Species recognition by male swordtails via chemical cues

Bob B.M. Wong 0 1 2 3 4 Heidi S. Fisher 0 1 4 Gil G. Rosenthal 0 1 4 0 The Author 2005. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions , please 1 helsinki.fi. Received 1 October 2004; revised 18 March 2005; accepted 21 April 2005 2 School of Botany and Zoology, Australian National University , Canberra ACT 0200 , Australia 3 Department of Biological and Environmental Sciences , P.O. Box 65, 00014 , University of Helsinki , Finland 4 Department of Biology, Boston University , 5 Cummington Street, Boston, MA 02215 , USA 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. [Behav Ecol 16:818-822 (2005)] - Pindividuals to recognize their mates. While the mating remating reproductive isolation hinges on the ability of 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 Ro Panuco 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 Animal collection and housing Xiphophorus birchmanni and X. variatus were collected from the Rio Garces, San Luis Potos, Mexico (Rauchenberger et al., 1990). Xiphophorus malinche were collected from the type locality in the Ro 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 collec (...truncated)