Male-trait-specific variation in female mate preferences

Animal Behaviour 87 (2014) 39e44

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Male-trait-specific variation in female mate preferences Susan M. Lyons 1, Debora Goedert, Molly R. Morris* Department of Biological Sciences, Ohio University, Athens, OH, U.S.A.

a r t i c l e i n f o Article history: Received 25 July 2013 Initial acceptance 6 September 2013 Final acceptance 25 September 2013 Available online 6 November 2013 MS. number: A13-00615 Keywords: context-dependent genetic benefit embryonic environment gene-by-environment interaction mate preference plasticity postembryonic environment signal reliability swordtail fish Xiphophorus multilineatus

Empirical studies identifying the causes of variation in mate preference are needed to assist in determining when variation is adaptive. We examined the strength of female preference in the swordtail fish Xiphophorus multilineatus for two sexually selected male traits (body size and symmetrical bar number) across variation in both embryonic and postembryonic environments. We measured brood size, then split fry from each brood into high- and low-quality diet treatments. Once females reached sexual maturity, we tested their mate preferences using dummies in dichotomous choice tests. Both the embryonic (brood size) and postembryonic (diet) environment influenced females’ strength of preference for symmetrical bar number; females from smaller broods as well as females raised on high-quality diets had a stronger preference for symmetrical bars. However, only the postembryonic environment influenced preference for male size, with females on the low-quality diet having a stronger preference for larger males. There was no relationship between the strength of preference for the two traits across females. Our results demonstrate that plasticity in mate preferences can depend on the specific traits being assessed. We hypothesize that at least one of the preferences may be tracking the conditions that influence signal reliability of the preferred trait. In addition, we demonstrate an influence of the embryonic environment on mate preference, which is rarely considered or controlled for in studies of adaptive variation in mate preferences. Ó 2013 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

An increasing number of studies are detecting relationships between environmental variation and female mate preferences, leading to adaptive hypotheses for plasticity in mate preferences (Cotton, Small, & Pomiankowski, 2006; Grether, Kolluru, Rodd, De la Cerda, & Shimazaki, 2005; Jennions & Petrie, 1997; Qvarnström, 2001). It has been hypothesized that females would be less discriminating in poor-quality environments due to the decreased ability to invest in the costs of mate discrimination (Cotton et al., 2006). However, recent findings that females in poor condition sometimes have stronger preferences (e.g. Fisher & Rosenthal, 2006; Griggio & Hoi, 2010; Tobler, Schlupp, & Plath, 2011) highlight the complexity of the relationship between the environment and mate preferences, as well as the need to further examine how both condition- and context-dependent factors interact to produce plasticity in mate preferences. Most studies that have examined adaptive variation in mate preferences have focused on how environmental conditions influence the individual with a mate preference (e.g. predation: Godin & Briggs, 1996; Stoner & Breden, 1988; Willis, Rosenthal, & Ryan,

* Correspondence: M. R. Morris, Department of Biological Sciences, Ohio University, Athens, OH 45701, U.S.A. E-mail address: [email protected] (M. R. Morris). 1 S. M. Lyons is now at the Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, U.S.A.

2012; nutritional environment: Hunt, Brooks, & Jennions, 2005; Syriatowicz & Brooks, 2004; social experience: Breden, Novinger, & Schubert, 1995; Jordan & Brooks, 2011; Tudor & Morris, 2009). However, environmental variation could influence the preferred traits as well, leading to situations where either the benefit of being choosy varies across environments (i.e. condition-dependent genetic benefits hypothesis: Cotton et al., 2006), and/or the information that the trait provides about benefits varies across environments (the signal reliability hypothesis: Wagner, 2011). Variation in the reliability of sexually selected signals could select for plasticity in mate preferences, as there would be selection for costly preferences to be stronger in those conditions where traits reveal the most reliable information about their potential benefits. Many sexually selected traits are condition dependent, and gene*environment interactions for sexually selected traits indicate that these traits will not be reliable signals of benefits under all conditions (Candolin, 2003; Greenfield & Rodriguez, 2004; Higginson & Reader, 2009; Ingleby, Hunt, & Hosken, 2010; Mills et al., 2007; Wagner, 2011). For example, because additive genetic variation for eyespan of stalk-eyed flies is greater in poor-quality environments (David, Bjorksten, Fowler, & Pomiankowski, 2000), this could select for stronger mate preferences for larger eye-stalks in the poor-quality environment, where being choosy would yield greater genetic benefits (Qvarnström, 2001). Signal reliability can vary across environments for signals of direct benefits as well, such as

0003-3472/$38.00 Ó 2013 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.anbehav.2013.10.001

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S. M. Lyons et al. / Animal Behaviour 87 (2014) 39e44

the noncongruent gene*environment interaction effects on male chirp rate in crickets (Tolle & Wagner, 2011). Examining the influence of environmental variation on multiple mate preferences provides an opportunity to determine whether variation in female mate preference is specific to the female regardless of the preferred male trait, or is male-trait specific. Females often have preferences for multiple male traits, and in many cases each trait provides the female with different information about a potential mate (i.e. Candolin, 2003; Hankison & Morris, 2003). Indeed, models suggest that multiple mate preferences may have evolved due to the impact of fluctuating environments on signal content, transmission or receiver interests (Bro-Jørgensen, 2010). Increased additive genetic variation of a trait will increase its signal content in relation to genetic benefits, and yet the conditions that produce the highest heritability are not the same for all traits, suggesting that there could be trait-specific variation in signal reliability. Hoffmann and Merilä (1999) reviewed the conditions (favourable versus unfavourable) that produce the highest heritability across several traits and organisms, and reported that some traits have higher heritability in favourable conditions, while others have higher heritability in unfavourable conditions. For example, while Drosophila thorax length has higher heritability in unfavourable conditions (De Moed, De Jong, & Scharloo, 1997), Drosophila melanogaster wing length has higher heritability in favourable conditions (Hoffmann & Schiffer, 1998). In addition, the environments that produce the most reliable signals of direct benefits may not be the same across preferred traits. If females use the environment in which they develop to determine which male traits are most reliable, and not all traits are reliable in the same environments, then the relationship between strength of preference and environmental variation would not be expected to be the same across a female’s multiple preferences. We examined the influences of both embryonic (brood size) and postembryonic (diet) developmental environments experienced by female swordtail fish Xiphophorus multilineatus on the strength of female mate preferences for two sexually selected traits: vertical bar number symmetry (Morris, Rios-Cardenas, Lyons, Tudor, & Bono, 2012) and male size (standard length, Rios-Cardenas, Tudor, & Morris, 2007). Both traits depend to some extent on condition during development but are fixed in adult males (Kallman, 1989; Morris et al., 2012). Wild-caught females prefer symmetrical bar numbers (Morris et al., 2012) and larger males (Rios-Cardenas et al., 2007). By examining how these two mate preferences vary across developmental conditions, we determined whether the variation is specific to the trait being assessed, as compared to the environment influencing the female independently of the male trait. If strength of preference depends on how environments influence the female, then we would expect a relationship between the strength of preference for the two traits across females. However, if variation in preference is trait specific, then we may detect a different response in the strength of preference for the two traits across conditions. Finally, the developmental environment that has the largest impact (in this case embryonic as compared to postembryonic) could also be male-trait specific (Crews, 2003), and therefore we wanted to determine the influence of both of these environments on both preferences. METHODS Subjects and Developmental Environments All fish were descendants of individuals collected in March 2004 from the Rio Oxitipa in San Luis Potosí, Mexico. Isolines were created by isolating pregnant females from four different laboratory mesocosms into individual 37.8-litre tanks. Most broods in this

species consist of full sibs (Luo, Sanetra, Schartl, & Meyer, 2005). Brood size, often negatively correlated with egg size (Bashey, 2006), was scored at parturition. At 15 days, fry were isolated into 18.9litre aquaria. At 30 days, siblings were divided into high-quality (Tetra-min Tropical Flakes (47% protein) 2X/day and bloodworms 3X/week) and low-quality (Nishikoi Wheat Germ Koi Food (20% protein) 2X/day) diet treatments. Primary differences were in protein content, previously shown to influence female reproductive performance in swordtail fish (Chong, Ishak, Osman, & Hashim, 2004). At sexual maturity (Rosen, 1960), we measured daughter’s standard length (SL, distance from snout to end of caudal peduncle) with callipers. Preference Tests Dichotomous choice tests were used to test daughters’ mate preferences for both bar number symmetry and male size. Test order was randomized and the two choice tests were conducted at least 2 weeks apart. We used three pairs of dummy males constructed from digital images of three different live males printed on plastic transparency for each test. For bar number symmetry stimuli, we altered the photographs of the three males using Adobe Photoshop CS4 (Adobe Systems) to create three pairs of dummies, with a symmetrical and an asymmetrical (total bar number held constant) version of each male (Supplementary Fig. S1a). For male size stimuli, we altered the photographs of the three males to create three pairs of dummies, with a larger (isometric increase in body size by 3 mm SL) and a smaller (isometric decrease in body size by 3 mm SL) version of each male (Fig. S1b). The dummy testing apparatus, which followed from Robinson, Tudor, and Morris (2011), consisted of a motorized pulley system that moved each dummy parallel to its respective side of the test tank, so they appeared to swim back and forth alongside the tank. The use of dummies allows for more control of variation in the stimuli than does the use of live males and removes potentially confounding influences of male behaviour. We used lines to divide the test tank (37.9-litre) into three equal compartments (a central, neutral area where we introduced the female, and two preference zones at opposite ends, one for each dummy stimulus) and summed the time that females spent in each preference zone across two 8minute trials. We switched the dummies to opposite sides of the tank between trials. The difference in time spent associating with each male type measured each female’s strength of preference. Association time is a good indicator of female mate choice in X. multilineatus (Morris, Rios-Cardenas, & Brewer, 2010). Data Analysis Only daughters with at least one sister on the opposite diet treatment were used in analyses (19 broods, high-quality diet ¼ 27 female fry; low-quality diet ¼ 30 female fry). We determined whether there was a correlation between strength of preference for male size and bar symmetry using a multiresponse mixed model (MCMCglmm package; Hadfield, 2010), with mother identity included as a random effect and no intercept. We specified a noninformative prior for the variance components of both response variables and for the random factors with variance limit (V) of 1 and a belief parameter (n) of 0.002. We ran the model for 1 000 000 iterations, sampling the chain with 100 iterations of interval, and a burn-in period of 10 000. We estimated the correlation between strength of preference for male size and strength of preference for male bar number symmetry as the covariance between the two measures of strength of preference divided by the square root of the product of the strength of preference for male size and bar symmetry variances (i.e. the

S. M. Lyons et al. / Animal Behaviour 87 (2014) 39e44

covariance divided by the product of the standard deviations; Sokal & Rohlf, 1995). We tested effects of embryonic and postembryonic environment on strength of preference for bar symmetry and male size using mixed effect models with mother identity, mesocosm and male pair stimulus as random effects, correcting for nonindependence (Pinheiro & Bates, 2000; Zuur, Ieno, Walker, Saveliev, & Smith, 2009). Each model was fitted using REML, including size at sexual maturity as a covariate, and brood size and diet as fixed effects. Size at sexual maturity was standardized and brood size was squareroot transformed to meet assumptions of the model. Significance levels and confidence intervals for the estimates of explanatory variables were obtained through Markov-chain Monte Carlo simulations (N ¼ 1 000 000), using the package languageR (Baayen, 2011). We tested assumptions of the model following Pinheiro and Bates (2000). We verified assumptions of normality of the withingroup errors, homogeneity of variance and normality of random effects by visual inspection of a normal probability plot of the residuals, a plot of the standardized within-group residuals by the within-group fitted values and a normal probability plot for each level of random effects, respectively (Pinheiro & Bates, 2000). The visualization of those plots also indicated the presence of possible outliers in the data. One outlier was removed for the model of preference for symmetry. Finally, we plotted residuals against predictor variables to check for possible patterns indicating nonlinearity (Pinheiro & Bates, 2000). All analyses were performed using R statistical software v.2.15 (R Development Core Team, 2012). RESULTS There was no relationship between female strength of preference for male size and strength of preference for bar number symmetry. The mean correlation was estimated as 0.040, and the 95% confidence interval was 0.294 to 0.298 (Fig. 1). Preference for bar symmetry decreased with increasing brood size (embryonic environment) and was greater for females on the high-quality diet (postembryonic environment; Fig. 2a, Table 1).

900

SOP for male size

600

300

0

−300

−600 −900

−600

−300

0

300

600

900

SOP for bar symmetry Figure 1. Relationship between strength of preference (SOP, s) for male size and bar number symmetry in swordtail fish across all females.

41

There was no influence of female size on preference for bar symmetry. Preference for male size was significantly influenced by female size, with larger females having a stronger preference for larger males. When controlling for female size, preference for male size was also influenced by diet but not by brood size; females raised on the lower-quality diet had stronger preferences for larger males (Fig. 2b, Table 2). For the model on strength of preference for size, variances estimated for mother identity, mesocosm of origin and dummy pair corresponded to 0.0%, 8.2% and 2.2% of the total variance, respectively. For the model on strength of preference for bar symmetry, the variance estimate for mother identity was 36.3% of the total variance, and that for the mesocosm of origin and dummy pair was 0.0%. DISCUSSION The impact of environmental variation on strength of female mate preferences for two sexually selected traits in X. multilineatus depended on the particular male trait being assessed. Our measure of embryonic environment (brood size) influenced preference for bar number symmetry but not for male size. The postembryonic environment (quality of a female’s diet prior to sexual maturity) significantly influenced mate preferences for both of the traits we examined, but in opposite directions. Preference for male size was stronger for females raised on a low-quality diet, while preference for bar number symmetry was stronger for females raised on a high-quality diet. The lack of a correlation between the strength of preference for the two traits across females, as well as the way in which diet influenced the two preferences, suggests that environmental conditions did not influence variation in strength of female mate preference independently of the male trait. These results also suggest that multiple stages of development, including the embryonic environment, can influence mate preferences. Measuring mate preferences using dummies rather than live males has a very long history in ethological studies. Tinbergen (1948) pioneered the use of dummies in his studies of threespine stickleback, Gasterosteus aculeatus, and they have been used extensively in studies of both fishes and birds (reviewed in Rowland, 1999). Preference for the sword in females of the swordless platyfish, Xiphophorus maculatus, first detected by Basolo (1990) using live males with swords surgically added, was detected by Haines & Gould (1994) using dummies. Dummies also remove any confounding influences of male behaviour, which can influence the strength and repeatability of visual preferences (i.e. guppies, Kodric-Brown & Nicoletto, 1997). Therefore, dummies allowed us to tease apart the female mate preferences of particular male traits (body size, bar number symmetry) while controlling for potentially confounding influences of male behaviours (i.e. larger males courting more than smaller males). The influence of gene*environment interactions on sexually selected traits has been identified as a problem for the evolution of mating preferences based on indirect benefits (Greenfield & Rodriguez, 2004; Grether et al., 2005; Kokko & Heubel, 2008), but also for preferences for signals of direct benefits if there are noncongruent gene*environment interaction effects (Tolle & Wagner, 2011). If what a female sees is not always what she gets (i.e. male traits are not reliable indicators of benefits in some conditions), then selection for costly mate choice would be weak. However, variability in signal reliability could select for plastic mate preferences if mate preferences are in some way able to track whether males have developed in the environments that produce the reliable signals (Qvarnström, 2001; Wagner, 2011). Evidence that selection is strongest on male traits in the common yellowthroat, Geothlypis trichas, when the traits are most reliable indicators of male quality (Freeman-Gallant et al., 2010) lends

42

S. M. Lyons et al. / Animal Behaviour 87 (2014) 39e44

(a)

(b) 800 * 600 SOP for male size

SOP for bar symmetry

500

0

400

200

0

−500

−200 2.0

2.5 3.0 3.5 Brood size (sqrt)

4.0

HQ

LQ Diet

Figure 2. (a) Strength of preference (SOP, s) for bar number symmetry in swordtail fish, as influenced by a female’s brood size and diet: sisters raised on high-quality diets (D, dashed line); sisters raised on low-quality diets (C, solid line). (b) Strength of preference (SOP, s) for male size in swordtail fish, as influenced by diet. Plot represents estimates and standard errors.

support to this hypothesis. In guppies, geographical variation has been detected in the strength and sign of preferences, as well as in the number of male traits that females assess (Endler & Houde, 1995), which could suggest that some traits are more reliable in some environments than others. The results from the current study demonstrate that variation in mate preferences in X. multilineatus is specific to the male trait being assessed. Therefore, given the gene*environment interaction for most sexually selected male traits, along with the patterns of mate preference variation described above, we hypothesize that mate preferences have in some cases been selected to track environmental changes in signal reliability. Male size in X. multilineatus is correlated with allelic and copy number variation of the melanocortin-4 receptor (Mc4r) gene on the Y chromosome (Lampert et al., 2010). The genetically influenced size classes of X. multilineatus males reach sexual maturity at different ages (Bono, Rios-Cardenas, & Morris, 2011), and both male size and age at sexual maturity are under selection due to mate preference and survival to sexual maturity (Rios-Cardenas & Morris, 2011). If variation in strength of female preference for larger males in X. multilineatus tracks conditions under which male size is a more reliable indicator of the number of Mc4r genes that a

female’s offspring would inherit (indirect benefits), then our results would suggest that male size should be a more reliable signal in low-quality, postembryonic environments. Lampert et al. (2010) detected a relationship between male size and number of copies of the melanocortin-4 receptor (Mc4r) gene in wild-caught males; therefore, we predict that this correlation will be weaker in males raised in a higher-quality laboratory environment. In addition, if female preference for bar number symmetry evolved due to indirect benefits, then we would expect signal reliability of bar number symmetry to be greater in a high-quality postembryonic environment. Our understanding of the gene*environment interaction for vertical bar symmetry in X. multilineatus males is limited, but there is evidence to suggest that genetic variation in growth strategies may be more reliably correlated with bar symmetry in high-quality environments. Males that optimize growth over development (as compared to development over growth) are more asymmetrical the faster they grow (Morris et al., 2012), suggesting that bar number symmetry would more reliably indicate the difference between males with two different growth strategies in higher-quality environments.

Table 1 Effects of embryonic (brood size) and postembryonic (diet) environments on strength of preferences for bar number symmetry in swordtail fish

Table 2 Effects of embryonic (brood size) and postembryonic (diet) environments on strength of preferences for male size in swordtail fish

Estimate

Intercept Size at SM (standardized) Brood size (square root) Diet: LQ

SE

95% confidence interval

pMCMC

2.5%

97.5%

539.45 57.75

246.83 44.58

57.11 151.96

998.263 26.757

0.0316 0.1664

148.00

77.4

281.54

9.101

0.0365*

210.57

75.67

364.92

27.744

0.023*

SM: sexual maturity; LQ: low-quality diet. Estimates and standard errors were obtained using mixed effects models with mother, mesocosm of origin and stimulus pair used in the test as random effects. Confidence intervals and pMCMC values were obtained through Markov-chain Monte Carlo simulations (N ¼ 1 000 000). *P < 0.05.

Intercept Size at SM (standardized) Brood size (square root) Diet: LQ

Estimate

SE

95% confidence interval 2.5%

97.5%

28.9 120.28

255.63 50.34

590.58 13.58

674.4 220.6

0.9462 0.0267*

21.29

78.58

203.4

152.3

0.8238

251.76

98.04

445.6

0.0137*

52.12

pMCMC

SM: sexual maturity; LQ: low-quality diet. Estimates and standard errors were obtained using mixed effects models with mother, mesocosm of origin and stimulus pair used in the test as random effects. Confidence intervals and pMCMC values were obtained through Markov-chain Monte Carlo simulations (N ¼ 1 000 000). *P < 0.05.

S. M. Lyons et al. / Animal Behaviour 87 (2014) 39e44

The importance of understanding the causes and consequences of plasticity in female mate preference has been highlighted previously (Cotton et al., 2006; Jennions & Petrie, 1997), and yet most studies focus on the influence of the postembryonic environment on female condition (Cotton et al., 2006) or on separating heritable variation in mate preference from the influence of the experiences of adults (e.g. Griggio & Hoi, 2010). The embryonic environment influences the expression of many adult behaviours (Crews, 2003), and therefore it should not be surprising to find embryonic influences on mate preferences. However, this environment is rarely considered (but see Putz & Crews, 2005) or controlled for in studies of plasticity in mate preference. Consideration of the influence of the embryonic environment could help explain variation in preferences from studies that have not controlled for its influence. Some environments in which females develop will not be as predictive of signal reliability and, therefore, plasticity in response to changes in these environments are less likely to be due to the signal reliability hypotheses. This could be the case for the embryonic environment in swordtail fish. We used brood size as an indicator of embryonic environment, as fry from larger broods are smaller in this species (Murphy, Goedert, & Morris, n.d.). However, variation in brood size can be based not only on the quality of the environment in which the mother develops (X. multilineatus; Murphy et al., n.d.), or the state of the mother (Xiphophorus birchmanni; Kindsvater, Rosenthal, & Alonzo, 2012) but also on the size class of the mother’s mate, which is influenced by allelic variation on the Y chromosome (X. multilineatus; Rios-Cardenas, Murphy, & Morris, in press). Self-matching genetic benefits (Qvarnström, 2001) might be a more plausible possibility to explore as an explanation for the relationship between brood size and strength of preference for symmetry. A potential problem for any hypothesis suggesting that the environmental condition in which males develop influences the benefits that females gain from being choosy is dispersal across conditions between life-history stages (Kokko & Heubel, 2008). In these situations, females would not be expected to use the environment in which they develop as a cue for male development, but they could instead assess an additional trait that provides information about the environment in which the males develop (Wagner, 2011). The extent to which swordtails disperse across environments that vary in quality is not known. However, if a population or species were to experience this type of dispersal, females could assess an ‘indicator’ trait that is correlated with the quality of the male’s developmental environment to determine the environment in which the male developed (i.e. the sword: Basolo, 1998; bar symmetry: Morris et al., 2012) in addition to the trait that provides information about benefits (Wagner, 2011). Female swordtails may appear to gain only indirect benefits from males (Constantz, 1989), but there are numerous ways by which females in this system could gain direct benefits from being choosy (Wagner, 2011). Females could gain direct benefits for mate choice through lower search costs for larger or more symmetrical males, lower costs of harassment from other males when associating with larger or symmetrical males, and either more sperm or more viable sperm from larger or more symmetrical males. As for sperm viability, the opposite has been shown in the closely related species Xiphophorus nigrensis, as smaller sneaker males have both more viable and longer-lived sperm than do larger courter males (Smith & Ryan, 2010). In the case of the current study, predictions for relationships between signals and either direct or indirect benefits across environmental conditions would be the same: reliability of body size as a signal of direct benefits would be greater in low-quality environments, while reliability for bar number symmetry would be greater in high-quality environments.

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Finally, note that the hypotheses proposed to explain the evolution of variation in mate preferences will not be mutually exclusive across preferences for different male traits, or even within a preference for the same trait. For example, the strength of preference for larger males was stronger for larger females, as previously detected in this species (Rios-Cardenas et al., 2007), as well as stronger for females raised on a low-quality diet. These apparently contradictory results suggest that females may be varying their preferences based on their own state as well as the environment in which choosing a larger male would be most beneficial to offspring fitness. In addition, the variation in mate preferences we detected could have been mediated through the development of the visual sensory system (e.g. Hingle, Fowler, & Pomiankowski, 2001). Ontogeny of the visual system in poeciliid fishes occurs primarily during the embryonic stage (Kunz, Ennis, & Wise, 1983), and so changes in visual acuity could explain the decreased preference for male symmetry in females from larger broods. Selection could act on visual acuity as a mechanism to correlate preferences with environmental conditions, or the variation could be nonadaptive due to developmental constraints. The differences between these two hypotheses will be an important distinction to make, and will require examining the fitness consequences across reaction norms of preferences and male traits. Mate preferences and the traits that are being assessed are most likely developing in a fluctuating environment, and therefore selection may be linking changes in the strength of preference to changes in the value of the information of the male traits. Furthermore, examining preferences in the context of gene*environment interactions is likely to reveal not only heritable variation in mate preferences, which has proven in some cases to be difficult to detect (Brooks & Endler, 2001; Schielzeth, Burger, Bolund, & Forstmeier, 2008; but see Bakker & Pomiankowski, 1995), but also heritable variation in the male traits. Interestingly, we detected a stronger preference for one male trait in the low-quality environment, as have other studies (Fisher & Rosenthal, 2006; Griggio & Hoi, 2010; Tobler et al., 2011). This suggests that the best environment for detecting heritability of female mate preferences or male traits may not be the higher-quality environments of most laboratories (Hoffmann & Merilä, 1999). It will be important to consider hypotheses that include how the environment influences the preferred trait as well as the individual with the preference, across several developmental environments before we can gain a clear picture of adaptive variation in mate preferences. Acknowledgments We thank B. Bond, S. Askins, P. Braun and B. Tarselli for fish care, S. Kuchta, D. Miles, K. Johnson, O. Rios-Cardenas and K. WilliamsSieg for comments on the manuscript, and the Mexican Government for permission to collect fish. Funding was provided by the National Science Foundation to M.R.M and O.R.C. All experiments comply with the Animal Care Guidelines of Ohio University (Animal Care and Use no. L01-01). Supplementary Material Supplementary material for this article is available, in the online version, at http://dx.doi.org/10.1016/j.anbehav.2013.10.001. References Baayen, R. H. (2011). LanguageR. http://cran.rproject.org/web/packages/languageR/ index.html. Bakker, C. M., & Pomiankowski, A. (1995). Mini-review: the genetic basis of female mate preferences. Journal of Evolutionary Biology, 8, 129e171.

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