introgressed populations
within both sides. Moreover, counterselection is evidenced by the absence of
introgression of the sex chromosomes (Dod
et al., 1993). Although the hybridization indicates that the two
subspecies did not have an incompatible MRS when they met, theory (first
introduced by Dobzhansky,
1940) predicts that selection against hybrids should favor
assortative mating in the vicinity of the hybrid zone
(Dieckmann and Doebeli, 1999;
Kirkpatrick, 2000;
Lande, 1982;
Liou and Price, 1994;
Servedio and Kirkpatrick,
1997).
In line with the above considerations, the present study addressed patterns
of mate recognition and preference in the two subspecies within their Danish
contact zone. A previous study (Christophe
and Baudoin, 1998) addressed population recognition in mice
strains derived from two populations from the same area of contact. Here we
intended to deal with a process of divergence leading to speciation, and hence
addressed subspecies as opposed to population recognition. To achieve this, we
analyzed patterns of female preference within two wild populations from each
of these subspecies and sought to identify stimuli used in subspecies
recognition. Specifically, using males as stimuli, we first asked whether
these two populations recognize each other as different. If so, we proposed to
determine if signals allowing this recognition can be found in the urine.
Then, assuming that urine from different populations characterizes each
subspecies, we used urine samples to assess subspecies recognition. We
expected females to prefer stimuli of their own subspecies, even when
unfamiliar (i.e., from a different population), if preference for subspecies
odors exists. Otherwise, if the females react differently to familiar as
opposed to unfamiliar conspecific stimuli, subspecific recognition may not
occur, and population recognition could be invoked for discrimination between
the two populations, as has been reported in other contexts
(Cox, 1984;
Hurst, 1990c;
Winn and Vestal, 1986).
Finally, following an analysis of the direction of female preferences across
the different experiments, we discuss the occurrence of assortative or
disassortative mate choice and its relevance to isolation between these
populations.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Population samples
This study concerns mice from Denmark where the hybrid zone between M. m. musculus and M. m. domesticus has benefited from many and still ongoing genetic studies (Alibert et al., 1997
; Dallas et al.,
1995; Dod et al.,
1993; Fel-Clair et al.,
1996; Vanlerberghe et al.,
1988). Mice were trapped in farm-houses in October and November
1998. Each sample originated from several buildings on a given farm. The
M. m. musculus sample consisted of adult mice trapped in Gosmer (57
47' N, 6°19' E) and Spoettrup (57°75' N,
6°19' E; two males), and the M. m. domesticus sample
consisted of adult mice trapped in Hojenkirk (53°10' N,
6°17' E) and Jerlev (52°80' N, 6°17' E; one
male). These localities are situated on the tails of the introgression cline
defining the hybrid zone (Dod et al.,
1993). Both populations bear genes of the other subspecies,
although to a limited extent (Raufaste,
2001). As an indication, the introgression index, calculated on
the basis of variation at four subspecific diagnostic allozyme loci and
expressed as the proportion of M. m. domesticus alleles over the
total number of loci (Vanlerberghe et al.,
1986) was 13% and 90%, respectively, in the M. m.
musculus and M. m. domesticus samples.
General experimental procedure
Preference was tested in female M. m. musculus and M. m.
domesticus (n = 8 and n = 9, respectively) trapped as
adults. During transport from the field, mice were housed per population, then
separated per sex. At the start of the first experiment the mice had spent 3
months in laboratory conditions, under a constant photo-period (light between
0700 and 1700 h). Food and water were available ad libitum. Three to
four weeks before being tested, the mice were isolated in small cages (26
x 16 x 14 cm). There are contradictory views on the influence of
the estrous cycle on preference (against:
Christophe and Baudoin, 1998;
Laukaitis et al., 1997; in
favor: D'udine and Alleva,
1983; Krackow and Matuschak,
1991). Here, we tested females while sexually receptive (estrus or
proestrus/estrus) to optimize expression of sexual preference. Vaginal smears
were performed 3 h before the start of a series of tests.
We measured a relative directional preference by presenting a female with a
two-way choice (Wagner, 1998).
A pair of stimuli was composed of a homosubspecific and a heterosubspecific
stimulus. All the experiments took place between 1400 and 1700 h. Four
experiments were performed at approximately 10-day intervals. The stimuli used
in the different experiments were either males (potential sexual partners) or
their olfactory signatures: soiled bedding (containing urine, feces, saliva,
and other products) or urine. The urine and the soiled bedding of several
males of a given population were pooled and kept at -20°C before the start
of the experiments. The behavioral apparatus was transparent (Plexiglas and
plastic ware) and consisted of a Y maze (5 cm diam; main branch: 35 cm long;
secondary branches: 25 cm long) connected to a start box (35 long x 23
wide x 13 cm high). When the experiments involved a pair of males or
samples of soiled bedding, two additional peripheral boxes (35 x 23
x 13 cm high), in which the stimuli were placed, were connected to the Y
maze (Figure 1).
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At the beginning of each test, we placed a female in the central box. A few minutes of habituation were allowed before opening the door that connected the box to the tunnel. Recording started when the mouse crossed the door. In all tests the females entered both branches of the Y maze repetitively. We considered that the female was in one or the other side of the Y maze when it had crossed the "decision zone" and entered one or the other secondary branches. Contact with a stimulus was recorded when the female either sniffed or licked the stimulus (when the stimuli were the males, contact was recorded when female sniffed or licked the transparent perforated door, both when the male was just behind or not). Time spent on each side ("side") and time spent in contact with the stimulus ("stimulus") were recorded using a Psion Organiser and the Observer software (Noldus Information Technology).
Data analysis
For each female, the following ratio was calculated to estimate preference:
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Two ratios were used to assess sexual preference: Rstimulus, corresponding to the actual time spent in contact with the stimuli, and Rside, based on the time spent in one or the other branch of the Y maze. Additionally, for each experiment we recorded the time of choice (time spent in the branches of the Y maze) and the time of sniff (total time spent sniffing both stimuli). Our experimental setting allowed the females to stay in a neutral part of the apparatus during the tests and hence the possibly low values of the ratios.
For every experiment involving several consecutive tests, the effect of testing order on preference (Rstimulus and Rside), time of choice, and time of sniffing was checked using an ANOVA. Depending on whether variances were equal, either a one-way ANOVA or a Kruskall-Wallis or Friedman test were performed (JMP, SAS Institute; Sall et al., 1996).
The data were analyzed at a population level by averaging the choice of all females. We determined preference by testing the value of R against a theoretical ratio of 0 (Ho: no preference), using a Student's t test (JMP). A Student's t test was also used for comparison between means. Descriptive statistics are given as means±SE. All p values are two-tailed, and the rejection limit was set at p =.05.
We controlled for laterality by alternating the position of each type of stimulus (left and right). However, a test was also performed by comparing time spent on the left side as opposed to time spent on the right side of the apparatus. Results did not reveal a significant preference for a particular branch of the Y maze (experiment 1: Rlaterality = 0.011±0.013, t = 0.84, p =.41; experiment 3a: Rlaterality = 0.104±0.103, t = 1.00, p =.34; experiment 3b: Rlaterality = -0.009±0.026, t = -0.35, p =.73; experiment 4: Rlaterality = -0.023±0.015, t = -1.27, p =.22).
Specific experimental procedures
Experiment 1: female preference when given a choice between a male
from her population versus a male of the other subspecies
In natural conditions, a given female could be presented with a choice
between individuals of the two subspecies in two circumstances: (1) after
immigration into an empty patch, where she could meet migrants of the two
types and (2) when a dispersing male arrives in her own population. This
experiment was designed to simulate the latter situation where a female had to
choose between a resident (familiar, same population) and a migrant male
(different population) belonging to the other subspecies. To avoid an
individual effect, four pairs of males were successively presented to each
female, and her preference was compared between the four tests. The order of
presentation of the pairs of stimuli was randomized between females. Each test
lasted 5 min.
Experiment 2: female mate choice
This experiment was designed to assess the relationship between female
sexual preference and the propensity to mate with the preferred male. To
control for interference of competition between males with female preference,
we designed an experiment preventing interactions between the males but not
between the female and each of the males. Only female M. m. musculus
showed such a preference in the first experiment and hence were involved in
this study.
The experiment took place in a terrarium (70 cm long x 30 cm wide
x 30 cm high) adapted from Van Zegeren
(1980) and composed of three
parts: two large areas to the left and right and a narrow central zone (10 cm)
that could be separated from the rest of the terrarium by two removable
plastic panels. Each test involved a female and two tethered males confined
either to the right or the left side of the terrarium. Soiled bedding from the
males' home cages was spread on each side of the terrarium. Before introducing
the males, the female was free to explore the terrarium for a period of 30
min, and preference for territories was recorded during two periods of 10 min.
The female was then blocked in the central part of the terrarium and the males
tethered to each side of the terrarium. Testing started when the two central
partitions were removed. The entire test lasted 2 h, and interactions between
the female and the two tethered males were recorded during 3 periods of 20
min. Behavioral items were grouped into three classes of interaction:
friendly, agonistic, and sexual (Table
1). A ratio for each category of behavior
(Rfriendly; Ragonistic, and
Rsexual) was calculated for each of the three testing
periods following the same principle as that for the ratio of preference. When
no significant differences between each period were observed, a ratio was
calculated for the total duration of the test (3 x 20 min). We predicted
that if preference relates to propensity to mate, sexual behavior would be
preferentially directed toward the type of male that was preferred during the
first experiment.
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Ethical note. Two pairs of males were used in experiment 2. To maintain them in their respective territories, we had to tether these animals. We used a 1 cm cotton strap to make a belt that was attached to their abdomen. A long, thin metal chain was then hooked to the belt of the mouse and fixed to the top of the terrarium. Although the first reaction of the mice was to try to cut or untie the belt, our procedure did not seem to provoke significant stress, as they very quickly investigated their environment and interacted with the female, displaying the complete repertoire of behavior (including attempts to copulate).
Experiment 3: localization of the recognition signals
This experiment concerned the two subspecies and was aimed to identify the
source of the recognition signals. The four pairs of males were substituted
first with their soiled bedding, which should contain the major part of their
olfactory signature, then with their urine.
In experiment 3a, the 8-day-old soiled bedding of the four pairs of males was mixed into two pools representing each of the two populations. Samples of 10 g were frozen at -20°C and thawed half an hour before the start of the experiment. The samples were put in petri dishes, one in each of the peripheral boxes. The test lasted 10 min.
In experiment 3b, urine samples were collected from the four pairs of males, mixed into two pools corresponding to the two population samples, and similarly kept at -20°C before testing. We placed 10-µl aliquots on a piece of blotting paper taped on the extremity of the branches (Figure 1). We assessed preference consistency by performing three successive 5-min tests during which the position of each stimulus was alternated between right and left. Each test was performed with fresh aliquots of urine. Here we predicted that if the olfactory stimuli contained the informative signals, a female would show the same pattern of preference as with a pair of males.
Experiment 4: a population or a subspecies recognition signal?
All the previous experiments involved a familiar homosubspecific stimulus.
The last experiment was designed to determine whether, when a preference was
observed, the preferred stimulus involved subspecies discrimination. To
address this question, we substituted the previous homosubspecific stimulus
with a pool of urine of males from several populations of the subspecies,
exclusive to the Danish population (geographic origin of the M. m.
musculus pool: Poland and Hungary; M. m. domesticus pool: Israel
and Morocco; from the genetic repository of the laboratory Génome,
populations, et interactions, Montpellier, France, UMR 5000). This foreign
homosubspecific stimulus was presented simultaneously with the
heterosubspecific Danish population stimulus. We assessed female preference
during a 5-min single test.
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RESULTS |
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Experiment 1: female preference when given a choice between a male from her population versus a male of the other subspecies
For both types of females, duration of choosing and sniffing did not vary between the four tests (Table 2, M. m. musculus: choosing: F3,25 = 1.33; p =.28; sniffing: F3,25 = 1.18; p =.33; M. m. domesticus: choosing: F3,29 = 0.98; p =.41; sniffing: F3,29 = 0.01; p =.99). However, on average, female M. m. domesticus spent twice as much time as M. m. musculus choosing and sniffing (Table 2, choosing: t = -4.95, p <.001; sniffing: t = -3.99, p =.001).
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The ratios of preference did not vary significantly across tests (Table 2, M. m. domesticus: Rstimulus: F3,29 = 1.01; p =.40; Rside: F3,29 = 1.08; p =.37; M. m. musculus: Rstimulus: F3,25 = 1.63; p =.20; Rside: F3,25 = 2.26; p =.10), hence an average ratio was calculated to test preference within each subspecies. Whereas a directional preference was not evidenced in M. m. domesticus (Rstimulus: R = 0.004±0.020, t = 0.25, p =.80; Rside: R = 0.015±0.020, t = 0.84, p =.42), M. m. musculus females preferred males of their own population (Rstimulus: R = 0.035±0.010; t = 3.49; p =.01; Rside: R = 0.036±0.010; t = 3.79; p =.007).
Experiment 2: female mate choice
During the phase of habituation, the ratio of preference for the
territories at the two record periods varied (t = -2.96; p
=.02), but no significant preference for a particular territory was detected
(Rperiod 1 = -0.016±0.055; t = -0.29;
p =.78; Rperiod 2 = 0.082±0.056;
t = 1.48; p =.18).
The ratios of each behavior did not show any variation across the three record-periods (Ragonistic: Friedman Fr = 3.25, df = 2, p =.19; Rfriendly: Friedman Fr = 0.74, df = 2, p =.42; Rsexual: Friedman Fr = 3.29, df = 2, p =.1). Thus, an average ratio was calculated. The results showed that although agonistic behavior was not preferentially directed toward one of the males (Ragonistic = -0.007±0.006; t = -1.27; p =.24), M. m. musculus females tended to be more friendly toward the male of their own population (Rfriendly = 0.089±0.040; t = 2.22; p =.06) and significantly directed their sexual behavior to/or accepted such behavior from M. m. musculus males (Rsexual = 0.042±0.019; t = 2.1; p =.04).
Experiment 3: localization of the recognition signals
Soiled bedding (a)
Only M. m. musculus preferentially sniffed the homosubspecific
signal (Rstimulus = 0.067±0.024; t = 2.76;
p =.028), although they did not spend significantly more time on the
side containing the preferred signal (Rside =
0.083±0.053, t = 1.56, p =.16). On the contrary, if
anything, female M. m. domesticus tended to spend more time with the
heterosubspecific stimulus (Rstimulus =
-0.049±0.022, t = -2.22, p =.06 and
Rside = -0.092±0.044, t = -2.08,
p =.07).
Urine (b)
Female M. m. musculus decreased their duration of sniffing across
the three tests (Table 3;
Kruskal-Wallis H = 12.42; p =.002), while duration of choice
remained constant (Table 3;
Kruskal-Wallis H = 3.55; p =.17), and neither duration of
choice nor of sniffing varied across the tests in female M. m.
domesticus (Table 3;
duration: Kruskal-Wallis H = 0.71; p =.67; sniffing:
H = 3.20; p =.20).
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Ratios of preference did not change significantly across tests (Table 3, Kruskal-Wallis, M. m. musculus: Rstimulus: H = 3.83, p =.15; Rside: H = 0.64, p =.73; M. m. domesticus: Rstimulus: H = 2.56, p =.28; Rside: H = 2.36, p =.37). Average ratio of preference of female M. m. musculus indicated a significant homosubspecific preference (Rstimulus: R = 0.01±0.002; t = 5.51; p <.001; and Rside: R = 0.030±0.008; t = 3.19; p =.01); a preference was not detected for M. m. domesticus (Rstimulus: R = 0.036±0.020; t = 1.59: p =.15 and Rside: R = 0.017±0.040; t = 0.42; p =.68).
Experiment 4: a population or a subspecies recognition signal?
Female M. m. musculus spent significantly more time in contact
with the homosubspecific stimulus (Rstimulus =
0.020±0.007; t = 2.85; p =.024) and tended to spend
more time in that branch of the Y maze (Rside =
0.049±0.025; t = 1.9; p =.09). Female M. m.
domesticus did not show a preference (Rstimulus =
-0.008±0.005; t = 1.62; p =.14;
Rside = -0.010±0.024; t = -0.43;
p =.67).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Female M. m. musculus from the Danish hybrid zone prefer males of their own population rather than males of the population from the other subspecies, suggesting that the signals carried by the two types of males are different. This preference correlates with mate choice, which is consistent with previous findings (Coopersmith and Lenington, 1992
; D'udine and
Alleva, 1983; Egid and Brown,
1989; Laukaitis et al.,
1997; Yanai and McClearn,
1973), and male urine suffices to trigger the same preference,
indicating that it contains signals allowing population mate recognition. The fact that M. m. musculus females display the same preference when the M. m. musculus stimulus originates from the same or a foreign population indicates that the signals involved have similar features in populations of different geographical origins. This result further demonstrates that recognition occurs at a subspecific level. Nevertheless, when the above stimuli are presented to female M. m. domesticus, if discrimination occurs, it does not lead to a preference (Table 4). During the first experiment, female M. m. domesticus spent significantly more time sniffing the males than did female M. m. musculus, whereas the latter reduced their sniffing time during the successive urine tests (experiment 3b). This indicates that habituation had occurred in female M. m. musculus, which was not observed in female M. m. domesticus. These additional differences between the two subspecies suggest that the two types of females may not perceive the signals in the same way.
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Subspecies recognition
Our results agree with the pattern showing a preference for own-population
stimuli in M. m. musculus previously evidenced by Christophe and
Baudoin (1998) but further
demonstrate that female preference is based, at least in part, on a
subspecific recognition. Hence, our study demonstrates, for the first time,
the occurrence of a subspecific recognition through urinary signals in the
house mouse.
Evidence for subspecies recognition suggests that cues that are used for
mate choice within and between populations
(Boyse et al., 1987;
Hurst and Barnard, 1992;
Lenington, 1983) may not be
relevant for mate choice decisions at a subspecies level. Although individual
and population recognition may influence within-taxa variability, subspecies
recognition can exert a control on gene flow between taxa and hence be a
factor in reproductive isolation.
Moreover, our study shows that subspecific recognition occurs, at least in
part, through signals present in urine. This result confirms the importance of
urine in communication between mice, as pointed out in other contexts
(Cox, 1989; Hurst,
1990a,b;
Wolff, 1985). In 1991, a
phylogeographical analysis on a gene coding for a salivary protein (androgen
binding protein; ABP) revealed that its allelic polymorphism corresponded to
diagnostic molecules, distinguishing the different subspecies
(Karn and Dlouhy, 1991). More
recently, ABP was shown to act as a subspecies recognition signal both in
M. m. domesticus and M. m. musculus females
(Laukaitis et al., 1997). In
our study, only female M. m. musculus exhibited a preference, whereas
M. m. domesticus females never did, either when presented with males
of the two subspecies or when the latter were substituted with their soiled
bedding (which contains saliva). The discrepancy between the results of these
different studies may be attributed to the fact that the Danish M. m.
domesticus strains involved in Christophe and Baudoin's study
(1998) and the wild populations
in the present study were slightly introgressed with M. m. musculus
genes, although not the ABP genes in our populations, or that our sample size
was too small to detect patterns of ABP preference
(Laukaitis et al., 1997).
However, neither introgression nor sample size limited the expression or
detection of a preference in M. m. musculus.
Another possibility is related to the different genetic backgrounds of the
mice involved in the three studies, suggesting a geographical variation of
preference in M. m. domesticus. Nevertheless, our study shows that
urine suffices to trigger a preference in M. m. musculus, and that it
is more effective than soiled bedding which contains both salivary and urinary
signals. Still, the complex process of recognition probably involves several
signals (Butlin and Ritchie,
1994), and our experimental design does not allow us to exclude
the possible involvement of other signals in preferences that lead to mating
(Coyne, 1993). Further
investigations are needed to evaluate the respective role of salivary and
urinary cues in mate choice between the two subspecies of the house mouse.
Evolution of the recognition system
We have shown that female M. m. musculus discriminate in favor of
M. m. musculus signals both when they are carried by males from the
same population (Denmark) and males from various allopatric populations.
Hence, it appears that M. m. musculus and M. m. domesticus
male signals have diverged in Denmark and that allopatric M. m.
musculus signals are also different from M. m. domesticus
signals. These results indicate that both a subspecies signal occurs in
populations of Denmark and that this male signal divergence from a putative
ancestral signal was at least partly initiated in allopatry.
Our experimental setting presents exactly the same pair of stimuli to
M. m. musculus and to M. m. domesticus females. Hence, the
narrower distribution of the ratio of preference within M. m.
musculus, as compared to M. m. domesticus, may suggest that the
former females would be sensitive to a smaller range of signals (only M.
m. musculus type signals) than M. m. domesticus (both types of
signals) (Figure 2). Moreover,
the overall higher variability of preference in M. m. domesticus may
be an indication that this subspecies has retained an ancestral wide-ranged
sensitivity (allowing a sensitivity to both M. m. musculus and M.
m. domesticus signals), as described for other species
(Ryan and Rand, 1995).
|
This variability in female M. m. domesticus preference may
parallel that of the signals in the males (coevolution of the system) and
hence may indicate that the divergence between the MRS of the two subspecies
is only due to a differentiation in M. m. musculus. Another
alternative involves uncoupled evolution of signals and preferences in M.
m. domesticus suggesting that, although male signals have diverged,
females have retained an ancestral wide-ranged preference
(Ryan and Wagner, 1987).
Still, discrepancies between the two subspecies may also be due to differences
in signal perception.
In the light of the above considerations, we propose that two types of
process may be involved in the evolution of the recognition system of the
house mouse. The first considers that the pattern of divergence, as evidenced
in Denmark, may characterize both subspecies across their entire range. Thus,
divergence may have taken place either during their independent evolution in
allopatry, or it may be the result of an earlier founder event
(Mayr, 1963). The first
alternative involves the accumulation of genetic differences through genetic
drift and/or adaptation to different environments. Still, overall differences
in the ecology or social structure of the two subspecies are not obvious
(Sage, 1981;
Van Zegeren and Van Oortmerssen,
1981), and the width of their geographical range suggests that
both occur in variable environments, supporting drift rather than adaptation
as the cause of divergence. The second alternative considers that the founder
groups that gave rise to the two subspecies retained a different part of the
ancestral polymorphism. Both alternatives imply that divergence between M.
m. musculus and M. m. domesticus recognition systems would have
been initiated in allopatry. A second process considers that the divergence
leading to isolation between the two taxa would have taken place after the
contact between the two subspecies, which refers to the process of
reinforcement (for reviews, see Howard,
1993; Noor,
1999).
The relevance of the first or the second process to the understanding of
the evolution of the house mouse recognition system relies on the presence or
absence of similar preferences and signals in populations from different
geographic areas. The salivary signals seem to have evolved in allopatry
(Karn and Dlouhy, 1991). As
far as the urinary signals and the preferences are concerned, a comparison
between allopatric versus hybrid zone populations is required before we can
draw firm conclusions.
Choosy M. m. musculus and nonchoosy M. m.
domesticus
If the different patterns of preference displayed by females of the two
populations represent differences that are characteristics of the two
subspecies in Denmark, they could either be the result of the two taxa
evolving at a different pace or the result of the two taxa being subjected to
different selective pressures in their area of contact. M. m.
musculus and M. m. domesticus have distinct genetic
characteristics (Dod et al.,
1993; Fel-Clair et al.,
1996,
1998), and their hybrids
exhibit an impaired fitness (Fel-Clair,
1995). However, so far, there are no data available suggesting
that reciprocal crosses between the two subspecies yield hybrids with
different levels of fitness (J. Britton-Davidian et al., unpublished results).
Hence, the causes of this nonsymmetric divergence are to be found
elsewhere.
Two studies suggest that M. m. musculus and M. m.
domesticus, whether in contact or not, differ in their aggressiveness. By
testing populations of mice from the Danish
(Thuesen, 1977) and German
hybrid zone (East Holstein) as well as allopatric populations
(Van Zegeren and Van Oortmerssen,
1981), several authors have shown that M. m. domesticus
males are more aggressive and always dominate male M. m. musculus
(either in their territory or in empty patches). Dominance of male M. m.
domesticus over male M. m. musculus suggests that, all things
being equal, female M. m. musculus could be more exposed to male
M. m. domesticus than female M. m. domesticus to male M.
m. musculus. Hence, when the two types of populations meet, the
probability of yielding hybrid progeny would be higher for female M. m.
musculus than for female M. m. domesticus. Thus, female M.
m. musculus could be under a stronger pressure to evolve assortative
mating than female M. m. domesticus for which access to a foreign
male would be limited by familiar males. This is a scenario consistent with a
stronger past flux of M. m. domesticus alleles into the M. m.
musculus genome (Dod et al.,
1993; Ferris et al.,
1983), which may have happened when the two taxa first met.
Consequently, the formation of the hybrid zone and the divergence of M. m.
musculus MRS could have taken place in parallel. The actual homogamic
mating regime of M. m. musculus would suffice to impede gene flow
between the two subspecies (Littlejohn,
1993). However, the hybrid zone is now-adays composed of highly
recombined populations, suggesting that direct contact and gene flow between
the two subspecies is probably rare. Hence, our latter scenario would need to
consider that for divergence of M. m. musculus to persist, either
discrimination against mice from intermediate hybrid populations occurs,
and/or hybrid males have features similar to those of male M. m.
domesticus as far as aggression and dominance are concerned.
Homogamic preference within the M. m. musculus population suggests that reproduction between the two populations would be limited. Nevertheless, further investigations involving a larger number of populations in and outside of the contact zone are needed to test the different scenarios presented in this article.
|
ACKNOWLEDGEMENTS |
|---|
We thank the 1998 field team with whom the trapping of these populations was done (Laboratory Genome Population Interaction, UMR 5000 and related). The same laboratory provided information on genetic characteristics of our mice. Special thanks go to J. Tønes Nielsen for kindly collecting the M. m. musculus sample and for his constant interest in the work done in the hybrid zone, as well as to Richard Østerballe and Givskud zoo. We are grateful to Gilbert Pistre for his skillful help in the design and the building of the behavioral apparatus, Marco Perriat-Sanguinet for looking after our mice, and J. Britton-Davidian and J. Catalan for their warm and constant support. We also thank R. Butlin and S. Brown for their comments on the manuscript. This work could not have been achieved without the extraordinary hospitality of Danish farmers. This is a contribution of UMR 5554, no. ISEM 2001/60.
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