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Female bias for enlarged male body and dorsal fins in Xiphophorus variatus
Behavioural Processes 87 (2011) 197–202
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Behavioural Processes journal homepage: www.elsevier.com/locate/behavproc
Female bias for enlarged male body and dorsal fins in Xiphophorus variatus R. David MacLaren a,∗ , John Gagnon b , Ran He c a
Merrimack College, Department of Biology, Mendel Center, North Andover, MA 01845, USA Immune Disease Institute, 100 Longwood Ave., Boston, MA 02115, USA c University of Illinois at Urbana-Champaign, Champaign, IL 61820, USA b
a r t i c l e
i n f o
Article history: Received 3 November 2010 Received in revised form 22 March 2011 Accepted 23 March 2011 Keywords: Female preference Poecilidae Sensory bias Sexual selection Xiphophorus variatus
a b s t r a c t Female preference for male fin elaborations in Poeciliid fishes may be driven by a sensory bias for increased lateral projection area (LPA) that has existed since the lineages diverged from a common ancestor. Previous research supports this hypothesis demonstrating female Poecilia latipinna, Poecilia mexicana, and Poecilia reticulata prefer males of larger body and dorsal fin size, but exhibit no such preferences when controlling for total LPA. In the current study, we further tested this hypothesis by presenting female platys, Xiphophorus variatus, with pairs of dummy males differing in: (1) body size (holding dorsal fin size constant); (2) dorsal fin size (holding body size constant); and (3) dorsal fin: body size ratio (holding total LPA constant). Females spent more time near dummies of greater body and dorsal fin size; however, in the third experiment, neither fin size, body size, nor any particular dorsal fin + body size combination was preferred. These results provide additional support for the LPA and sensory bias hypotheses, demonstrating that female X. variatus not only prefer males with “swords”, but sailfin-like dorsal fins as well when body size is held constant. Shared preference for increased LPA is consistent with common ancestry of the sensory/neural systems in females of all four species. © 2011 Elsevier B.V. All rights reserved.
1. Introduction Females may develop perceptual biases in mate preferences due to a sensory bias in their nervous systems formed by natural selection, sexual selection, or pleiotropic effects (Kirkpatrick and Ryan, 1991; Endler, 1992). Such biases may reflect ecological constraints (Proctor, 1991; Endler, 1992) or basic properties of nervous systems (Ryan and Keddy-Hector, 1992; Rosenthal and Evans, 1998; MacLaren, 2006). Regardless of the bias origin, females are preferentially attracted to males that stimulate their sensory systems more than other males. If a male sends a novel signal which taps into a latent bias, these males are preferred as mates. Thus, a preexisting bias may affect the nature and direction of sexual selection when a new trait arises (Basolo, 1995a). Support for the preexisting bias hypothesis requires evidence that the female preference evolved within the species’ lineage prior to the evolution of the male trait that exploits the preference (Basolo, 1990a). The role of preexisting biases on female preference for male traits has been well studied in certain species of livebearing fishes (Poecilidae). For example, males of some species of the genus Xiphophorus possess an elongation of certain ventral caudal fin rays (the sword) that even females of related but unsworded
∗ Corresponding author. Tel.: +1 9788373543. E-mail address: [email protected] (R.D. MacLaren). 0376-6357/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.beproc.2011.03.006
species find attractive (e.g. X. maculatus; Basolo, 1990b, Xiphophorus variatus; Basolo, 1995b, Priapella olmecae; Basolo, 1995a). Phylogenetic information and mate choice tests suggest that female preference for swords arose before the Xiphophorus-Priapella clade diverged, pre-dating the evolution of the sword within Xiphophorus (Basolo, 1996). Species within the subgenus Poecilia (mollies) provide additional evidence of female bias for male fin elaborations. Male sailfin mollies (Poecilia latipinna) have an enlarged dorsal fin (sailfin) that is presented to females in courtship (Ptacek and Travis, 1996). Female P. latipinna as well as Poecilia mexicana (a species whose males do not naturally possess the sailfin phenotype) prefer to associate and mate with males of larger dorsal fin (MacLaren et al., 2004; MacLaren and Rowland, 2006; Jordan et al., 2006) and body size (Ptacek and Travis, 1997; MacLaren et al., 2004; MacLaren and Rowland, 2006). As with the sword ornament of Xiphophorus, phylogenetic information (Ptacek and Breden, 1998; Breden et al., 1999) suggests that female preference for enlarged dorsal fins arose before the monophyletic sailfin clade diverged from a shortfin ancestor, pre-dating the evolution of the sailfin trait within the subgenus Poecilia. Additionally, males of numerous guppy populations (Poecilia reticulata) show polymorphism in dorsal and caudal fin length including homoplastic “swords”, elongated tails and enlarged dorsal fins (Houde, 1997; Brooks and Endler, 2001; Karino and Matsunaga, 2002; MacLaren et al., submitted for publication)
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that along with body size (Endler and Houde, 1995; Karino and Matsunaga, 2002; MacLaren et al., unpublished data) offer a selective advantage in female mate choice in at least some populations (Bischoff et al., 1985; Endler and Houde, 1995; MacLaren et al., submitted for publication). These elongated caudal and dorsal fins, among other poeciliid fin elaborations may have originated from a shared female preference for larger apparent size in males, a preference that is common in many species (Andersson, 1994) and widespread among the Poecilidae (Ryan, 1998). Because a larger male projects a larger image onto the female’s retina at a given viewing distance (O’Brien et al., 1976, 1985; Rowland, 1989a,b), this could elicit a stronger sexual response (MacLaren, 2006). Fin elaborations may therefore have evolved as a way for males to increase their apparent size or lateral projection area (LPA) and consequent attractiveness to females (Haines and Gould, 1994; Rosenthal and Evans, 1998; Karino and Matsunaga, 2002; MacLaren et al., 2004). If females respond primarily to greater LPA rather than increased body or fin size per se, then female preference should be proportional to the male’s total LPA (body + fin area) regardless of his fin: body size ratio (MacLaren et al., 2004). The LPA hypothesis predicts that females: (1) prefer males of larger body and fin size; (2) show no preference between two males whose total LPAs (fin + body surface areas) are equal (i.e. increases in fin surface area compensate for decreases in body surface area and vice versa); and (3) show no preference for males with the fin elaboration over a finless male of equivalent LPA. Preference experiments with P. latipinna (MacLaren et al., 2004), P. mexicana (MacLaren and Rowland, 2006), and P. reticulata (MacLaren et al., submitted for publication) support all three of the predictions above. In this study we further test the LPA hypotheses by examining female preferences for male body size, dorsal fin size, and dorsal fin: body size ratio in X. variatus—a series of experiments similar to those previously conducted with P. latipinna, P. mexicana, and P. reticulata. Moreover, we want to know whether this preference stems from a preexisting bias. Female preference for increased male LPA not only in the subgenera Poecilia (“mollies”) and Lebistes (“guppies”) but the more distantly related genus Xiphophorus would support the preexisting bias hypothesis, demonstrating that female X. variatus (a species sexually monomorphic with respect to fin morphology) not only prefer males with artificial “sword” ornaments (Basolo, 1995b) but supernormal size dorsal fins and perhaps other forms of size manipulation that increase male LPA (Haines and Gould, 1994). A shared preference for sailfin-like dorsal fins and/or increased LPA would be consistent with common ancestry of the sensory/neural systems in females of P. latipinna, P. mexicana, P. reticulata, and X. variatus. 2. Methods 2.1. Subjects Test subjects were X. variatus, Zarco collected from the Arroyo Zarco locality west of Encino, Tamaulipas, Mexico (locale described by Borowsky (1984); stock source: Dr. Steve Kazianis, New York University, 6th of September 1996). The fish were shipped to the laboratory at Merrimack College from the Xiphophorus Genetic Stock Center, Texas State University, San Marcos, TX in the fall of 2008, placed in 378-l and 70-l mixed-sex stock tanks (water temperature 23–25 ◦ C; 16 h light:8 h dark cycle) and fed TetraMin fish flakes two times daily. We removed females from stock tanks at random and placed them in 70-l all-female subject tanks for a minimum of two months prior to testing. Females were then transferred to separate 8.75-l isolation tanks (30 cm × 15 cm × 20 cm) for approximately 48 h before becoming eligible for use as subjects. Each female was subjected to one of three experiments: body size
preference (expt I), dorsal fin preference (expt II), and fin: body size ratio preference (expt III). All three experiments were run concurrently between December 2008 and May 2010 as time permitted. All fish were kept in the laboratory under similar conditions for the same amount of time throughout the testing period. 2.2. Dummy construction In order to control for variation in male behavior among other traits, we used dummy males as stimuli, varying one trait (body size in expt I, dorsal fin size in expt II, and dorsal fin: body size ratio in expt III) while holding all other traits constant. The use of dummies allowed us to modify each variable independently while compromising little in the way of visual detail (Rowland, 1999). The dummies were produced as described in MacLaren et al. (2004). The Constant Fin Size Series for expt I consisted of three images measuring 35, 45 and 55 mm from the anterior tip of the fish to the end of the caudal fin, with proportional increases in the sizes of all fins except the dorsal, which was held constant at 12.5 mm in length (approximating the average dorsal fin size of mature males in our laboratory population, unpublished data). The Constant Body Size Series for expt II consisted of three images all measuring 45 mm from the anterior tip of the fish to the end of the caudal fin (approximating the average total length of mature males in our laboratory population, unpublished data) with dorsal fins measuring 12.5, 17.5 and 22.5 mm in length and proportional changes in fin allometry (i.e. no changes in fin shape). The Constant Body Ratio Series for expt III consisted of five dummies that differed in dorsal fin: body size ratio. The dummies included a male with no dorsal fin, and males with 0.28, 0.55, 0.83, and 1.11 cm2 fins with compensatory decreases in body area to ensure that all five maintained a constant LPA of 5.06 cm2 . This constant was determined by calculating the composite LPA of a male of average dorsal fin and body size from our study population (unpublished data). Thus, the dummies for expt III were designed such that the difference in body LPA between males in all 10 paired combinations of the five stimuli were equal to their difference in dorsal fin LPA. The dummies were identified as ‘small’ (S), ‘intermediate’ (I) and ‘large’ (L) in experiments I and II, in correspondence with their dorsal fin size/total lengths. For the fin: body ratio series (expt III), each dummy within a series was assigned a ranking from “1” to “5” in relation to its body LPA, from smallest (1) to largest (5) (Fig. 1). 2.3. Testing apparatus and procedure The testing environment consisted of three 17.5-l aquaria (50 cm × 26 cm × 13.5 cm each) lined up end to end using an apparatus and protocol identical to that used in previous mate preference experiments with Xiphophorus helleri (MacLaren and Daniska, 2008) and P. reticulata (MacLaren et al., submitted for publication). Female subjects were placed in an aquarium that was divided into three zones by two black vertical lines drawn on the front wall: a 30 cm × 26 cm × 13.5 cm ‘neutral zone’ flanked on each side by a 10 cm × 26 cm × 13.5 cm ‘preference zone’. A pair of aquaria flanking the female’s tank each housed an adjustable motorized belt and pulley system to which the dummy stimuli were attached (see MacLaren and Daniska, 2008 for further details). Each subject (expt I: n = 23; expt II: n = 22; and expt III: n = 22) was introduced into the center aquarium and allowed to acclimate for 15 min. Opaque screens blocking the female’s view of the dummies were then removed and the apparatus was turned on so that the dummies began to move. Using a Canon ZR930 digital video recorder, the female’s behavior was recorded for 5 min. The dummies were then switched to opposite sides of the arena for another 5 min of observation for a total of 10 min of testing per treatment. The subject was left undisturbed for 5 min before proceeding to the
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Fig. 1. Dummy males varying in body size, dorsal fin size, and dorsal fin-to-body size ratio used in expts. I, II, and III, respectively. Dummy letter designations S, I, and L (top left margin) correspond to the small, intermediate, and large body and fin size variants for experiments I and II. Dummy number designations 1–5 (bottom left margin) correspond to dorsal fin: body size variants from smallest (1) to largest (5) body size used in expt III.
next treatment of the series. For experiments I and II, all three possible paired combinations of the three dummies (dummy ‘L’ paired with dummy ‘S’, ‘L’ with ‘I’, and ‘S’ with ‘I’) were presented in random order to each female in a single day. In expt. III, all 10 paired combinations of the five dummies were presented in random order to each female over a period of two days; five of the 10 paired combinations on each day of testing (MacLaren and Daniska, 2008). No female was subjected to more than one set of treatments (i.e. one experiment).
2.4. Behavioral measures and statistical analyses As in previous experiments of this kind (MacLaren et al., 2004, submitted for publication; MacLaren and Rowland, 2006; MacLaren and Daniska, 2008), we played back all video data in real time to determine the total time each female spent in each preference zone as well as time spent in the neutral zone per 10-min treatment. Paired samples t-tests were used to compare the total time females spent in association with dummy A vs. dummy B in each treatment (e.g. L vs. S treatment of expt I). Female strength of preference was defined as time spent with dummy A − time with dummy B per 10 min treatment. Because each female received three treatments in experiments I and II, and ten treatments in expt III, all significance levels were adjusted to P < 0.017 and P < 0.005, respectively (Bonferroni procedure; Sokal and Rohlf, 1981). All probabilities given are two-tailed. In order to make easier inters-study comparisons, we used Cohen’s d to calculate the effect size (with 95% confidence interval) related to the preference strength for each treatment in all three experiments (Nakagawa and Cuthill, 2007). We conducted all statistical tests using the statistical program Sigmastat Ver. 11.2 (Systat Software, Point Richmond, CA, USA) with the exception of effect size calculations, which were made using software by David B. Wilson available online at http://mason.gmu.edu/∼dwilsonb/ma.html.
3. Results The female behaviors observed during both experiments included unison swimming, circling, and backing toward the male, all of which are activities attributed to mating behavior in the literature for poeciliids (Farr, 1989; Houde, 1997; Basolo, 2002a). There were no significant effects of dummy presentation order on female strength of preference in any of the three experiments (expt I: oneway repeated measures ANOVA, df = 2, F = 0.327, P = 0.723; expt II: one-way repeated measures ANOVA, df = 2, F = 0.186, P = 0.831; expt III: one-way repeated measures ANOVA; df = 9, F = 0.982, P = 0.456). Additionally, female total length (±SE) did not differ across experiments (expt I: 35.4 ± 0.05 mm, max = 4.10, min = 3.10; expt II: 36.0 ± 0.06 mm, max = 4.10, min = 3.00; expt III: 36.3 ± 0.06 mm, max = 4.20, min = 3.10; df = 2, F = 0.659, P = 0.521). Moreover, we found no evidence of female size differentially affecting female preference across treatments within any of the three experiments given that: (1) all subjects received all treatments within an experiment and (2) one-way repeated measures ANOVAs revealed no effect of female total length on strength of preference in any of the three treatments of experiments I (n = 23) and II (n = 22), nor in any of the ten treatments of expt III (n = 22). Paired samples t-tests comparing the total time females (n = 23) spent with the larger- vs. smaller-bodied male dummy and associated reports of the effect size (Cohen’s d with 95% confidence interval) in experiment I revealed that females spent significantly more time with the larger bodied of the paired males in each of the three treatments (P < 0.017; Table 1 and Fig. 2). Similarly, paired samples t-tests and associated Cohen’s d calculations comparing the total time females (n = 22) spent with the larger- vs. smaller-finned male in experiment II revealed a preference for the larger-finned dummy in all three treatments (P < 0.017; Table 1 and Fig. 2). However, paired samples t-tests comparing total time females (n = 22) spent in association with the larger-bodied, smaller-finned
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Fig. 2. Results from expt I, II, and III. (a) Expt I: The average amount of time (s) females (n = 23) spent in association with the smaller vs. larger of two dummy males in each of three 10 min treatments (dummy I vs. S, L vs. S, and L vs. I). (b) Expt II: The average amount of time (s) females (n = 22) spent in association with the smaller vs. larger of two dummy males in each of three 10 min treatments. (c) Expt III: The average amount of time (s) females (n = 22) spent in association with the smaller-bodied, larger-finned vs. larger-bodied, smaller-finned of two dummy males in each of ten 10 min treatments. * indicates Bonferroni corrected significant preference (paired samples t-tests; P < 0.017) for the larger of the paired males.
male vs. the smaller-bodied, larger-finned male in experiment III revealed no significant preferences in any of the 10 treatments (P > 0.005; Table 2 and Fig. 2). Thus, females did not exhibit a preference for any particular male across treatments in experiment III, including the dummy that best approximated the fin: body ratio of a typical X. variatus male (dummy no. 3; Fig. 1). Furthermore, in none of the four treatments that involved dummy no. 5 (a male lacking a dorsal fin; Fig. 1) did females prefer to associate with the alternative dummy that possessed a dorsal fin.
4. Discussion As demonstrated in similar studies with P. latipinna, P. mexicana, and P. reticulata, the preferences of female X. variatus satisfy all three predictions of the LPA hypothesis, suggesting that increased dorsal fin size can compensate for decreased body size and vice versa, and that preference is for male LPA rather than for dorsal fin and body size per se. Haines and Gould (1994) explored the basis of female preference for a male fin elaboration – the sword – in X.
R.D. MacLaren et al. / Behavioural Processes 87 (2011) 197–202 Table 1 Results from experiments I and II (female preference for male body and dorsal fin size, respectively): mean female strength of preference (SOP) (i.e. time spent in association with the larger male–time with the smaller male per 10 min test period) in each of three treatments of expt I (n = 23) and expt II (n = 22). Results of paired samples t-tests comparing total time (s) females spent in association with the larger vs. smaller male in each treatment and associated Cohen’s d calculations of the effect size (with 95% confidence interval) related to preference strength (Nakagawa and Cuthill, 2007). Treatment
Mean SOP (s)
t-value
p-value
Cohen’s d (95% C.I.)
Experiment I: preference for male body size (fin size control series) I vs. S 114.4 ± 35.7 3.20 0.004 1.147 (0.523–1.771) L vs. S 116.9 ± 28.1 4.16 < 0.001 1.253 (0.621–1.885) L vs. I 109.2 ± 36.9 2.96 0.007 0.923 (0.319–1.54) Experiment II: Preference for male dorsal fin size (body size control series) I vs. S 104.4 ± 36.0 2.90 0.009 0.958 (0.334–1.582) L vs. S 134.0 ± 29.7 4.51 <0.001 1.512 (0.842–2.182) L vs. I 97.3 ± 36.6 2.65 0.015 0.9561 (0.3323–1.58)
variatus and came to a similar conclusion, suggesting that the general feature females are responding to is total length as measured along the male’s ventral surface rather than sword or tail length per se. Females in the current study, however, did not base their preferences on total length alone. If they had, we would expect females to prefer the larger-bodied, smaller-finned dummies in experiment III, which did not occur. Still, the results of both studies suggest that female preference in platys may be for males of larger apparent size (Rosenthal and Evans, 1998). Preference for male dorsal fin size/LPA may be favored by females either through greater stimulation of the female sensory system and brain or due to an adaptive reason (Rowland, 1989a; Ryan and Keddy-Hector, 1992). The greater response of perceptual systems to increased stimulation often leads animals to prefer larger, brighter, or more vigorous mates, particularly in species where mate choice is mediated by visual cues (Rowland, 1989a; Kirkpatrick and Ryan, 1991). Increased body height in the form of a dorsal fin and/or body length in the form of an elongated tail are factors that enlarge the area of the retina swept by male images during courtship (Endler and Houde, 1995; MacLaren, 2006), perhaps favoring the evolution of such traits in males. Once established, the apparent size/LPA preference will be maintained through the female preexisting bias as well as Fisherian coevolution (Fisher, 1930). Additionally, female preference for larger male fin and/or body size may be adaptive in populations where size confers an advantage in intrasexual competition for resources and/or mating opportunities as observed in numerous poeciliids including X. variatus (Bisazza et al., 1996), among other heritable fitness Table 2 Results from experiment III (female preference for male dorsal fin: body size ratio): mean female strength of preference (SOP) (i.e. time spent in association with the larger-bodied, smaller-finned male-time with the smaller-bodied, larger-finned male per 10 min test period) in each of 10 treatments (n = 22). Results of paired samples t-tests comparing total time (s) females spent in association with the larger-finned, smaller bodied vs. smaller-finned, larger-bodied dummy male in each treatment and associated Cohen’s d calculations of the effect size (with 95% confidence interval) related to preference strength (Nakagawa and Cuthill, 2007). Treatment
Mean SOP (s)
1 vs. 2 1 vs. 3 1 vs. 4 1 vs. 5 2 vs. 3 2 vs. 4 2 vs. 5 3 vs. 4 3 vs. 5 4 vs. 5
35.3 −44.2 87.9 36.3 −26.8 35.2 25.4 −10.5 −40.0 7.1
± ± ± ± ± ± ± ± ± ±
22.4 27.4 44.2 47.6 36.1 38.4 39.7 23.6 36.0 30.7
t-value
p-value
Cohen’s d (95% C.I.)
1.57 −1.61 1.99 0.76 −0.74 0.92 0.64 −0.45 −1.11 0.23
0.130 0.122 0.060 0.455 0.466 0.370 0.530 0.660 0.280 0.820
0.412 (−0.185 to 1.010) − 0.444 (−1.043 to 0.154) 0.742 (0.131 to 1.353) 0.276 (−0.318 to 0.869) −0.257 (−0.851 to 0.336) 0.327 (−0.268 to 0.922) 0.225 (−0.368 to 0.818) −0.188 (−0.709 to 0.474) −0.392 (−0.989 to 0.204) 0.072 (−0.519 to 0.663)
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benefits correlated with male size (reviewed in MacLaren et al., 2004; MacLaren and Rowland, 2006). Alternatively, such a preference may be a correlated response to selection on male choice of larger, more fecund females (Ptacek and Travis, 1997; Gabor, 1999; Herdman et al., 2004; Dosen and Montgomerie, 2004). From the males’ prospective, if greater LPA increases attractiveness to females and improves reproductive success, then selection should favor male allocation of energy to body parts such as dorsal and caudal growth that maximize total LPA. This, however, assumes that females have opportunities to choose amongst males and that the costs of trait expression (e.g. increased predation or decreased swimming performance) do not exceed the mating benefits. Violation of either or both assumptions, along with genetic/developmental constraints, may explain the traits’ absence in male X. variatus. There is morphological and ontogenetic evidence that the swords and sailfin-like fins found in Xiphophorus, sailfins in mollies, and sword- and sailfin-like fins observed in certain populations of P. reticulata, have separate evolutionary origins (Rauchenberger et al., 1990; Basolo, 1996; Breden et al., 1999) and thus resemble one another as a result of parallel evolution (Basolo, 1995a). The common selective force behind such convergence may be female bias for males of larger apparent size or LPA. Just as the same initial bias may select different traits in different lineages (e.g. a sword vs. a sailfin) depending on the chance appearance of new variation, an initial bias could select for similar traits in different lineages (e.g. the independent evolution of swords in Xiphophorus and some guppy populations; Basolo, 1995a). There are however, several studies of female preference in poeciliid fishes that, although not designed to test LPA, produced results inconsistent with our hypothesis. Some mate preference experiments, for example, have demonstrated female discrimination against male fin elaborations (Basolo, 2002b; Rosenthal et al., 2002; Witte and Klink, 2005; Wong and Rosenthal, 2006; Fisher and Rosenthal, 2007; MacLaren and Daniska, 2008). Perhaps preference for male LPA and/or fin elaborations is an ancestral trait within the poeciliid family that has been secondarily lost or altered in some populations as a result of genetic drift (Rosenthal et al., 2002) or for some adaptive reason (e.g. caused females to mate at a suboptimal rate, mate with inferior males, or risk mating with heterospecifics; Pfennig, 2000; Hankison and Morris, 2002; Basolo, 2002b; Witte and Klink, 2005). Alternatively, the LPA bias may have evolved independently in the poeciliid species examined. This could suggest parallel evolution of the preference as hypothesized for male fin elaborations above. Shared preference for increased LPA is consistent with common ancestry of the sensory/neural systems in P. latipinna, P. mexicana, P. reticulata, and X. variatus females providing support for the single origin/secondary loss hypothesis. However, the same logic could be used to explain multiple gains of preference in that the system may be conducive to evolving the bias based on homologous genes shared in their sensory/neural systems. Secondary loss seems a more parsimonious explanation than multiple gains of preference since it is arguably far more difficult to gain than to lose a preference. However, given the LPA bias appears evolutionarily labile even within genera, it is a weak argument at best. Further studies of additional poeciliid species are necessary before any definitive conclusions can be drawn. Although studies suggest fin and body size preferences are products of a single bias for larger male apparent size or LPA (Haines and Gould, 1994; Rosenthal and Evans, 1998; Karino and Matsunaga, 2002; MacLaren et al., 2004, submitted for publication; MacLaren and Rowland, 2006) we cannot rule out the possibility that these preferences are independently evolved traits that tap into different biases (e.g. separate preferences for male height and ventral body length). The apparent lack of dorsal fin and/or body size preferences
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in our fin: body ratio experiments supports the LPA hypothesis (MacLaren et al., 2004). However, we might expect a similar result if females see the two traits as separate but equivalent measures of male quality. The data from the current study do not allow us to distinguish between these two possibilities. The interaction between dorsal fin and body size during female mate choice in X. variatus may be more complicated than the additive effect predicted by the LPA hypothesis (MacLaren et al., 2004). Do the traits interact or act individually to influence female choice in this and other poeciliid species? Future experiments that offer females a choice between males with different combinations of the traits while permitting total LPA to vary accordingly, will allow us to test whether sailfin, body size, and sword length interact synergistically (Jennions and Petrie, 1997; Hankison and Morris, 2002) or additively on female preference in X. variatus. Acknowledgements This study was supported in part by a Merrimack College Faculty Development Grant. E. ElAchi, and P. Imbriano offered valuable assistance in data collection and analysis. C. MacLaren and two anonymous reviewers provided helpful comments on the manuscript. We thank D. Tombarelli for her assistance in lab maintenance. We also thank the Xiphophorus Genetic Stock Center, Texas State University, San Marcos, TX. for supplying the fish used in this study. The research methods presented herein were described in Research Protocol 1RDM1008 and approved by the Institutional Animal Care and Use Committee of Merrimack College. References Andersson, M., 1994. Sexual Selection. Princeton University Press, Princeton, NJ. Basolo, A.L., 1990a. Female preference for male sword length in the green swordtail Xiphophorus helleri (Pisces: Poeciliidae). Anim. Behav. 40, 332–338. Basolo, A.L., 1990b. Female preference predates the evolution of the sword in swordtail fish. Science 250, 808–810. Basolo, A.L., 1995a. Phylogenetic evidence for the role of a pre-existing bias in sexual. selection. Proc. Roy. Soc. Lond. B: Biol. 259, 307–311. Basolo, A.L., 1995b. A further examination of a preexisting bias favoring a sword in the genus Xiphophorus. Anim. Behav. 50, 365–375. Basolo, A.L., 1996. Phylogenetic distribution of a female preference. Syst. Biol. 45, 290–310. Basolo, A.L., 2002a. Congruence between the sexes in preexisting receiver responses. Behav. Ecol. 13, 832–837. Basolo, A.L., 2002b. Female discrimination against sworded males in a poeciliid fish. Anim. Behav. 63, 463–468. Bisazza, A., Pilastro, A., Palazzi, R., Marin, G., 1996. Sexual behaviour of immature. male eastern mosquitofish: a way to measure intensity of intra-sexual selection. J. Fish Biol. 48, 726–737. Bischoff, R.J., Gould, J.L., Rubenstein, D.I., 1985. Tail size and female choice in the guppy (Poecilia reticulata). Behav. Ecol. Sociobiol. 17, 253–255. Borowsky, R.L., 1984. The evolutionary genetics of Xiphophorus. In: Turner, B.J. (Ed.), Evolutionary Genetics of Fishes. Plenum Publishing Corp., pp. 235–310. Breden, F., Ptacek, M.B., Rashed, M., Taphorn, D., Figueiredo, C.A., 1999. Molecular Phylogeny of the live-bearing fish genus Poecilia (Cyprinodontiformes: Poeciliidae). Mol. Phylogent. Evol. 12, 95–104. Brooks, R., Endler, J.A., 2001. Direct and indirect sexual selection and quantitative. genetics of male traits in guppies (Poecilia reticulata). Evolution 55, 1002–1015. Dosen, L.D., Montgomerie, R., 2004. Female size influences mate preferences of male guppies. Ethology 110, 245–255. Endler, J.E., 1992. Signals, signal conditions and the direction of evolution. Am. Nat. 139, S125–S153. Endler, J.E., Houde, A.E., 1995. Geographic variation in female preferences for male traits. in Poecilia reticulata. Evolution 49, 456–468. Farr, J.A., 1989. Sexual selection and secondary sexual differentiation in poeciliids: determinants of male mating success and the evolution of female choice. In: Meffe, G.K., Snelson Jr., F.F. (Eds.), Ecology and Evolution of Livebearing Fishes. Englewood Cliffs, Prentice Hall Inc., NJ, pp. 91–124.
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MacLaren, R.D., Rowland, W.J., Morgan, N., 2004. Female preferences for sailfin and body size in the sailfin molly, Poecilia latipinna. Ethology 110, 363–379. MacLaren, R.D., Fontaine, A., Iacozzi, S., Ash, M., Ash, P. Female preference for male lateral projection area in Poecilia reticulata, submitted for publication. Nakagawa, S., Cuthill, I.C., 2007. Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol. Rev. 82, 591–605. O’Brien, W.J., Slade, N.A., Vinyard, G.L., 1976. Apparent size as the determinant of prey selection by bluegill sunfish (Lepomis macrochirus). Ecology 57, 1304–1310. O’Brien, W.J., Evans, B., Luecke, C., 1985. Apparent size choice of zooplanktivorous sunfish—exceptions to the rule. Environ. Biol. Fish. 13, 225–233. Pfennig, K.S., 2000. Female spadefoot toads compromise on mate quality to ensure conspecific matings. Behav. Ecol. 11, 220–227. Proctor, H.C., 1991. Courtship in the water mite Neumania papillator: males capitalize on female adaptations for predation. Anim. Behav. 42, 589–598. Ptacek, M.B., Breden, F., 1998. Phylogenetic relationships among the mollies (Poeciliidae: Poecilia: Mollienesia group) based on mitochondrial DNA sequences. J. Fish. Biol. 53 (Supplement A), 64–81. Ptacek, M.B., Travis, J., 1996. Inter-population variation in male mating behaviours in the sailfin molly, Poecilia latipinna. Anim. Behav. 52, 59–71. Ptacek, M.B., Travis, J., 1997. Mate choice in the sailfin molly, Poecilia latipinna. Evolution 51, 1217–1231. Rauchenberger, M., Kallman, K., Morizot, D.C., 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, G.G., Evans, C.S., 1998. Female preference for swords in Xiphophorus helleri. reflects a bias for large apparent size. Proc. Natl. Acad. Sci. U.S.A. 95, 4431–4436. Rosenthal, G.G., Wagner, W.E.J., Ryan, M.J., 2002. Secondary reduction of preference for sword ornament in the pygmy swordtail Xiphophorus nigrensis (Pisces: Poeciliidae). Anim. Behav. 63, 37–45. Rowland, W.J., 1989a. The ethological basis of mate choice in male threespine sticklebacks, Gasterosteus aculeatus. Anim. Behav. 38, 112–120. Rowland, W.J., 1989b. Mate choice and the supernormality effect in female sticklebacks (Gasterosteus aculeatus). Behav. Ecol. Sociobiol. 24, 433–438. Rowland, W.J., 1999. Studying visual cues in fish behavior: a review of ethological techniques. Environ. Biol. Fish. 56, 285–305. Ryan, M.J., 1998. Sexual selection, receiver biases, and the evolution of sex differences. Science 281, 1999–2003. Ryan, M.J., Keddy-Hector, A., 1992. Directional patterns of female mate choice and the role of sensory biases. Am. Nat. Suppl. 139, S4–S35. Sokal, R.R., Rohlf, F.J., 1981. Biometry and the Principles and Practice of Statistics in Biological Research, 2nd edn. 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Contents lists available at ScienceDirect
Behavioural Processes journal homepage: www.elsevier.com/locate/behavproc
Female bias for enlarged male body and dorsal fins in Xiphophorus variatus R. David MacLaren a,∗ , John Gagnon b , Ran He c a
Merrimack College, Department of Biology, Mendel Center, North Andover, MA 01845, USA Immune Disease Institute, 100 Longwood Ave., Boston, MA 02115, USA c University of Illinois at Urbana-Champaign, Champaign, IL 61820, USA b
a r t i c l e
i n f o
Article history: Received 3 November 2010 Received in revised form 22 March 2011 Accepted 23 March 2011 Keywords: Female preference Poecilidae Sensory bias Sexual selection Xiphophorus variatus
a b s t r a c t Female preference for male fin elaborations in Poeciliid fishes may be driven by a sensory bias for increased lateral projection area (LPA) that has existed since the lineages diverged from a common ancestor. Previous research supports this hypothesis demonstrating female Poecilia latipinna, Poecilia mexicana, and Poecilia reticulata prefer males of larger body and dorsal fin size, but exhibit no such preferences when controlling for total LPA. In the current study, we further tested this hypothesis by presenting female platys, Xiphophorus variatus, with pairs of dummy males differing in: (1) body size (holding dorsal fin size constant); (2) dorsal fin size (holding body size constant); and (3) dorsal fin: body size ratio (holding total LPA constant). Females spent more time near dummies of greater body and dorsal fin size; however, in the third experiment, neither fin size, body size, nor any particular dorsal fin + body size combination was preferred. These results provide additional support for the LPA and sensory bias hypotheses, demonstrating that female X. variatus not only prefer males with “swords”, but sailfin-like dorsal fins as well when body size is held constant. Shared preference for increased LPA is consistent with common ancestry of the sensory/neural systems in females of all four species. © 2011 Elsevier B.V. All rights reserved.
1. Introduction Females may develop perceptual biases in mate preferences due to a sensory bias in their nervous systems formed by natural selection, sexual selection, or pleiotropic effects (Kirkpatrick and Ryan, 1991; Endler, 1992). Such biases may reflect ecological constraints (Proctor, 1991; Endler, 1992) or basic properties of nervous systems (Ryan and Keddy-Hector, 1992; Rosenthal and Evans, 1998; MacLaren, 2006). Regardless of the bias origin, females are preferentially attracted to males that stimulate their sensory systems more than other males. If a male sends a novel signal which taps into a latent bias, these males are preferred as mates. Thus, a preexisting bias may affect the nature and direction of sexual selection when a new trait arises (Basolo, 1995a). Support for the preexisting bias hypothesis requires evidence that the female preference evolved within the species’ lineage prior to the evolution of the male trait that exploits the preference (Basolo, 1990a). The role of preexisting biases on female preference for male traits has been well studied in certain species of livebearing fishes (Poecilidae). For example, males of some species of the genus Xiphophorus possess an elongation of certain ventral caudal fin rays (the sword) that even females of related but unsworded
∗ Corresponding author. Tel.: +1 9788373543. E-mail address: [email protected] (R.D. MacLaren). 0376-6357/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.beproc.2011.03.006
species find attractive (e.g. X. maculatus; Basolo, 1990b, Xiphophorus variatus; Basolo, 1995b, Priapella olmecae; Basolo, 1995a). Phylogenetic information and mate choice tests suggest that female preference for swords arose before the Xiphophorus-Priapella clade diverged, pre-dating the evolution of the sword within Xiphophorus (Basolo, 1996). Species within the subgenus Poecilia (mollies) provide additional evidence of female bias for male fin elaborations. Male sailfin mollies (Poecilia latipinna) have an enlarged dorsal fin (sailfin) that is presented to females in courtship (Ptacek and Travis, 1996). Female P. latipinna as well as Poecilia mexicana (a species whose males do not naturally possess the sailfin phenotype) prefer to associate and mate with males of larger dorsal fin (MacLaren et al., 2004; MacLaren and Rowland, 2006; Jordan et al., 2006) and body size (Ptacek and Travis, 1997; MacLaren et al., 2004; MacLaren and Rowland, 2006). As with the sword ornament of Xiphophorus, phylogenetic information (Ptacek and Breden, 1998; Breden et al., 1999) suggests that female preference for enlarged dorsal fins arose before the monophyletic sailfin clade diverged from a shortfin ancestor, pre-dating the evolution of the sailfin trait within the subgenus Poecilia. Additionally, males of numerous guppy populations (Poecilia reticulata) show polymorphism in dorsal and caudal fin length including homoplastic “swords”, elongated tails and enlarged dorsal fins (Houde, 1997; Brooks and Endler, 2001; Karino and Matsunaga, 2002; MacLaren et al., submitted for publication)
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that along with body size (Endler and Houde, 1995; Karino and Matsunaga, 2002; MacLaren et al., unpublished data) offer a selective advantage in female mate choice in at least some populations (Bischoff et al., 1985; Endler and Houde, 1995; MacLaren et al., submitted for publication). These elongated caudal and dorsal fins, among other poeciliid fin elaborations may have originated from a shared female preference for larger apparent size in males, a preference that is common in many species (Andersson, 1994) and widespread among the Poecilidae (Ryan, 1998). Because a larger male projects a larger image onto the female’s retina at a given viewing distance (O’Brien et al., 1976, 1985; Rowland, 1989a,b), this could elicit a stronger sexual response (MacLaren, 2006). Fin elaborations may therefore have evolved as a way for males to increase their apparent size or lateral projection area (LPA) and consequent attractiveness to females (Haines and Gould, 1994; Rosenthal and Evans, 1998; Karino and Matsunaga, 2002; MacLaren et al., 2004). If females respond primarily to greater LPA rather than increased body or fin size per se, then female preference should be proportional to the male’s total LPA (body + fin area) regardless of his fin: body size ratio (MacLaren et al., 2004). The LPA hypothesis predicts that females: (1) prefer males of larger body and fin size; (2) show no preference between two males whose total LPAs (fin + body surface areas) are equal (i.e. increases in fin surface area compensate for decreases in body surface area and vice versa); and (3) show no preference for males with the fin elaboration over a finless male of equivalent LPA. Preference experiments with P. latipinna (MacLaren et al., 2004), P. mexicana (MacLaren and Rowland, 2006), and P. reticulata (MacLaren et al., submitted for publication) support all three of the predictions above. In this study we further test the LPA hypotheses by examining female preferences for male body size, dorsal fin size, and dorsal fin: body size ratio in X. variatus—a series of experiments similar to those previously conducted with P. latipinna, P. mexicana, and P. reticulata. Moreover, we want to know whether this preference stems from a preexisting bias. Female preference for increased male LPA not only in the subgenera Poecilia (“mollies”) and Lebistes (“guppies”) but the more distantly related genus Xiphophorus would support the preexisting bias hypothesis, demonstrating that female X. variatus (a species sexually monomorphic with respect to fin morphology) not only prefer males with artificial “sword” ornaments (Basolo, 1995b) but supernormal size dorsal fins and perhaps other forms of size manipulation that increase male LPA (Haines and Gould, 1994). A shared preference for sailfin-like dorsal fins and/or increased LPA would be consistent with common ancestry of the sensory/neural systems in females of P. latipinna, P. mexicana, P. reticulata, and X. variatus. 2. Methods 2.1. Subjects Test subjects were X. variatus, Zarco collected from the Arroyo Zarco locality west of Encino, Tamaulipas, Mexico (locale described by Borowsky (1984); stock source: Dr. Steve Kazianis, New York University, 6th of September 1996). The fish were shipped to the laboratory at Merrimack College from the Xiphophorus Genetic Stock Center, Texas State University, San Marcos, TX in the fall of 2008, placed in 378-l and 70-l mixed-sex stock tanks (water temperature 23–25 ◦ C; 16 h light:8 h dark cycle) and fed TetraMin fish flakes two times daily. We removed females from stock tanks at random and placed them in 70-l all-female subject tanks for a minimum of two months prior to testing. Females were then transferred to separate 8.75-l isolation tanks (30 cm × 15 cm × 20 cm) for approximately 48 h before becoming eligible for use as subjects. Each female was subjected to one of three experiments: body size
preference (expt I), dorsal fin preference (expt II), and fin: body size ratio preference (expt III). All three experiments were run concurrently between December 2008 and May 2010 as time permitted. All fish were kept in the laboratory under similar conditions for the same amount of time throughout the testing period. 2.2. Dummy construction In order to control for variation in male behavior among other traits, we used dummy males as stimuli, varying one trait (body size in expt I, dorsal fin size in expt II, and dorsal fin: body size ratio in expt III) while holding all other traits constant. The use of dummies allowed us to modify each variable independently while compromising little in the way of visual detail (Rowland, 1999). The dummies were produced as described in MacLaren et al. (2004). The Constant Fin Size Series for expt I consisted of three images measuring 35, 45 and 55 mm from the anterior tip of the fish to the end of the caudal fin, with proportional increases in the sizes of all fins except the dorsal, which was held constant at 12.5 mm in length (approximating the average dorsal fin size of mature males in our laboratory population, unpublished data). The Constant Body Size Series for expt II consisted of three images all measuring 45 mm from the anterior tip of the fish to the end of the caudal fin (approximating the average total length of mature males in our laboratory population, unpublished data) with dorsal fins measuring 12.5, 17.5 and 22.5 mm in length and proportional changes in fin allometry (i.e. no changes in fin shape). The Constant Body Ratio Series for expt III consisted of five dummies that differed in dorsal fin: body size ratio. The dummies included a male with no dorsal fin, and males with 0.28, 0.55, 0.83, and 1.11 cm2 fins with compensatory decreases in body area to ensure that all five maintained a constant LPA of 5.06 cm2 . This constant was determined by calculating the composite LPA of a male of average dorsal fin and body size from our study population (unpublished data). Thus, the dummies for expt III were designed such that the difference in body LPA between males in all 10 paired combinations of the five stimuli were equal to their difference in dorsal fin LPA. The dummies were identified as ‘small’ (S), ‘intermediate’ (I) and ‘large’ (L) in experiments I and II, in correspondence with their dorsal fin size/total lengths. For the fin: body ratio series (expt III), each dummy within a series was assigned a ranking from “1” to “5” in relation to its body LPA, from smallest (1) to largest (5) (Fig. 1). 2.3. Testing apparatus and procedure The testing environment consisted of three 17.5-l aquaria (50 cm × 26 cm × 13.5 cm each) lined up end to end using an apparatus and protocol identical to that used in previous mate preference experiments with Xiphophorus helleri (MacLaren and Daniska, 2008) and P. reticulata (MacLaren et al., submitted for publication). Female subjects were placed in an aquarium that was divided into three zones by two black vertical lines drawn on the front wall: a 30 cm × 26 cm × 13.5 cm ‘neutral zone’ flanked on each side by a 10 cm × 26 cm × 13.5 cm ‘preference zone’. A pair of aquaria flanking the female’s tank each housed an adjustable motorized belt and pulley system to which the dummy stimuli were attached (see MacLaren and Daniska, 2008 for further details). Each subject (expt I: n = 23; expt II: n = 22; and expt III: n = 22) was introduced into the center aquarium and allowed to acclimate for 15 min. Opaque screens blocking the female’s view of the dummies were then removed and the apparatus was turned on so that the dummies began to move. Using a Canon ZR930 digital video recorder, the female’s behavior was recorded for 5 min. The dummies were then switched to opposite sides of the arena for another 5 min of observation for a total of 10 min of testing per treatment. The subject was left undisturbed for 5 min before proceeding to the
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Fig. 1. Dummy males varying in body size, dorsal fin size, and dorsal fin-to-body size ratio used in expts. I, II, and III, respectively. Dummy letter designations S, I, and L (top left margin) correspond to the small, intermediate, and large body and fin size variants for experiments I and II. Dummy number designations 1–5 (bottom left margin) correspond to dorsal fin: body size variants from smallest (1) to largest (5) body size used in expt III.
next treatment of the series. For experiments I and II, all three possible paired combinations of the three dummies (dummy ‘L’ paired with dummy ‘S’, ‘L’ with ‘I’, and ‘S’ with ‘I’) were presented in random order to each female in a single day. In expt. III, all 10 paired combinations of the five dummies were presented in random order to each female over a period of two days; five of the 10 paired combinations on each day of testing (MacLaren and Daniska, 2008). No female was subjected to more than one set of treatments (i.e. one experiment).
2.4. Behavioral measures and statistical analyses As in previous experiments of this kind (MacLaren et al., 2004, submitted for publication; MacLaren and Rowland, 2006; MacLaren and Daniska, 2008), we played back all video data in real time to determine the total time each female spent in each preference zone as well as time spent in the neutral zone per 10-min treatment. Paired samples t-tests were used to compare the total time females spent in association with dummy A vs. dummy B in each treatment (e.g. L vs. S treatment of expt I). Female strength of preference was defined as time spent with dummy A − time with dummy B per 10 min treatment. Because each female received three treatments in experiments I and II, and ten treatments in expt III, all significance levels were adjusted to P < 0.017 and P < 0.005, respectively (Bonferroni procedure; Sokal and Rohlf, 1981). All probabilities given are two-tailed. In order to make easier inters-study comparisons, we used Cohen’s d to calculate the effect size (with 95% confidence interval) related to the preference strength for each treatment in all three experiments (Nakagawa and Cuthill, 2007). We conducted all statistical tests using the statistical program Sigmastat Ver. 11.2 (Systat Software, Point Richmond, CA, USA) with the exception of effect size calculations, which were made using software by David B. Wilson available online at http://mason.gmu.edu/∼dwilsonb/ma.html.
3. Results The female behaviors observed during both experiments included unison swimming, circling, and backing toward the male, all of which are activities attributed to mating behavior in the literature for poeciliids (Farr, 1989; Houde, 1997; Basolo, 2002a). There were no significant effects of dummy presentation order on female strength of preference in any of the three experiments (expt I: oneway repeated measures ANOVA, df = 2, F = 0.327, P = 0.723; expt II: one-way repeated measures ANOVA, df = 2, F = 0.186, P = 0.831; expt III: one-way repeated measures ANOVA; df = 9, F = 0.982, P = 0.456). Additionally, female total length (±SE) did not differ across experiments (expt I: 35.4 ± 0.05 mm, max = 4.10, min = 3.10; expt II: 36.0 ± 0.06 mm, max = 4.10, min = 3.00; expt III: 36.3 ± 0.06 mm, max = 4.20, min = 3.10; df = 2, F = 0.659, P = 0.521). Moreover, we found no evidence of female size differentially affecting female preference across treatments within any of the three experiments given that: (1) all subjects received all treatments within an experiment and (2) one-way repeated measures ANOVAs revealed no effect of female total length on strength of preference in any of the three treatments of experiments I (n = 23) and II (n = 22), nor in any of the ten treatments of expt III (n = 22). Paired samples t-tests comparing the total time females (n = 23) spent with the larger- vs. smaller-bodied male dummy and associated reports of the effect size (Cohen’s d with 95% confidence interval) in experiment I revealed that females spent significantly more time with the larger bodied of the paired males in each of the three treatments (P < 0.017; Table 1 and Fig. 2). Similarly, paired samples t-tests and associated Cohen’s d calculations comparing the total time females (n = 22) spent with the larger- vs. smaller-finned male in experiment II revealed a preference for the larger-finned dummy in all three treatments (P < 0.017; Table 1 and Fig. 2). However, paired samples t-tests comparing total time females (n = 22) spent in association with the larger-bodied, smaller-finned
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Fig. 2. Results from expt I, II, and III. (a) Expt I: The average amount of time (s) females (n = 23) spent in association with the smaller vs. larger of two dummy males in each of three 10 min treatments (dummy I vs. S, L vs. S, and L vs. I). (b) Expt II: The average amount of time (s) females (n = 22) spent in association with the smaller vs. larger of two dummy males in each of three 10 min treatments. (c) Expt III: The average amount of time (s) females (n = 22) spent in association with the smaller-bodied, larger-finned vs. larger-bodied, smaller-finned of two dummy males in each of ten 10 min treatments. * indicates Bonferroni corrected significant preference (paired samples t-tests; P < 0.017) for the larger of the paired males.
male vs. the smaller-bodied, larger-finned male in experiment III revealed no significant preferences in any of the 10 treatments (P > 0.005; Table 2 and Fig. 2). Thus, females did not exhibit a preference for any particular male across treatments in experiment III, including the dummy that best approximated the fin: body ratio of a typical X. variatus male (dummy no. 3; Fig. 1). Furthermore, in none of the four treatments that involved dummy no. 5 (a male lacking a dorsal fin; Fig. 1) did females prefer to associate with the alternative dummy that possessed a dorsal fin.
4. Discussion As demonstrated in similar studies with P. latipinna, P. mexicana, and P. reticulata, the preferences of female X. variatus satisfy all three predictions of the LPA hypothesis, suggesting that increased dorsal fin size can compensate for decreased body size and vice versa, and that preference is for male LPA rather than for dorsal fin and body size per se. Haines and Gould (1994) explored the basis of female preference for a male fin elaboration – the sword – in X.
R.D. MacLaren et al. / Behavioural Processes 87 (2011) 197–202 Table 1 Results from experiments I and II (female preference for male body and dorsal fin size, respectively): mean female strength of preference (SOP) (i.e. time spent in association with the larger male–time with the smaller male per 10 min test period) in each of three treatments of expt I (n = 23) and expt II (n = 22). Results of paired samples t-tests comparing total time (s) females spent in association with the larger vs. smaller male in each treatment and associated Cohen’s d calculations of the effect size (with 95% confidence interval) related to preference strength (Nakagawa and Cuthill, 2007). Treatment
Mean SOP (s)
t-value
p-value
Cohen’s d (95% C.I.)
Experiment I: preference for male body size (fin size control series) I vs. S 114.4 ± 35.7 3.20 0.004 1.147 (0.523–1.771) L vs. S 116.9 ± 28.1 4.16 < 0.001 1.253 (0.621–1.885) L vs. I 109.2 ± 36.9 2.96 0.007 0.923 (0.319–1.54) Experiment II: Preference for male dorsal fin size (body size control series) I vs. S 104.4 ± 36.0 2.90 0.009 0.958 (0.334–1.582) L vs. S 134.0 ± 29.7 4.51 <0.001 1.512 (0.842–2.182) L vs. I 97.3 ± 36.6 2.65 0.015 0.9561 (0.3323–1.58)
variatus and came to a similar conclusion, suggesting that the general feature females are responding to is total length as measured along the male’s ventral surface rather than sword or tail length per se. Females in the current study, however, did not base their preferences on total length alone. If they had, we would expect females to prefer the larger-bodied, smaller-finned dummies in experiment III, which did not occur. Still, the results of both studies suggest that female preference in platys may be for males of larger apparent size (Rosenthal and Evans, 1998). Preference for male dorsal fin size/LPA may be favored by females either through greater stimulation of the female sensory system and brain or due to an adaptive reason (Rowland, 1989a; Ryan and Keddy-Hector, 1992). The greater response of perceptual systems to increased stimulation often leads animals to prefer larger, brighter, or more vigorous mates, particularly in species where mate choice is mediated by visual cues (Rowland, 1989a; Kirkpatrick and Ryan, 1991). Increased body height in the form of a dorsal fin and/or body length in the form of an elongated tail are factors that enlarge the area of the retina swept by male images during courtship (Endler and Houde, 1995; MacLaren, 2006), perhaps favoring the evolution of such traits in males. Once established, the apparent size/LPA preference will be maintained through the female preexisting bias as well as Fisherian coevolution (Fisher, 1930). Additionally, female preference for larger male fin and/or body size may be adaptive in populations where size confers an advantage in intrasexual competition for resources and/or mating opportunities as observed in numerous poeciliids including X. variatus (Bisazza et al., 1996), among other heritable fitness Table 2 Results from experiment III (female preference for male dorsal fin: body size ratio): mean female strength of preference (SOP) (i.e. time spent in association with the larger-bodied, smaller-finned male-time with the smaller-bodied, larger-finned male per 10 min test period) in each of 10 treatments (n = 22). Results of paired samples t-tests comparing total time (s) females spent in association with the larger-finned, smaller bodied vs. smaller-finned, larger-bodied dummy male in each treatment and associated Cohen’s d calculations of the effect size (with 95% confidence interval) related to preference strength (Nakagawa and Cuthill, 2007). Treatment
Mean SOP (s)
1 vs. 2 1 vs. 3 1 vs. 4 1 vs. 5 2 vs. 3 2 vs. 4 2 vs. 5 3 vs. 4 3 vs. 5 4 vs. 5
35.3 −44.2 87.9 36.3 −26.8 35.2 25.4 −10.5 −40.0 7.1
± ± ± ± ± ± ± ± ± ±
22.4 27.4 44.2 47.6 36.1 38.4 39.7 23.6 36.0 30.7
t-value
p-value
Cohen’s d (95% C.I.)
1.57 −1.61 1.99 0.76 −0.74 0.92 0.64 −0.45 −1.11 0.23
0.130 0.122 0.060 0.455 0.466 0.370 0.530 0.660 0.280 0.820
0.412 (−0.185 to 1.010) − 0.444 (−1.043 to 0.154) 0.742 (0.131 to 1.353) 0.276 (−0.318 to 0.869) −0.257 (−0.851 to 0.336) 0.327 (−0.268 to 0.922) 0.225 (−0.368 to 0.818) −0.188 (−0.709 to 0.474) −0.392 (−0.989 to 0.204) 0.072 (−0.519 to 0.663)
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benefits correlated with male size (reviewed in MacLaren et al., 2004; MacLaren and Rowland, 2006). Alternatively, such a preference may be a correlated response to selection on male choice of larger, more fecund females (Ptacek and Travis, 1997; Gabor, 1999; Herdman et al., 2004; Dosen and Montgomerie, 2004). From the males’ prospective, if greater LPA increases attractiveness to females and improves reproductive success, then selection should favor male allocation of energy to body parts such as dorsal and caudal growth that maximize total LPA. This, however, assumes that females have opportunities to choose amongst males and that the costs of trait expression (e.g. increased predation or decreased swimming performance) do not exceed the mating benefits. Violation of either or both assumptions, along with genetic/developmental constraints, may explain the traits’ absence in male X. variatus. There is morphological and ontogenetic evidence that the swords and sailfin-like fins found in Xiphophorus, sailfins in mollies, and sword- and sailfin-like fins observed in certain populations of P. reticulata, have separate evolutionary origins (Rauchenberger et al., 1990; Basolo, 1996; Breden et al., 1999) and thus resemble one another as a result of parallel evolution (Basolo, 1995a). The common selective force behind such convergence may be female bias for males of larger apparent size or LPA. Just as the same initial bias may select different traits in different lineages (e.g. a sword vs. a sailfin) depending on the chance appearance of new variation, an initial bias could select for similar traits in different lineages (e.g. the independent evolution of swords in Xiphophorus and some guppy populations; Basolo, 1995a). There are however, several studies of female preference in poeciliid fishes that, although not designed to test LPA, produced results inconsistent with our hypothesis. Some mate preference experiments, for example, have demonstrated female discrimination against male fin elaborations (Basolo, 2002b; Rosenthal et al., 2002; Witte and Klink, 2005; Wong and Rosenthal, 2006; Fisher and Rosenthal, 2007; MacLaren and Daniska, 2008). Perhaps preference for male LPA and/or fin elaborations is an ancestral trait within the poeciliid family that has been secondarily lost or altered in some populations as a result of genetic drift (Rosenthal et al., 2002) or for some adaptive reason (e.g. caused females to mate at a suboptimal rate, mate with inferior males, or risk mating with heterospecifics; Pfennig, 2000; Hankison and Morris, 2002; Basolo, 2002b; Witte and Klink, 2005). Alternatively, the LPA bias may have evolved independently in the poeciliid species examined. This could suggest parallel evolution of the preference as hypothesized for male fin elaborations above. Shared preference for increased LPA is consistent with common ancestry of the sensory/neural systems in P. latipinna, P. mexicana, P. reticulata, and X. variatus females providing support for the single origin/secondary loss hypothesis. However, the same logic could be used to explain multiple gains of preference in that the system may be conducive to evolving the bias based on homologous genes shared in their sensory/neural systems. Secondary loss seems a more parsimonious explanation than multiple gains of preference since it is arguably far more difficult to gain than to lose a preference. However, given the LPA bias appears evolutionarily labile even within genera, it is a weak argument at best. Further studies of additional poeciliid species are necessary before any definitive conclusions can be drawn. Although studies suggest fin and body size preferences are products of a single bias for larger male apparent size or LPA (Haines and Gould, 1994; Rosenthal and Evans, 1998; Karino and Matsunaga, 2002; MacLaren et al., 2004, submitted for publication; MacLaren and Rowland, 2006) we cannot rule out the possibility that these preferences are independently evolved traits that tap into different biases (e.g. separate preferences for male height and ventral body length). The apparent lack of dorsal fin and/or body size preferences
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in our fin: body ratio experiments supports the LPA hypothesis (MacLaren et al., 2004). However, we might expect a similar result if females see the two traits as separate but equivalent measures of male quality. The data from the current study do not allow us to distinguish between these two possibilities. The interaction between dorsal fin and body size during female mate choice in X. variatus may be more complicated than the additive effect predicted by the LPA hypothesis (MacLaren et al., 2004). Do the traits interact or act individually to influence female choice in this and other poeciliid species? Future experiments that offer females a choice between males with different combinations of the traits while permitting total LPA to vary accordingly, will allow us to test whether sailfin, body size, and sword length interact synergistically (Jennions and Petrie, 1997; Hankison and Morris, 2002) or additively on female preference in X. variatus. Acknowledgements This study was supported in part by a Merrimack College Faculty Development Grant. E. ElAchi, and P. Imbriano offered valuable assistance in data collection and analysis. C. MacLaren and two anonymous reviewers provided helpful comments on the manuscript. We thank D. Tombarelli for her assistance in lab maintenance. We also thank the Xiphophorus Genetic Stock Center, Texas State University, San Marcos, TX. for supplying the fish used in this study. The research methods presented herein were described in Research Protocol 1RDM1008 and approved by the Institutional Animal Care and Use Committee of Merrimack College. References Andersson, M., 1994. Sexual Selection. Princeton University Press, Princeton, NJ. Basolo, A.L., 1990a. Female preference for male sword length in the green swordtail Xiphophorus helleri (Pisces: Poeciliidae). Anim. Behav. 40, 332–338. Basolo, A.L., 1990b. Female preference predates the evolution of the sword in swordtail fish. Science 250, 808–810. Basolo, A.L., 1995a. Phylogenetic evidence for the role of a pre-existing bias in sexual. selection. Proc. Roy. Soc. Lond. B: Biol. 259, 307–311. Basolo, A.L., 1995b. A further examination of a preexisting bias favoring a sword in the genus Xiphophorus. Anim. Behav. 50, 365–375. Basolo, A.L., 1996. Phylogenetic distribution of a female preference. Syst. Biol. 45, 290–310. Basolo, A.L., 2002a. Congruence between the sexes in preexisting receiver responses. Behav. Ecol. 13, 832–837. Basolo, A.L., 2002b. Female discrimination against sworded males in a poeciliid fish. Anim. Behav. 63, 463–468. Bisazza, A., Pilastro, A., Palazzi, R., Marin, G., 1996. Sexual behaviour of immature. male eastern mosquitofish: a way to measure intensity of intra-sexual selection. J. Fish Biol. 48, 726–737. Bischoff, R.J., Gould, J.L., Rubenstein, D.I., 1985. Tail size and female choice in the guppy (Poecilia reticulata). Behav. Ecol. Sociobiol. 17, 253–255. Borowsky, R.L., 1984. The evolutionary genetics of Xiphophorus. In: Turner, B.J. (Ed.), Evolutionary Genetics of Fishes. Plenum Publishing Corp., pp. 235–310. Breden, F., Ptacek, M.B., Rashed, M., Taphorn, D., Figueiredo, C.A., 1999. Molecular Phylogeny of the live-bearing fish genus Poecilia (Cyprinodontiformes: Poeciliidae). Mol. Phylogent. Evol. 12, 95–104. Brooks, R., Endler, J.A., 2001. Direct and indirect sexual selection and quantitative. genetics of male traits in guppies (Poecilia reticulata). Evolution 55, 1002–1015. Dosen, L.D., Montgomerie, R., 2004. Female size influences mate preferences of male guppies. Ethology 110, 245–255. Endler, J.E., 1992. Signals, signal conditions and the direction of evolution. Am. Nat. 139, S125–S153. Endler, J.E., Houde, A.E., 1995. Geographic variation in female preferences for male traits. in Poecilia reticulata. Evolution 49, 456–468. Farr, J.A., 1989. Sexual selection and secondary sexual differentiation in poeciliids: determinants of male mating success and the evolution of female choice. In: Meffe, G.K., Snelson Jr., F.F. (Eds.), Ecology and Evolution of Livebearing Fishes. Englewood Cliffs, Prentice Hall Inc., NJ, pp. 91–124.
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