Behavioral Ecology Advance Access originally published online on June 19, 2006
Behavioral Ecology 2006 17(5):757-764; doi:10.1093/beheco/arl014
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Divergence of mate recognition in the African striped mouse (Rhabdomys)
a School of Animal, Plant and Environmental Sciences, University of the Witwatersrand, WITS 2050, Johannesburg, South Africa and b Laboratoire Génétique et Environnement, Institut des Sciences de l'Évolution, UMR 5554 (CNRS), Université Montpellier II, France
Address correspondence to N. Pillay. E-mail: nevillep{at}biology.biol.wits.ac.za.
Received 1 February 2006; revised 12 April 2006; accepted 3 May 2006.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Mate recognition systems (MRSs) are complex signal-receiver traits. The present study addressed the roles of phylogeny, ecology, and geography in shaping the MRS of the African striped mouse (Rhabdomys), which has a wide distribution in southern Africa. Two putative species are recognized, which have different ecologies: Rhabdomys pumilio (arid) and Rhabdomys dilectus (mesic). The latter may be further subdivided into 2 subspecies (R. dilectus dilectus and R. dilectus chakae). Using 2 discrete populations per taxon, we investigated within- and between-taxon variations in male odor quality and female perception using habituation-discrimination and habituation-generalization tests, and female preference in 2-way choice tests. Our results indicate: 1) no within-taxon variation in odor quality, perception, or preference; 2) the 2 subspecies of R. dilectus carry signals of different qualities but share a common odor characteristic distinct from that of R. pumilio; 3) female R. pumilio did not show a preference when their own species and R. d. chakae odors were presented simultaneously but displayed assortative preference when the alternative was R. d. dilectus; 4) females of the 2 subspecies showed dissimilar preferences: R. d. chakae for the genetically more similar taxon and R. d. dilectus for the most different one. Although we could not rule out the influence of ecology, we concluded that phylogeny appeared a more parsimonious explanation for the pattern of divergence in Rhabdomys. Further, we discuss our results in light of current models on signal-receiver coevolution.
Key words: allopatric divergence, female preference, mate recognition, odor, signal-receptor coevolution, soiled bedding.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Geography, ecology, and phylogeny are some of the major factors that shape the evolution of mate recognition systems (MRSs). Examples of geographical influences include genetic drift and sexual selection (West-Eberhard 1983
; Herring and Verrell 1996; Mousseau and Olvido 2001) and evolution in small populations after founder events (Kaneshiro and Boake 1987). Ecological influences may be direct, such as interactions with competitors and/or predators, adaptation of signals to the transmission properties of different habitats (Endler and Basolo 1998; Nagel and Schluter 1998; Podos 2001), or indirect through adaptations to specific characteristics of the environment (e.g., resource availability; Rundle et al. 2005), and through ecologically induced morphology that may influence signal characteristics (Seddon 2005). Phylogeny may determine the mode of communication involved (e.g., olfaction, auditory), and shared ancestry and genetic relatedness may constrain the evolution of mate signaling and recognition as these may be innovations of ancestral conditions (Phelps and Ryan 2000; de Kort and ten Cate 2001; Ryan et al. 2001). Further, some studies have suggested that signal and genome similarities covary (Heth et al. 2001; Todrank and Heth 2003).
The MRS involves 2 components: the emitter of the signal and the receptor. Functionality of the system involves coherence between the 2 entities and hence a form of coevolution between them as a consequence of strong stabilizing selection. Empirical studies tend to reject the genetic coupling hypothesis that supposes a common genetic basis for the 2 communication entities (Butlin and Ritchie 1994). An increasing number of studies also suggest that signal and receiver may coevolve in a nonparallel rather than in a lock-step fashion (Schul and Bush 2002; Gerhardt 2005). Nonparallel evolution may be the result of sensory drive (Endler 1992) and/or sensory exploitation (Ryan et al. 1990; Endler and Basolo 1998), 2 mechanisms that can explain "hidden preference" and evolution of new signals. Nevertheless, the generality of these mechanisms has been questioned (Schul and Bush 2002).
Understanding the evolution of MRSs requires an assessment of both signal and perception characteristics. Unlike visual and acoustic mate recognition traits (Butlin and Ritchie 1994; Gerhardt 2005), olfactory ones are rarely described (Singer et al. 1997; Kayali-Sayadi et al. 2003), possibly because they are cryptic to human observers, complex to analyze, and the actual mate signal is difficult to isolate from the entire chemical mixture. Behavioral techniques such as habituation-discrimination (designed to assess differences among odors; see review in Halpin 1986) and the habituation-generalization (designed to assess odor similarities; Todrank and Heth 2003) can be used to provide qualitative assessments of odor signals and to compare their perception characteristics in individuals, populations, and species (Gregg and Thiessen 1981; Todrank and Heth 2003).
The aim of our study was to investigate variation in mate recognition characteristics within and between taxa of the African striped mouse (genus Rhabdomys). Rhabdomys is an excellent model for assessing the influences of geography, ecology, and phylogeny on an odor-based MRS. It has a wide geographic distribution occurring in most biomes in southern Africa (Skinner and Smithers 1990). Moreover, previous breeding studies revealed behavioral incompatibilities and reduced interpopulation reproductive success among 3 widely spaced (>900 km) populations (Pillay 2000a, 2000b), strongly suggesting that the signal and receiver components of the MRS may vary geographically. Historically, Rhabdomys was described as a monospecific genus, Rhabdomys pumilio (De Graaff 1981). However, a recent phylogeographical study, using complete sequences of the mtDNA cytochrome b gene and cytogenetic approaches, revealed 2 major lineages, supporting the existence of 2 putative species: R. pumilio (clade 2) occurring in the western (i.e., xeric) parts of South Africa and characterized by the ancestral karyotype of the genus (2n = 48) and Rhabdomys dilectus (clade 1) occurring in mesic areas (Rambau et al. 2003). Within clade 1, diploid number dichotomy coupled with sequence divergence suggested the distinction of 2 subspecies: Rhabdomys dilectus chakae (2n = 48) in the east of South Africa and R. dilectus dilectus (2n = 46) in the northern parts of the Rhabdomys range (Rambau et al. 2003). Ecological differences between the 2 clades also underpin differences in social organization (Schradin and Pillay 2005). Rhabdomys pumilio in the arid succulent karoo forms social groups, comprising multiple adults of both sexes that share a nest and the same territory, and which defend their shared territory against other groups (Schradin 2004), whereas R. d. chakae in the moist grasslands of South Africa is solitary and territorial (Schradin and Pillay 2005). The social organization of R. d. dilectus seems to be similar to that of R. d. chakae (Brooks 1974). The 2 subspecies are parapatric in parts of their range in northern South Africa, but no contact zone or naturally occurring hybrids have been located despite intensive field surveys (N Pillay, personal observation).
Using 2 geographically distinct populations for each of the putative taxa, we assessed differences and similarities in male odor quality as well as variation in female perception during habituation-discrimination and habituation-generalization tests and assessed female preference during 2-way choice tests. We tested female subjects because mate choice is more easily detected in female Rhabdomys (Bennett and Pillay 2001), and we used soiled bedding as the odor source, which is known to be an effective carrier of mate choice signals (Pillay 2000a).
We predicted that if geography was the major factor shaping mate recognition in Rhabdomys, within-taxon variation should be similar to between-taxon variation, resulting in a negative relationship between mate recognition and geographical distance. If phylogeny had a major role in shaping Rhabdomys MRS, we predicted lower within-taxon variation and greater differences between R. pumilio and R. dilectus than between the 2 putative R. dilectus subspecies. However, we realize that R. pumilio and R. dilectus occur in different ecological circumstances, so that the influence of ecology and phylogeny may be coupled. Still, we hypothesized that if divergence occurs between the 2 R. dilectus subspecies, which occur in similar environmental conditions, it may reflect phylogenetic rather than ecological differences. Finally, we assessed patterns of divergence in signal quality and perception in light of current models of signal-receiver coevolution.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Mice and odor samples
Study subjects were captive born progeny (G2–G4) of striped mice originating from 6 different South African localities (Figure 1), including representatives of 2 populations of each of the 3 putative taxa. Mice were housed singly or in the same sex groups (2–3 individuals). Cages (25 x 25 x 12 cm; Labotec, South Africa) were provided with a 2-cm layer of wood shavings for bedding and hay for nesting material. Food (mouse cubes) and water were available ad libitum. Populations were kept in separate rooms under the same controlled laboratory conditions.
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Four weeks before the start of experiments, test females and scent donor males were kept singly. Only estrous females were used (confirmed by vaginal smears taken 2 h before the start of tests). The stimulus used was soiled bedding of adult males, which was expected to contain the males' odor. The odors present in the soiled bedding most likely contained several volatile and nonvolatile components. We controlled for variation in odors by housing the donor males singly and under the same standardized conditions, and for individual differences between donors by pooling bedding from at least 5 different mice to produce a population odor signal. The soiled bedding were kept at –20°C prior to experiments and thawed at room temperature immediately before tests. An odor stimulus consisted of 30 g soiled bedding presented in a petri dish. All experiments took place between 08:00 AM and 01:00 PM, which is the peak activity period of Rhabdomys (Schradin 2006
).
Experimental procedures
Odor discrimination tests
Habituation-discrimination is a procedure used to assess perception of differences in odor signals (Halpin 1986). We used 2 variations of this procedure. Both procedures start with a habituation phase during which the test subject is presented with a "habituation" odor; habituation occurs when the subject's interest in the odor decreases. In the first procedure, the habituation phase is followed by a test phase during which the subject is presented simultaneously with the habituation odor again (but a different sample) and a different test odor. If the subject spends more time investigating the test odor, it is interpreted that it perceives the test odor as different from the habituation odor. In the second procedure, known as habituation-generalization (Todrank and Heth 2003), the 2 odors presented in the test phase are different to the habituation odor. Hence, this procedure allows for the assessment of the similarities between the 2 test odors and the habituation odor. Significant differences in the time spent investigating the test odors (i.e., discrimination) indicate that they are perceived differently, and the lesser investigated odor is regarded as more similar to the habituation odor. Presenting the stimuli only once as opposed to repeatedly (see e.g., Isles et al. 2001) reduced our interference of test subjects in both procedures.
Our aim was to compare differences in odor quality (i.e., quantitative and/or qualitative) and in odor perception. Although a lack of discrimination could be ascribed either to odor similarity or to perception deficiency, discrimination provides unambiguous evidence that the 2 odors presented are different.
A total of 10–30 females per population were used in the odor discrimination tests (a series of 19 experiments, n = 10 for each). Females were never used more than twice; those used 2 times were exposed to different stimuli and had a rest period of 3 days between experiments. In order to compare odor qualities and assess variation in perception of odor differences within and among taxa, females of different populations were presented with odor of males in different taxon combinations. Tests took place in a plexiglas apparatus, comprising 2 boxes: a start box and a test box (both: length = 36 cm, width = 20 cm, height = 16 cm) connected by a short tunnel (internal diameter 4.6 x 18 cm). Between each experiment, the entire apparatus was thoroughly washed with soap, water, and a 20% alcohol solution.
The habituation phase lasted 18 min. We chose this time because the results of pilot tests showed comparatively slow response times of females to the test apparatus, and we believed that this time interval was short enough to prevent substantial odor degradation. Indeed, the chemical characteristics of rodent scent marks (i.e., presence of protein carriers) result in a slow release of volatiles and relative resistance to air degradation (Hurst et al. 1998). During the habituation phase, a test female was placed in the start box, and the stimulus was placed in the test box at the wall furthest away from the entry into the box. After a short familiarization period, the female was allowed to enter the test box, and the time she spent sniffing the stimulus was recorded. A 9-min discrimination phase immediately followed the habituation phase; the test box was replaced and 2 other stimuli were placed on the floor of the new test box at the left and right extremities. We controlled for laterality by alternating the left and right position of each type of stimulus presented to test females within each population. We recorded the time spent sniffing each stimulus.
Preference tests
In order to assess preferences of female striped mice for male odors of different taxa, we conducted 2-way choice tests, each lasting 18 min. The responses of 10–12 females per population were tested in a series of 12 experiments in a choice apparatus built of transparent plexiglas material, comprising a start box (length = 36 cm, width = 20 cm, height = 16 cm) connected via a Y maze (internal diameter 4.6 cm; main branch: 32 cm long; secondary branches/arms: 22 cm long) to 2 choice chambers (length = 36 cm, width = 20 cm, height = 16 cm).
At the beginning of each test, a female was placed in the start box, and 30 g of soiled bedding was placed in each choice chamber. After a few minutes of familiarization, the test female was allowed to enter the Y maze. Recording started once the mouse had entered the maze. In all tests, females entered both branches of the Y maze repeatedly. We controlled for laterality by alternating the position of the 2 stimuli (left and right) between tests. We recorded the time a female spent in contact with, sniffed or licked each stimulus.
Data recording and analysis
All observations were recorded live using the Observer software (version 3.0 for Windows; Noldus Information Technology, B. V. Wageningen, The Netherlands) on a personal computer. Habituation was assessed by comparing the time that females spent with the stimulus during six 3-min segments using a Friedman ANOVA test. Data sets for the discrimination phase and preference experiments were analyzed using the Wilcoxon matched-pairs test. The 
was set at 0.05, and all tests were 2 tailed except for the test phase in the standard habituation-discrimination procedure which was 1 tailed because one of the test odors was identical to the habituation odor.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Odor quality and perception
To establish whether habituation occurred during the habituation-discrimination tests, we compared the time spent sniffing the habituation odor in six 3-min segments. In all 190 tests, females showed a significant decline of interest in the habituation odor from the first 3 min onwards (Fr = 489.62, P < 0.001; Figure 2), indicating that they had become habituated to the stimulus during the habituation phase.
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Between-taxa comparisons of perception and odor qualities
Females of the 3 taxa consistently discriminated between odor of their own population males and those of the other taxa. Female R. pumilio discriminated between odor stimuli of male R. pumilio and those of R. d. chakae (Table 1, line a) and R. d. dilectus (Table 1, line b), females of both R. dilectus subspecies discriminated between stimuli of males of their own and the other subspecies (Table 1, lines c, d), and female R. d. chakae discriminated between odors of R. pumilio and R. d. dilectus (Table 1, line e). However, there appeared to be differences in perception characteristics of the 2 putative Rhabdomys species because unlike R. dilectus, female R. pumilio did not discriminate between the odor stimuli of R. d. dilectus and R. d. chakae males (Table 1, lines f and g).
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Consistently across populations and taxa, odor stimuli of R. d. dilectus and R. d. chakae males were perceived as more similar to each other than to those of male R. pumilio (Table 1, lines h–m). Moreover, R. pumilio and R. d. chakae females perceived odors of males of both subspecies as equally different from R. pumilio (Table 1, lines n–p).
Within-taxon comparison of perception and odor qualities
Females of all 3 taxa did not differentiate between the odor of males of their own population and of males of distant populations of the same taxon (Table 1, lines q–s), indicating that the odor characteristics of different populations of the same taxon are perceived as similar. Consistency across populations of a given taxon in the assessment of odor qualities of other taxa (Table 1) further suggests low geographical variation in odor qualities and perception within each of the 3 taxa.
Odor preference
The 2 R. dilectus subspecies did not display the same pattern of preference. Rhabdomys d. dilectus significantly preferred odors of male R. pumilio when the alternative choice was odors of male R. d. chakae, whereas R. d. chakae preferred odors of R. d. dilectus when the alternative was odors of R. pumilio (Figure 3), these results being consistent across populations regardless of geographical distance (Figures 1 and 3). In contrast, female R. pumilio spent a similar duration of time sniffing the odor of males of both subspecies of R. dilectus when they were presented simultaneously (Figure 3). Moreover, in choice tests where the alternatives were stimuli of a different population of R. pumilio versus the other species, female R. pumilio (Goegap) sniffed odor of their own species (Gariep Dam) and that of R. d. chakae (Suikerbosrand) to the same extent (n = 10, T = 16, P = 0.274), whereas they displayed a significant assortative preference when the alternative was the odor of male R. d. dilectus (Cullinan; n = 10, T = 2, P = 0.006). Finally, test females of all 3 taxa did not show a directional preference when presented with stimuli of males from their own population versus those from a distant population of the same taxon: R. pumilio females from Geogap (n = 11, T = 21, P = 0.286) and Gariep Dam (n = 10, T = 27, P = 0.95); R. d. dilectus females from Cullinan (n = 10, T = 23, P = 0.656) and Potchefstroom (n = 11, T = 27, P = 0.594); and R. d. chakae females from Suikerbosrand (n = 12, T = 14, P = 0.091) and Willem Pretorius (n = 10, T = 21, P = 0.508).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Four general patterns were revealed in our study. Firstly, within-taxon differences were not detected, which contrasts with evidence for divergent olfactory signals in the 3 taxa. Moreover, patterns of preference and odor perception were consistent within a taxon but differed between taxa. Secondly, across populations and taxa, odors of the 2 R. dilectus subspecies were perceived as more similar to each other than to that of R. pumilio, and R. pumilio and R. d. chakae consistently assessed odors of the 2 R. dilectus subspecies as equally different from that of R. pumilio, suggesting that the 2 subspecies of R. dilectus share a common odor characteristic, distinct from that of R. pumilio. Thirdly, females of both R. dilectus subspecies discriminated between male odors of the 2 subspecies. However, although habituation occurred, female R. pumilio did not discriminate between the odors of the 2 subspecies, suggesting differences in the perception characteristics of females of the 2 Rhabdomys species. In fact, female R. pumilio did not treat odors of the 2 R. dilectus subspecies differently when these were presented simultaneously, whereas they did when the R. pumilio odor was presented together with either one of the subspecies odors, indicating that discrimination of R. dilectus male odors by R. pumilio females may be context dependent. Finally, although females of both R. dilectus subspecies showed an assortative preference for male odors of their own versus the other taxon previously (Pillay 2000a
), in the present study, when the choice was between R. pumilio and the other subspecies of R. dilectus, females of the 2 subspecies showed dissimilar preferences: one for odor of the more genetically similar taxon and the other for the most different odor, indicating that patterns of preference within R. dilectus have diverged (Table 2).
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Geography, ecology, and phylogeny
Within-taxon comparisons of odor quality, perception, and preference yielded remarkably consistent results, suggesting that geographical variation within the Rhabdomys taxa is very low. Nonetheless, gene flow between these populations is likely to be restricted by extrinsic barriers, such as long distances (e.g., >500 km between the 2 R. pumilio populations) and major obstacles to migration (natural and anthropogenic). An absence of between-population variation is not commonly reported (Ritchie 1991
; Ryan et al. 1992; Herring and Verrell 1996; Foster 1999) and contradicts results obtained for other rodents, which show discrimination between odor sources of individuals from different demes (Cox 1984, 1989; Hurst and Barnard 1992) or geographically distant populations (Pillay et al. 1995; Theiler and Blanco 1996; Heth et al. 2001). The latter studies involved individual odor stimuli compared with pooled odors in our study, which we expected to minimize interindividual differences and not mask characteristics supposedly shared by all individuals of a given population. Hence, "population odors" may not exist in Rhabdomys or alternatively that population divergence in this genus may involve odor components of specific characteristics (e.g., high volatility) that may not be easily detected in our experimental design. Notwithstanding, odor components that facilitated discrimination between taxa were detected in this study.
The absence of variation between geographically distant populations within each of the 3 taxa may reflect that isolation between populations is relatively recent and/or that the Rhabdomys MRS may be subjected to strong stabilizing selection (e.g., specific environmental constraints). All 3 taxa have wide geographic distributions (Rambau et al. 2003), which may include different habitat types and potentially result in between-population geographic variation, specifically, the 2 populations of R. pumilio occur in slightly different habitats (Table 3). Nevertheless, our results suggest that such geographic differences may not be the primary factors causing signal divergence. Further laboratory and field investigations involving genetic and behavioral ecology approaches of populations occurring in different habitats may be necessary to elucidate the causes underlying apparent within-taxon homogeneity in the Rhabdomys MRS.
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Between-taxa comparisons of odor quality and perception revealed marked divergence between R. dilectus and R. pumilio and a lesser pattern of divergence between R. d. dilectus and R. d. chakae. This pattern is in agreement with the recent proposal of Rhabdomys taxonomy based on an mtDNA phylogeny (Rambau et al. 2003
). The cladogenesis event resulting in R. pumilio and R. dilectus is dated at 2.9 MYA, which was a period of extensive paleoclimatic oscillations, resulting in vegetation changes and habitat fragmentation (references within Rambau et al. 2003). In contrast, subspeciation within R. dilectus would have taken place more recently (some 600 000 years ago). Hence, under the phylogenetic hypothesis, the MRS of the 2 Rhabdomys species has most probably diverged in allopatry. Similarly, chromosomal divergence and mtDNA variation within R. dilectus presupposes a period of isolation between R. d. dilectus and R. d. chakae (Rambau et al. 2003). Our results concur with other studies, showing a consistency between phylogeny and signal (Heth et al. 2001, 2002) and/or perception similarities (Ryan and Rand 1999; de Kort and ten Cate 2001; Ryan et al. 2001). However, unlike other studies involving several rodent species (Heth and Todrank 2000; Heth et al. 2002, 2003), we did not observe parallel evolution at the population level in Rhabdomys. Hence, our results do not seem to support the odor-genes covariance hypothesis (Todrank and Heth 2003) as a mechanism of evolution of Rhabdomys MRS.
Divergence between R. pumilio and the 2 R. dilectus subspecies is also consistent with ecological differences (arid versus moist grassland habitats, Table 3), which is associated with differences in population density (high in arid and low in grasslands) and social organization (Schradin and Pillay 2005). However, such differences have not been documented between the 2 R. dilectus subspecies. We are yet to establish the role of ecological factors, such as competition for signal space, predation, and habitat structure, which are known to influence the evolution of mate signaling systems in other taxa (Nelson 1989; Ryan 1990; Butlin and Ritchie 1994; Seddon 2005), but to our knowledge, they were never investigated in odor-based systems. We realize that only tight covariance between ecological divergence and mate recognition characteristics may explain the patterns observed in our study, and consequently, although we do not exclude the influence of ecology in shaping Rhabdomys recognition system, at this stage of our investigations, phylogeny is a more parsimonious explanation for the patterns of divergence.
Patterns of coevolution of signal and receiver within Rhabdomys
Previous studies involving mammal models have either addressed signal evolution in different rodent species (Heth and Todrank 2000; Heth et al. 2001, 2002) or investigated variation in perception in a single species (e.g., the tufted capuchin Cebus paella (Ueno 1994). To our knowledge, ours is the first study that addresses both signal and receiver evolution in an odor-based mammal MRS.
The 2 R. dilectus subspecies carry a common odor characteristic, different from that of R. pumilio, which we can code as follows: R. pumilio = A, R. d. dilectus = Ac, and R. d. chakae = AC. "C" and "c" may be 2 states of the same character which could be, for example, a new molecule at 2 different concentrations. Using this coding, our results indicate that female R. pumilio (A) habituated to AC but could not discriminate between AC and Ac, suggesting, firstly, that the receiver component of R. pumilio recognition system does not recognize C in either of its states (C or c) or, secondly, that R. pumilio does recognize "C or c" but assesses them as similar to each other. Both explanations may be consistent with the absence of preference by female R. pumilio when given a choice between R. d. dilectus and R. d. chakae, despite spending approximately 70% of the tests in contact with the 2 odors. However, only the second explanation is consistent with patterns of preference of R. pumilio when the choice was between male R. pumilio odor and the odor of one of the 2 subspecies. Indeed, R. pumilio preferred homotypic male odors when the alternative was R. d. dilectus, whereas they did not display a preference when the alternative was R. d. chakae (this study; Pillay 2000a), suggesting that female R. pumilio may consider R. d. chakae males, but not R. d. dilectus males, as potential mates. Rhabdomys d. chakae (C) seems to match a preexisting template of R. pumilio female preference, which may be consistent with the sensory bias exploitation hypothesis (Ryan and Rand 1993; Ryan 1998). Conversely, R. d. dilectus (c) is recognized but does not initiate a preference response in R. pumilio, which further underlines divergence in signal characteristics within R. dilectus.
Rhabdomys d. chakae preferred odors of R. d. dilectus when the alternative was R. pumilio, which is consistent with preference for more similar odors as shown in other studies (McLennan and Ryan 1999; Heth et al. 2003), and might suggest parallel signal-preference evolution in this taxon. In contrast, R. d. dilectus displayed a preference for R. pumilio when the alternative was R. d. chakae, indicating a preference for the more dissimilar odor, and suggesting that although odor quality and perception ability have diverged between R. pumilio and R. d. dilectus, the odor of R. pumilio is still assessed as that of a potential mate. An interpretation of these patterns may be that R. pumilio, the most basal species in the phylogeny (Rambau et al. 2003), retained an ancestral characteristic that does not facilitate perception of derived odor characteristics in R. dilectus. Moreover, R. d. dilectus, unlike R. d. chakae, would have retained the ancestral receiver characteristic, resulting in it regarding R. pumilio as a potential mate when the alternative is R. d. chakae. Our results indicate asymmetrical behavioral compatibilities among the different taxa, but they suffice to hinder interbreeding as breeding studies showed that such crosses yielded marked agonistic interactions, resulting in reproductive failure (Pillay 2000a, 2000b).
In conclusion, our results indicate that the evolution of the Rhabdomys MRS has involved qualitative differences in signal characteristics, preferences, and underlying mechanisms of perception, suggesting an absence of a lock-step mode of divergence. Moreover, evolution within the 2 R. dilectus subspecies and between the 2 Rhabdomys species seems to follow distinct trajectories. Further investigations of perception characteristics and chemical characterization of the odor signals of the 3 Rhabdomys taxa should allow for testing of some of the issues raised here and for gaining a better insight into the mechanisms involved in the divergence between the Rhabdomys taxa.
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ACKNOWLEDGEMENTS |
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Funding was provided by a Centre National de la Recherche Scientifique (France) and National Research Foundation (South Africa) joint research agreement. We thank Victor Rambau, Terry Robinson, Carole Smadja, and Carsten Schradin for commenting on an earlier version of the manuscript. Technical support was provided by Tracy Aenmey, Mike Bester, Jenny Lancaster, Kerry Nel, and Mathew van Lierop. This study was approved by the University of the Witwatersrand Animal Ethics Screening Committee (AESC 2002/86/3). Institut des Sciences de l'Evolution, Univeristé de Montpellier II 2006/026.
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REFERENCES |
|---|
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Bennett LN, Pillay N. 2001. Responses of male Rhabdomys pumilio to urine of conspecific females in different reproductive states. Proceedings of the 8th International Symposium on African Small Mammals; 1999 July; Paris. Paris, France: IRD Editions, Institut de Recherche pour le dévelopment—collection Colloques et seminaries. p 321–30.
Brooks PM. 1974. The ecology of the four-striped field mouse, Rhabdomys pumilio (Sparrman, 1784), with particular reference to a population on the Van Riebeeck Nature Reserve, Pretoria [DSc dissertation]. Pretoria, South Africa: University of Pretoria.
Butlin RK, Ritchie MG. 1994. Behaviour and speciation. In: Slater PJB, Halliday TR, editors. Behaviour and evolution. Cambridge, UK: Cambridge University Press. p 43–79.
Cox TP. 1984. Ethological isolation between local populations of house mice (Mus musculus) based on olfaction. Anim Behav 32:1068–77.[CrossRef]
Cox TP. 1989. Odor-based discrimination between noncontiguous demes of wild Mus. J Mammal 70:549–56.[CrossRef]
De Graaff G. 1981. The rodents of southern Africa. Durban, South Africa: Butterworths.
de Kort SR, ten Cate CT. 2001. Response to interspecific vocalizations is affected by degree of phylogenetic relatedness in Streptopelia doves. Anim Behav 61:239–47.[CrossRef][Web of Science][Medline]
Endler JA. 1992. Signals, signal conditions, and the direction of evolution. Am Nat 139:S125–53.[CrossRef][Web of Science]
Endler JA, Basolo AL. 1998. Sensory ecology, receiver biases and sexual selection. Trends Ecol Evol 13:415–20.[CrossRef]
Foster SA. 1999. The geography of behavior: an evolutionary perspective. Trends Ecol Evol 14:190–5.[CrossRef][Medline]
Gerhardt HC. 2005. Advertisement-call preferences in diploid-tetraploid treefrogs (Hyla chrysoscelis and Hyla versicolor): implications for mate choice and the evolution of communication systems. Evolution 59:395–408.[CrossRef][Web of Science][Medline]
Gregg B, Thiessen DD. 1981. A simple method of olfactory discrimination of urine for the Mongolian gerbil, Meriones unguiculatus. Physiol Behav 26:1133–6.[CrossRef][Medline]
Halpin ZT. 1986. Individual odors among mammals: origins and functions. Adv Study Behav 16:39–70.
Herring K, Verrell P. 1996. Sexual incompatibility and geographical variation in mate recognition systems: tests in the salamander Desmognathus ochrophaeus. Anim Behav 52:279–87.
Heth G, Todrank J. 2000. Individual odor similarities across species parallel phylogenetic relationships in the S. ehrenbergi superspecies of mole-rats. Anim Behav 60:789–95.
Heth G, Todrank J, Burda H. 2002. Individual odor similarities within colonies and across species of Cryptomys mole rats. J Mammal 83:569–75.[CrossRef]
Heth G, Todrank J, Busquet N, Baudoin C. 2001. Odor-genes covariance and differential investigation of individual odors in the Mus species complex. Biol J Linn Soc 73:213–20.[CrossRef]
Heth G, Todrank J, Busquet N, Baudoin C. 2003. Genetic relatedness assessment through individual odor similarities in mice. Biol J Linn Soc 78:595–603.[CrossRef]
Hurst JL, Barnard CJ. 1992. Kinship and social behavior in wild house mice: effects of social group membership and relatedness on the responses of dominant males toward juveniles. Behav Ecol 3:196–206.
Hurst JL, Roberston DHL, Tolladay U, Beynon RJ. 1998. Proteins in urine scent marks of male house mice extend longevity of olfactory signals. Anim Behav 55:1289–97.[CrossRef][Web of Science][Medline]
Isles AR, Baum MJ, Ma D, Keverne EB, Allen ND. 2001. Urinary odor preferences in mice. Nature 409:783–4.[Medline]
Kaneshiro KY, Boake CRB. 1987. Sexual selection and speciation: issues raised by Hawaiian Drosophila. Trends Ecol Evol 2:207–12.[CrossRef]
Kayali-Sayadi MN, Bautista JM, Polo-Diez LM, Salazar I. 2003. Identification of pheromones in mouse urine by head-space solid phase microextraction followed by gas chromatography-mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 796:55–62.[Web of Science][Medline]
Low AB, Rebelo AG. 1998. Vegetation of South Africa, Lesotho and Swaziland, 2nd ed. Pretoria, South Africa: Environmental Affairs and Tourism.
McLennan DA, Ryan MJ. 1999. Interspecific recognition and discrimination based upon olfactory cues in northern swordtails. Evolution 53:880–8.[CrossRef]
Mousseau TA, Olvido AE. 2001. Geographical variation. Encyclopedia of life sciences. Hoboken, NJ: Wiley. Available from: www.els.net. Accessed 6 June 2006.
Nagel L, Schluter D. 1998. Body size, natural selection, and speciation in sticklebacks. Evolution 52:209–18.[CrossRef][Web of Science]
Nelson DA. 1989. The importance of invariant and distinctive features in species recognition of birdsong. Condor 91:120–30.
Phelps SM, Ryan MJ. 2000. History influences signal recognition: neural network models of tungara frogs. Proc R Soc Lond B Biol Sci 267:1633–9.[Medline]
Pillay N. 2000a. Female mate preference and reproductive isolation in populations of the striped mouse Rhabdomys pumilio. Behaviour 137:1431–41.[CrossRef]
Pillay N. 2000b. Reproductive isolation in three populations of the striped mouse Rhabdomys pumilio (Rodentia, Muridae): interpopulation breeding studies. Mammalia 64:461–70.
Pillay N, Willan K, Meester J. 1995. Evidence of pre-mating reproductive isolation in two allopatric populations of the vlei rat (Otomys irroratus). Ethology 100:61–71.
Podos J. 2001. Correlated evolution of morphology and vocal signal structure in Darwin's finches. Nature 409:185–8.[CrossRef]
Rambau RV, Robinson TJ, Stanyon R. 2003. Molecular genetics of Rhabdomys pumilio subspecies boundaries: mtDNA phylogeography and karyotypic analysis by fluorescence in situ hybridization. Mol Phylogenet Evol 28:564–75.[CrossRef][Web of Science][Medline]
Ritchie MG. 1991. Female preference for "song races" of Ephippiger ephippiger (Orthoptera: Tettigoniidae). Anim Behav 42:518–20.[CrossRef]
Rundle HD, Chenoweth SF, Doughty P, Blows MW. 2005. Divergent selection and the evolution of signal traits and mating preferences. PLoS Biol 3:e368.[CrossRef][Medline]
Ryan MJ. 1990. Signals, species, and sexual selection. Am Sci 78:46–52.
Ryan MJ. 1998. Sexual selection, receiver biases, and the evolution of sex differences. Science 281:1999–2003.
Ryan MJ, Fox JH, Wilczynski W, Rand AS. 1990. Sexual selection for sensory exploitation in the frog Physalaemus pustulosus. Nature 343:66–7.[CrossRef][Medline]
Ryan MJ, Perrill SA, Wilczynski W, Rand AS. 1992. Auditory tuning and call frequency predict population-based mating preferences in the cricket frog, Acris crepitans. Am Nat 139:1370–83.[CrossRef]
Ryan MJ, Phelps SM, Rand AS. 2001. How evolutionary history shapes recognition mechanisms. Trends Cogn Sci 5:143–8.[CrossRef][Web of Science][Medline]
Ryan MJ, Rand AS. 1993. Species recognition and sexual selection as a unitary problem in animal communication. Evolution 47:647–57.[CrossRef]
Ryan MJ, Rand AS. 1999. Phylogenetic influence on mating call preferences in female tungara frogs, Physalaemus pustulosus. Anim Behav 57:945–56.[CrossRef][Web of Science][Medline]
Schradin C. 2004. Territorial defense in a group-living solitary forager: who, where, against whom? Behav Ecol Sociobiol 55:439–46.[CrossRef]
Schradin C. 2006. Whole-day follows of striped mice (Rhabdomys pumilio), a diurnal murid rodent. J Ethol 24:27–43.[CrossRef]
Schradin C, Pillay N. 2005. Intraspecific variation in the spatial and social organization of the African striped mouse. J Mammal 86:99–107.[CrossRef]
Schul J, Bush SL. 2002. Non-parallel coevolution of sender and receiver in the acoustic communication system of treefrogs. Proc R Soc Lond B Biol Sci 269:1847–52.[Medline]
Seddon N. 2005. Ecological adaptation and species recognition drives vocal evolution in neotropical suboscine birds. Evolution 59:200–15.[CrossRef][Web of Science][Medline]
Singer AG, Beauchamp GK, Yamazaki K. 1997. Volatile signals of the major histocompatibility complex in male mouse urines. Proc Natl Acad Sci USA 94:2210–4.
Skinner JD, Smithers RHN. 1990. The mammals of the southern African subregion. Pretoria, South Africa: University of Pretoria.
Theiler GR, Blanco A. 1996. Patterns of evolution in Graomys griseoflavus (Rodentia, Muridae). III. Olfactory discrimination as a premating isolation mechanism between cytotypes. J Exp Zool 274:346–50.[CrossRef]
Todrank J, Heth G. 2003. Odor-genes covariance and genetic relatedness assessments: rethinking odor-based "recognition" mechanisms in rodents. Adv Study Behav 32:77–130.
Ueno Y. 1994. Olfactory discrimination of urine odors from five species by tufted capucin (Cebus apella). Primates 35:311–23.[CrossRef]
West-Eberhard MJ. 1983. Sexual selection, social competition, and speciation. Q Rev Biol 58:155–83.[CrossRef]
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