Behavioral Ecology Advance Access originally published online on May 18, 2005
Behavioral Ecology 2005 16(4):818-822; doi:10.1093/beheco/ari058
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Species recognition by male swordtails via chemical cues
a Department of Biology, Boston University, 5 Cummington Street, Boston, MA 02215, USA, b School of Botany and Zoology, Australian National University, Canberra ACT 0200, Australia, and c Department of Biological and Environmental Sciences, P.O. Box 65, 00014, University of Helsinki, Finland
Address correspondence to B.B.M. Wong. E-mail: bob.wong{at}helsinki.fi.
Received 1 October 2004; revised 18 March 2005; accepted 21 April 2005.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Species recognition can often play a key role in female mating preferences. Far less is known about conspecific mate recognition from the male perspective. In many closely related taxa, females exhibit few obvious visual differences and males might have to attend to chemical cues in mate recognition, a possibility that has rarely been explored in vertebrates. Here, we examine male species recognition via odor cues in the swordtail fish, Xiphophorus birchmanni. In dichotomous choice experiments we first tested whether males respond to female odor cues. We found that males were attracted to conspecific female odor and those of a related allopatric congener, Xiphophorus malinche, over a water control. Males did not, however, respond to the female odor of the more distantly related sympatric platyfish, Xiphophorus variatus. We then gave male X. birchmanni the choice between conspecific and heterospecific female stimuli. Males, in this scenario, significantly preferred the conspecific odor when the alternative was platyfish. However, when offered odor cues of X. malinche, male X. birchmanni actually preferred the heterospecific female cue. The complex array of preferences reported here, previously documented only in females, underscores the need to consider the behavior of both sexes in dictating actual mating outcomes.
Key words: chemical communication, mate choice, Poeciliidae, reproductive isolation, sexual selection, speciation.
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Premating reproductive isolation hinges on the ability of individuals to recognize their mates. While the mating preferences of females have widely been shown to favor conspecifics over heterospecifics (de Kort and ten Cate, 2001
; Pfennig, 2000), males have generally been assumed to play a minimal role in mate discrimination. Male behavior, however, can influence matings by reinforcing what females want or, in some instances, by subverting female mating preferences (Wong, 2004; Wong and Candolin, in press). For example, males can be indiscriminate and court both heterospecific and conspecific females alike (Gabor and Ryan, 2001). More insidiously, males can engage in forced or surreptitious fertilization, thereby circumventing female choice (Magurran, 1998). Male mate choice can also be important. Studies have shown, for example, that mate searching and courtship can both impose fitness constraints that limit male mating opportunities, causing males to allocate their mating effort strategically and to discriminate between potential mates (Gowaty et al., 2003; Wong and Jennions, 2003). Although males might be expected to avoid heterospecific females and to prefer conspecifics (Gabor and Ryan, 2001; McKinnon and Liley, 1987; McLennan, 2005; Wiernasz, 1995), there is no a priori reason why male preferences and female cues cannot be decoupled. We know, for instance, that females may sometimes prefer to mate with heterospecific males expressing traits that are more attractive than those found in their own species (Ryan and Wagner, 1987). In a similar way, males could also respond in favor of heterospecific females.
In many taxa, females from closely related species exhibit few obvious visual differences. Chemical cues, however, are often species specific (Wyatt, 2003) and may therefore provide a mechanism for males to discriminate among potential mates. Despite this, almost all the studies that have examined the role of odor cues in vertebrate mate recognition have looked at the question solely from a female choice perspective (Crapon de Caprona and Ryan, 1990; Hankison and Morris, 2003; McLennan and Ryan, 1997, 1999; but see Cardwell et al., 1992; McKinnon and Liley, 1987; McLennan, 2005; Yambe and Yamazaki, 2001). In this study, we sought to test the role of chemical signals in species recognition by males in a group of closely related fishes with few apparent interspecific differences in female phenotypes (Rauchenberger et al., 1990).
Xiphophorus birchmanni is a small, sexually dimorphic poeciliid fish belonging to the monophyletic northern, or Río Pánuco Basin, clade of swordtails (Morris et al., 2001; Rauchenberger et al., 1990). When in sympatry, X. birchmanni hybridizes freely with Xiphophorus malinche (Rosenthal et al., 2003), a closely related swordtail (Morris et al., 2001; Rauchenberger et al., 1990), yet there is no evidence of hybridization with the more distantly related platyfish, Xiphophorus variatus. Studies focusing on female choice in a range of swordtail species suggest that chemical signals play an especially prominent role in species recognition and mate choice (Crapon de Caprona and Ryan, 1990; Hankison and Morris, 2003; McLennan and Ryan, 1997, 1999). For instance, female swordtails often prefer the visual cues of heterospecifics and yet show robust preferences for conspecific male odor cues (Crapon de Caprona and Ryan, 1990; Hankison and Morris, 2003). In X. birchmanni, recent work on female mate recognition demonstrated that females prefer the odor cues of conspecific males over those of male X. malinche (Fisher HS, Wong BBM, Rosenthal GG, unpublished data). What about conspecific recognition of females by male X. birchmanni? In this study we evaluated whether male X. birchmanni attend to species differences in female chemical cues by measuring their responses to odor from female conspecifics and two congeners, X. malinche and X. variatus.
|
METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Animal collection and housing
Xiphophorus birchmanni and X. variatus were collected from the Rio Garces, San Luis Potosí, México (Rauchenberger et al., 1990
). Xiphophorus malinche were collected from the type locality in the Río Claro at Tlatzintla, a population in allopatry from X. birchmanni (Rauchenberger et al., 1990). Sexually mature females were isolated from males for at least 3 weeks prior to testing and were housed in well-planted single-species 40-l aquaria. Animals were maintained on a 12:12 h light:dark cycle and were fed TetraMin flakes, brine shrimp, bloodworms, and mysids. All fish were fed the same diet to control for the possibility that individuals maintained on different diets may elicit different responses (Murray and Jenkins, 1999). Food was delivered in a wash bottle to train test subjects to investigate surface disturbance (see Chemical Preference Tests; McLennan and Ryan, 1997).
Chemical stimulus preparation
We collected female odor cues using 40-l aquaria that were thoroughly cleaned using a solution of soap and hydrogen peroxide. Water in collecting tanks was carbon filtered and aerated for 24 h prior to introduction of females. Female odor stimuli were prepared by placing five sexually mature females of the same species into a single tank (a given stimulus tank, therefore, only contained the odor cues from one species). The mean standard lengths (SL) ± SD of stimulus females were as follows: X. birchmanni = 36.75 ± 3.37 mm, X. malinche = 36.33 ± 3.08 mm, and X. variatus = 36.17 ± 3.54 mm. The tank housing the females was located adjacent to another aquarium containing two conspecific males to provide them with visual stimulation. After 24 h, females were removed from collection tanks, and stimulus water was used in experiments within 48 h (McLennan and Ryan, 1999). Using this procedure, we obtained stimulus water containing cues from female X. birchmanni, X. malinche, or X. variatus. We also collected stimulus water free from any odor cues by following the same procedure described above but without introducing any fish into collecting tanks.
Chemical preference tests
We used a dichotomous choice setup to assess the response of male X. birchmanni to female chemical cues. First, we examined whether males actually respond to the female odor cues collected from conspecifics (X. birchmanni) and heterospecifics (X. malinche, X. variatus) by testing male preference for each female stimulus against a plain water control. Second, we offered males the choice between the female odor of conspecifics and each of the two heterospecifics.
All chemical preference tests were conducted in a thoroughly cleaned aquarium (length x width x height = 75 x 30 x 30 cm) divided lengthwise into three equal sections (left, right, and center) by lines drawn on the sides of the tank with a waterproof marker and filled with 40 l of filtered, aerated water. Each test tank had two stimulus delivery systems, one at either end of the test tank. Each stimulus delivery system consisted of a 20-l glass aquarium containing stimulus water connected to a 12-mm pipette by 2.5-mm silicone tubing. The pipette was attached to the test tank 2 cm above the water surface, creating a perturbation on the surface when water was dripped into the aquarium.
For each trial, a male X. birchmanni (mean SL ± SD = 36.71 ± 3.87 mm) was placed into the test tank and allowed to acclimatize for 30 min. Stimulus flow was then initiated simultaneously, dripping water from both stimulus delivery systems into the tank. Flow was controlled with the use of plastic clamps set at 10 ml/min. We observed focal males behind a screen to minimize disturbance to the fish. The preference test began once the male had passed into both side compartments (left and right) and ran for 10 min. If the male did not visit both compartments within 10 min, the trial was aborted. Association preference for each stimulus in a trial was measured as the time spent by the male in each compartment. Association time is widely used in studies of mate choice in fishes (see Wong, 2004, and references therein) and is the standard measure of mating preferences in poeciliids, including swordtails (Basolo, 1990; Crapon de Caprona and Ryan, 1990; Hankison and Morris, 2002; Kingston et al., 2003; McLennan and Ryan, 1997, 1999; Rosenthal et al., 2002). In a closely related species, Xiphophorus nigrensis, association time in laboratory trials is a strong predictor of association in open-field trials and of observed mate choices in the wild (Ryan et al., 1990, 1992). In our study, proximity to the odor source was often accompanied by flexing of the gonopodium, or intromittent organ, a characteristic sexual display (Gabor and Ryan, 2001; Park and Propper, 2002). In the wild, males observed within 1–2 body lengths of females are nearly always performing courtship displays toward those females (Rosenthal, 2000, personal observations). Association time is thus a robust and meaningful estimate of mating preference.
Visual preference tests
In light of the results obtained for the chemical preference trials (see below), we also decided to test the visual preference of male X. birchmanni for females of their own species versus those of the closely related congener, X. malinche. We followed protocols described in Kingston et al. (2003) and Rosenthal et al. (2002). The experimental setup involved two small aquaria (20 x 12 x 12 cm) placed at opposite ends of a larger aquarium (51 x 28 x 33 cm) housing the test male. A stimulus female X. birchmanni was released randomly into one of the two small aquaria; a size-matched stimulus female X. malinche was released into the other. The use of separate containers allowed fish to see one another but prevented the transfer of any odor cues. Fish were acclimatized for 5 min prior to the start of a trial. During this time, a sheet of white cardboard was inserted between the large aquarium and each of the two smaller aquaria to prevent the fish from seeing and interacting with one another. Just before a trial commenced, the white sheets were gently lifted and the amount of time the male spent associating with each female was recorded over a 5-min period. A male was deemed to be associating with a particular female if he was within 10 cm of her aquarium. After the 5-min recording period, the white sheets were reinserted between the aquaria. The females were then switched between the two small aquaria, and after a second 5-min acclimatization period, association time with each female was remeasured for another 5-min recording period. At the end of the trial, we tallied the total time a male spent associating with a particular female during each of the two 5-min recording periods.
All statistical tests are two tailed, and results are presented as mean ± SE unless indicated otherwise.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Chemical preference tests
Male X. birchmanni were attracted to the cues of female X. birchmanni (Wilcoxon signed-rank test: z = 2.39, n = 15, p = .017; Figure 1a) and X. malinche (Wilcoxon signed-rank test: z = 2.78, n = 15, p = .005; Figure 1b) versus plain water. They did not, however, spend more time with the female X. variatus stimulus over plain water (Wilcoxon signed-rank test: z = 0.568, n = 15, p = .57; Figure 1c).
|
When offered the choice between the female odor cues of conspecifics and heterospecifics, the amount of time that male X. birchmanni spent associating with the conspecific cue depended on which stimulus was offered as the alternative (Mann-Whitney U test: U = 26, n1 = n2 = 15, p < .001). We found that male X. birchmanni preferred the X. malinche stimulus over the odor cues of their own females (Wilcoxon signed-rank test: z = 1.93, n = 15, p = .053; Figure 2a). When given the choice between stimuli from conspecific females and those of X. variatus, however, males strongly preferred odors of their own species (Wilcoxon signed-rank test: z = 2.78, n = 15, p = .005; Figure 2b).
|
Given our results, we considered the possibility that the female X. variatus used to create the stimulus water may have been unresponsive and/or were not releasing any cues. To address this possibility we subsequently offered male X. variatus (mean SL ± SD = 41.2 ± 2.15 mm) the choice between the X. variatus stimulus and water and found that male X. variatus were significantly attracted to the stimulus of their own species (time with X. variatus = 334.2 ± 40.5 s, water = 169.6 ± 39.8 s; Wilcoxon signed-rank test: z = 1.99, n = 10, p = .047). We, therefore, ruled out the possibility that the lack of response of male X. birchmanni to X. variatus had been due to a problem with females used to collect the X. variatus stimulus.
Visual preference tests
Male X. birchmanni did not discriminate between size-matched, sexually mature female X. birchmanni and X. malinche based on visual cues (mean association time ± SE with female X. birchmanni = 257 ± 33 s, X. malinche = 221 ± 29 s; Wilcoxon signed-rank test: z = 0.31, n = 17, p = .76).
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Males have generally been regarded as fairly indiscriminate in their mating preferences. The male X. birchmanni in our study, however, not only discriminated among conspecific and heterospecific odor stimuli but also showed a complex array of preferences that has previously been documented only in females. First, male X. birchmanni differed in their response to the odor cues of different species. Males were attracted to odors from female conspecifics and the closely related, allopatric X. malinche. They did not, however, associate more with the odor cues of the sympatric platyfish, X. variatus, over plain water, suggesting that male X. birchmanni do not recognize X. variatus as potential mates. Second, male preference for conspecifics also varied depending on which heterospecific was offered as an alternative. When given the choice between the conspecific stimulus and that of the platyfish, male X. birchmanni strongly preferred the conspecific odor. However, when offered odor cues of X. malinche, male X. birchmanni actually showed a weak preference for the heterospecific.
Although female preference for heterospecifics is not uncommon, very few studies (if any) have reported mate preference for the cues of another species in males. More typically, studies examining male mate recognition tend to find either a preference for conspecifics or no preference. In Pieris butterflies, for example, males of one species, Pieris occidentalis, discriminated against heterospecific females in favor of conspecifics (Wiernasz, 1995). In contrast, males in another species, Pieris protodice, showed no interspecific mate choice. A similar result was reported for male response to female sex pheromones in two species of gourami, Trichogaster trichopterus and Trichogaster pectoralis (McKinnon and Liley, 1987). It is unclear why male X. birchmanni may be more attracted to X. malinche. Work on female mate recognition in other species suggests that individuals could be drawn to novel traits that are not expressed in their own species (e.g., Basolo, 1995; Ryan and Rand, 1990) or, if expressed, are present in a more intense form in heterospecifics (Pfennig, 2000).
The structure of pheromones in Xiphophorus is unknown. Females in another poeciliid fish, the guppy, Poecilia reticulata, release an ovarian pheromone after parturition (Crow and Liley, 1979). Sex hormones—steroids and prostaglandins—have been implicated as important chemical cues in several fish species (Stacey et al., 2003). Periovulatory females may sequentially release a preovulatory steroid pheromone and/or a postovulatory prostaglandin pheromone that can dramatically affect male behavior and physiology. In goldfish, Poling et al. (2001) found that the three steroid components of the female preovulatory pheromone each had distinct effects on male behavior. In several poeciliid species, females advertise their fertility through odor cues (Park and Propper, 2002; Sumner et al., 1994). Males, in turn, may be selected to discriminate among females based on these cues. The weak preference of X. birchmanni males for X. malinche odors, however, suggests that a species-typical component of the X. birchmanni odor cue is not necessary to provoke a male sexual response. In order to explain this rather counterintuitive result, we need to characterize the olfactory cue in these fishes.
Regardless of which cues may be involved, a preference for the heterospecific stimulus has important consequences. The result of our visual preference trials suggests that male X. birchmanni do not discriminate between X. birchmanni and X. malinche based on visual cues. If they rely, instead, on chemical cues, it is possible that their preferences could mediate hybridization with X. malinche. This would, of course, depend on whether female X. malinche are permissive. Although female mate recognition in X. malinche has not yet been tested, it is interesting to note that both species often hybridize in nature when they occur in sympatry (Rosenthal et al., 2003).
The degree of any geographic overlap between species may play an important role in the evolution of male preference for conspecific females. Specifically, selection may favor divergence of mate recognition systems in areas of sympatry between congeners if there is a high enough fitness cost to individuals who mate with heterospecifics (Pfennig, 2000). This, in turn, may cause individuals to discriminate more strongly in favor of conspecifics (or against the heterospecific) when offered a closely related but sympatric heterospecific as a prospective suitor. For example, male sailfin mollies, Poecilia latipinna, discriminated less strongly against females of the gynogenetic Poecilia formosa as the geographic distance from sympatric populations increased (Gabor and Ryan, 2001). In our study, we used a population of X. birchmanni that was allopatric with X. malinche but sympatric with X. variatus. A preference for X. birchmanni may therefore be unsurprising when the alternative is the odor cues of sympatric X. variatus (Gabor and Ryan, 2001; McKinnon and Liley, 1987). Future studies could, perhaps, explore male responses using females from populations of X. malinche and X. variatus that are both sympatric and allopatric with X. birchmanni.
Phylogenetic relationships may also play an important role in the evolution of species recognition. In a study examining the response of Streptopelia doves to interspecific vocalizations, de Kort and ten Cate (2001) found that females were more responsive to the calls of closely related heterospecifics. Similarly, in swordtails, McLennan and Ryan (1999) showed that females of two closely related species, Xiphophorus cortezi and X. nigrensis, were more strongly attracted to the olfactory cues of each other than they were to the cue of a more distantly related species, Xiphophorus montezumae. Our results suggest a similar pattern of species recognition in males. There are, at present, several alternative hypotheses concerning the phylogenetic relationship of swordtail fishes. In the context of our study, however, one thing is uncontroversial: all phylogenetic hypotheses agree that X. birchmanni and X. malinche are more closely related to one another than either are to the platyfish, X. variatus (reviewed in Morris et al., 2001). Notwithstanding the possible effects of geographic overlap, phylogenetic distance could thus provide another plausible explanation for why X. birchmanni shows a strong preference for conspecifics when offered X. variatus. It cannot, however, explain why X. birchmanni males show a preference for the scent of a heterospecific. All other things being equal, we might expect males to have the greatest difficulty when distinguishing between conspecific odor and the scent of females from their sister species (i.e., show "no choice"). A preference for the heterospecific is, however, unexpected.
Male mate choice, though little studied, is no less important than female choice. Although females are typically regarded as the choosier sex, we now know that males can also be choosy (Gowaty et al., 2003). This relatively recent revelation can have important evolutionary implications. Within a given system, it is possible for members of one or both sexes to be attracted to conspecifics, show no species preference, or even prefer heterospecifics (Wong et al., 2004). The match or mismatch between male and female preference patterns could have important evolutionary consequences. Lande et al. (2001) argued, for example, that mutual male and female mate choice could lead to rapid sympatric speciation by sexual selection. Sexual asymmetry in mate choice, meanwhile, can lead to sex-biased asymmetry in hybridization with heterospecifics (Wirtz, 1999). Finally, preference asymmetries between the sexes can yield opposing effects of sexual selection on traits that are genetically correlated between the sexes (Wiernasz, 1995). Theoretical and empirical studies of mate choice should thus consider the role of both male and female preferences in structuring evolutionary outcomes.
|
ACKNOWLEDGEMENTS |
|---|
We thank F.J. García de León, R. Struminger, J. Tovar Ortiz, and the Lara family for assistance in the field and D.G. Chapple, S. Downes, D. McLennan, L. Rowe, J. Stapley, M. Zuk, and anonymous reviewers for comments on the manuscript. We also thank the Government of Mexico for permission to collect fish. Finally, we thank C. O'Keefe, Z. Khalifa, and C. Schacter for assistance in the laboratory. B.B.M.W. is supported by a Sir Keith Murdoch Fellowship and H.S.F. by a Palmer McLeod Fellowship.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Basolo AL, 1990. Female preference predates the evolution of the sword in swordtail fish. Science 250:808–810.
Basolo AL, 1995. Phylogenetic evidence for the role of a pre-existing bias in sexual selection. Proc R Soc Lond B 259:307–311.[Medline]
Cardwell JR, Dulka JG, Stacey NE, 1992. Acute olfactory sensitivity to prostaglandins but not to gonadal steroids in two species of Catostomus (Pisces: Cypriniformes). Can J Zool 70:1897–1903.
Crapon de Caprona MD, Ryan MJ, 1990. Conspecific mate recognition in swordtails, Xiphophorus nigrensis and X. pygmaeus: olfactory and visual cues. Anim Behav 39:290–296.[CrossRef]
Crow RT, Liley NR, 1979. Sexual pheromone in the guppy, Poecilia reticulata (Peters). Can J Zool 57:184–188.
de Kort SR, ten Cate C, 2001. Response to interspecific vocalisations is affected by degree of phylogenetic relatedness in Streptopelia doves. Anim Behav 61:239–247.[CrossRef][Web of Science][Medline]
Gabor CR, Ryan MJ, 2001. Geographical variation in reproductive character displacement in mate choice by male sailfin mollies. Proc R Soc Lond B 268:1063–1070.[Medline]
Gowaty PA, Steinichen R, Anderson WW, 2003. Indiscriminate females and choosy males: within- and between-species variation in Drosophila. Evolution 57:2037–2045.[CrossRef][Web of Science][Medline]
Hankison SJ, Morris MR, 2002. Sexual selection and species recognition in the pygmy swordtail, Xiphophorus pygmaeus: conflicting preferences. Behav Ecol Sociobiol 51:140–145.[CrossRef]
Kingston J, Rosenthal GG, Ryan MJ, 2003. The role of sexual selection in maintaining a colour polymorphism in the pygmy swordtail Xiphophorus pygmaeus. Anim Behav 65:735–743.[CrossRef]
Lande R, Seehausen O, van Alphen JJM, 2001. Mechanisms of rapid sympatric speciation by sex reversal and sexual selection in cichlid fish. Genetica 112:435–443.
Magurran AE, 1998. Population differentiation without speciation. Philos Trans R Soc Lond B 353:275–286.[CrossRef]
McKinnon JS, Liley NR, 1987. Asymmetric species specificity in response to female sexual pheromone by males of two species of Trichogaster (Pisces: Belontiidae). Can J Zool 65:1129–1134.
McLennan DA, 2005. Male brook sticklebacks' (Culaea inconstans) response to olfactory cues. Behaviour (in press).
McLennan DA, Ryan MJ, 1997. Responses to conspecific and heterospecific olfactory cues in the swordtail Xiphophorus cortezi. Anim Behav 54:1077–1088.[CrossRef][Web of Science][Medline]
McLennan DA, Ryan MJ, 1999. Interspecific recognition and discrimination based upon olfactory cues in swordtails. Evolution 53:880–888.[CrossRef]
Morris MR, De Queiroz K, Calhoun SW, Morizot DC, 2001. Phylogenetic relationships among the northern swordtails (Xiphophorus) as inferred from allozyme data. Copeia 2001:65–81.
Murray DL, Jenkins CL, 1999. Perceived predation risk as a function of predator dietary cues in terrestrial salamanders. Anim Behav 57:33–39.[CrossRef][Web of Science][Medline]
Park D, Propper CR, 2002. Pheromones from female mosquitofish at different stages of reproduction differentially affect male sexual activity. Copeia 2002:1113–1117.[CrossRef]
Pfennig KS, 2000. Female spadefoot toads compromise on mate quality to ensure conspecific matings. Behav Ecol 11:220–227.
Poling KR, Fraser EJ, Sorensen PW, 2001. The three steroidal components of the goldfish preovulatory pheromone signal evoke different behaviors in males. Comp Biochem Physiol B 129:645–651.[CrossRef][Medline]
Rauchenberger M, Kallman KD, Morizot DC, 1990. Monophyly and geography of the Rio Panuco Basin swordtails (Genus Xiphophorus) with descriptions of four new species. Am Mus Novit 2975:1–41.
Rosenthal GG, de la Rosa Reyna XF, Kazianis S, Stephens MJ, Morizot DC, Ryan MJ, Garcia de Leon FL, 2003. Dissolution of sexual signal complexes in a hybrid zone between the swordtails Xiphophorus birchmanni and Xiphophorus malinche (Poeciliidae). Copeia 2003:299–307.[CrossRef]
Rosenthal GG, Wagner WE Jr, Ryan MJ, 2002. Secondary loss of preference for swords in the pygmy swordtail Xiphophorus nigrensis (Pisces: Poeciliidae). Anim Behav 63:37–45.[CrossRef]
Ryan MJ, Fox JH, Wilczynski W, Rand AS, 1990. Sexual selection for sensory exploitation in the frog Physalaemus pustulosus. Nature 343:66–67.[CrossRef][Medline]
Ryan MJ, Rand AS, 1990. The sensory basis of sexual selection for complex calls in the tungara frog, Physalaemus pustulosus (sexual selection for sensory exploitation). Evolution 44:305–314.[CrossRef][Web of Science]
Ryan MJ, Wagner WE Jr, 1987. Asymmetries in mating preferences between species: female swordtails prefer heterospecific males. Science 236:595.
Stacey N, Chojnacki A, Narayanan A, Cole C, Murphy C, 2003. Hormonally derived sex pheromones in fish: exogenous cues and signals from gonad to brain. Can J Physiol Pharm 81:329–341.[CrossRef][Web of Science][Medline]
Sumner T, Travis J, Johnson CD, 1994. Methods of fertility advertisement and variation among males in responsiveness in the sailfin molly (Poecilia latipinna). Copeia 1994:27–34.
Wiernasz DC, 1995. Male choice on the basis of female melanin pattern in Pieris butterflies. Anim Behav 49:45–51.[CrossRef]
Wirtz P, 1999. Mother species - father species: unidirectional hybridization in animals with female choice. Anim Behav 58:1–12.[CrossRef][Web of Science][Medline]
Wong BBM, 2004. Superior fighters make mediocre fathers in the Pacific blue-eye fish. Anim Behav 67:583–590.[CrossRef]
Wong BBM, Candolin U, in press. How is female mate choice affected by male competition? Biol Rev.
Wong BBM, Jennions MD, 2003. Costs influence male mate choice in a freshwater fish. Proc R Soc Lond B (Suppl) Biol Lett 270:s36–s38.
Wong BBM, Keogh JS, Jennions MD, 2004. Mate recognition in a freshwater fish: geographical distance, genetic differentiation, and variation in female preference for local over foreign males. J Evol Biol 17:701–708.[CrossRef][Web of Science][Medline]
Wyatt TD, 2003. Pheromones and animal behavior. Cambridge: Cambridge University Press.
Yambe H, Yamazaki F, 2001. Species-specific releaser effect of urine from ovulated femal masu salmon and rainbow trout. J Fish Biol 59:1455–1464.[CrossRef]
Hankison SJ, Morris MR, 2003. Avoiding a compromise between sexual selection and species recognition: female swordtail fish assess multiple species-specific cues. Behav Ecol 14:282–287.
Rosenthal GG, 2000. Design considerations and techniques for constructing video stimuli. Acta Ethol 3:49–54.[CrossRef]
Ryan MJ, Pease CM, Morris MR, 1992. A genetic polymorphism in the swordtail Xiphophorus nigrensis: testing the prediction of equal fitnesses. Am Nat 139:21–31.[CrossRef][Web of Science]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  B. B. M. Wong and M. McCarthy Prudent male mate choice under perceived sperm competition risk in the eastern mosquito fish Behav. Ecol., March 1, 2009; 20(2): 278 - 282. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. U. Heubel and I. Schlupp Seasonal plasticity in male mating preferences in sailfin mollies Behav. Ecol., November 1, 2008; 19(6): 1080 - 1086. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. R. Gabor and A. S. Aspbury Non-repeatable mate choice by male sailfin mollies, Poecilia latipinna, in a unisexual-bisexual mating complex Behav. Ecol., July 1, 2008; 19(4): 871 - 878. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. S Fisher and G. G Rosenthal Male swordtails court with an audience in mind Biol Lett, February 22, 2007; 3(1): 5 - 7. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. S. Fisher and G. G. Rosenthal Hungry females show stronger mating preferences Behav. Ecol., November 1, 2006; 17(6): 979 - 981. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||