Behavioral Ecology Advance Access originally published online on May 7, 2007
Behavioral Ecology 2007 18(4):696-700; doi:10.1093/beheco/arm032
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Mate preference for multiple cues: interplay between male and nest size in the sand goby, Pomatoschistus minutus
Department of Biological and Environmental Sciences, University of Helsinki, PO Box 65, FI–00014 University of Helsinki, Finland
Address correspondence to T.K. Lehtonen, who is now at Department of Biology, University of Konstanz, D–78457 Konstanz, Germany. E-mail: topi.lehtonen{at}uni.konstanz.de. K. Lindström is now at the Environmental and Marine Biology, Åbo Akademi University, FI–20500 Turku, Finland.
Received 29 December 2006; revised 5 March 2007; accepted 20 March 2007.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Female mating preferences are often based on more than one cue. In empirical studies, however, different mate choice cues are typically treated separately ignoring their possible interactions. In the current work, we studied how male body size and size of the male's nest jointly affect mate preferences of female sand gobies, Pomatoschistus minutus. The females were given a binary choice between males that differed either in body size or size of their nest or both. We found that neither body size nor size of the nest alone affected male attractiveness, but together these 2 cues had a significant effect. Specifically, large males were more popular among females when they had a large nest than when they occupied a small nest. The results suggest that if interaction effects between multiple mate choice cues are not considered, there is a danger of ignoring or underestimating the importance of these cues in sexual selection by female choice.
Key words: mate choice, multiple cues, nest size, Pomatoschistus minutus, sexual selection.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Females often base mating decisions on more than one mate choice cue (Candolin 2003
). The effects of the different male traits and other target cues of mate choice are not necessarily additive (e.g., Kirkpatrick et al. 2006). Nevertheless, the prevailing practice has been to reduce the properties of target traits to a single preference value that is independent of other traits. Consequently, relatively little is known about interaction effects of different cues in mate choice.
On the one hand, when resources provided by males are crucial for female reproductive success, females are expected to base their mate choice on the quality of the resources directly rather than on male traits such as size or dominance position (Qvarnström and Forsgren 1998). On the other hand, several mechanisms may cause male body size to be an important mate choice cue even when resources possessed by the males are important. For example, large males may be efficient in caring and defending the offspring, or large body size may correlate with genetic quality (reviewed in Andersson 1994; Berglund et al. 1996). Indeed, large males are preferred mating partners in species with a variety of different mating systems (Andersson 1994). In teleost fishes, in which male parental care is exceptionally common (Gross and Sargent 1985), the crucial resource held by males is often a nest site, where the female will deposit her eggs. Females are likely to gain direct benefits by preferring appropriate nest sites: the nest may shield the parents or the offspring from harmful environmental factors or predation (e.g., Lindström and Ranta 1992; Jones and Reynolds 1999; Hansell 2000). The location of the nest may also be important (Candolin and Voigt 1998; Östlund-Nilsson 2000). When the ability of a male to build or defend the nest depends on his condition, females have an opportunity to gather information about male quality by assessing characteristics of the nest (e.g., Kvarnemo et al. 1998; Barber et al. 2001). Moreover, a female may benefit by choosing a large nest site for egg deposition if males allocate more care to these nests (Pampoulie et al. 2004) or if filial cannibalism or predation of the female's reproductive output is diluted as a consequence of a higher number of egg clutches in the nest (Rohwer 1978).
When male size is important for nest holding potential, male body size and nest characteristics are expected to correlate. This has often been found to be the case (e.g., Downhower and Brown 1980, Lindström 1992b; Oliveira et al. 2000; Candolin and Voigt 2001), though not always (Östlund-Nilsson 2000; Lehtonen and Lindström 2004). Male choice for nest sites, independent of direct competition, may also favor the correlation between properties of nests and nest holders (Kvarnemo 1995). Despite the extensive literature on independent effects of male size and nest characteristics on mate choice, and on correlations between these 2, very little is known about their joint effect on female mating decisions. The interesting, but rarely addressed, topics include whether females do assess these 2 cues simultaneously, whether attractiveness of all male types is similarly affected by a certain nest type, and how preferences are affected by a possible mismatch in information contents of different cues.
In a small marine fish, the sand goby (Pomatoschistus minutus), males alone take care of the nest and offspring. It has been suggested that in this species, a large number of eggs in a nest, or a large nest site as such, has a positive effect on male care behavior and hatching success of eggs (Forsgren et al. 1996; Pampoulie et al. 2004). Large males are dominant in male–male interactions (Magnhagen and Kvarnemo 1989; Lindström 1992b), and male size correlates with the male's nest holding potential (Lindström 1992b; Lindstöm and Pampoulie 2005). Females prefer large males under some conditions (Forsgren 1992; Kvarnemo and Forsgren 2000), but not under some other circumstances (Magnhagen and Kvarnemo 1989; Lindström and Kangas 1996; Forsgren 1997). In addition, females choose males according to nest characteristics (the amount of sand on the top of nest: Svensson and Kvarnemo 2005; Lehtonen 2007), and they prefer male behavior associated with a large nest size (Lindström et al. 2006). Field data indicates that small males in large nests may receive eggs less frequently than similar-sized males in small nests (Lindström 1992b) and males with large nests may have to exceed a threshold body size before being able to attract females (Lindström 1992a). However, the possible interaction effects between male and nest size on female choice have not been experimentally assessed before. In this study, we addressed the question by providing females a choice between different combinations of small and large males with a small or a large nest site.
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METHODS |
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The experiment was conducted at Tvärminne zoological station (59°50'N, 23°15'E) during the sand goby breeding season in 2005 using wild-caught fish. Before the experiment, fish were stocked in large (100 l), single-sex tanks and fed twice a day with live mysids, Neomysis integer, or frozen chironomid larvae. All stocking and experimental tanks were exposed to natural light and had a continuous seawater throughflow.
The experiment was designed to measure the effects of male size, nest size, and male size x nest size interaction on female preferences. We assessed preferences by allowing females to choose between 2 males holding a nest site. The test tanks were divided into 3 compartments by 2 removable, transparent Plexiglass dividers with holes for water exchange between the compartments. A middle female compartment consisted of the space between 2 male compartments at each end of the tank (Figure 1). Thus, the female was able to see both males, but the female compartment separated the males from each other. We noticed no interactions between the males. The bottom of all 3 compartments was covered with a 4-cm layer of fine sand. Water was pumped into the male compartments and flowed out from the female compartment. Plastic blinds shielded the tanks against external disturbance.
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Before the experiment, we weighed the fish and measured their total lengths. All females tested were gravid and ready to spawn. The males had revealed high breeding motivation by building a nest. If this did not happen within 48 h, we replaced both males. The preference tests consisted of 2 trials. A preference trial was initiated when we placed a female in the central compartment. After an acclimatization period of 10 min, we noted the position and behavior of the female and any courtship behavior of both males every 5 min for a total of 20 observation events, giving a total duration of 105 min. After this first trial was completed, we removed the female from the tank. In order to control for possible side biases, we then turned the tank around its vertical axis 180° and conducted an identical preference trial a few hours later. We considered the female to associate with a male when her body was orientated towards that male and the distance between her and the male compartment was no more than 3 cm. Females in this position were actively observing male movements, and most of these females were also responding clearly to any courtship of the male and tried to follow him to his nest through the divider. If the combined number of times a female was observed in this position was less than 5, we did not consider the female to be eager to spawn and disregarded the preference test. In the sand goby, results of this association preference method correspond to actual mating decisions of females when an opportunity to mate is given (Lehtonen and Lindström 2007
). Male courtship behavior was classified according to the following scale—1: no or passive courtship (the number of times the male was seen engaged in courtship was 2 or less), 2: intermediate level of courtship, 3: intensive courtship (courtship was noticed on at least 10 observation events). Each individual was used only once.
The males used in the experiment were either small (<45 mm) or large (
50 mm). The average weight of small males was 0.47 g (standard deviation [SD] = 0.076, n = 183) and that of large males 1.08 g (SD = 0.18, n = 185). These 2 size classes represent the low and high ends of the size distribution of male gobies holding a nest site in the field (Lehtonen and Lindström 2004). We provided the males with halved clay flowerpots, which served as small (diameter 4 cm) or large (diameter 10 cm) nest sites. The small nest site was comparable in size with a shell of the mollusc Mya arenaria. Mya shells are commonly used by sand gobies as nest sites in the Baltic Sea (Lehtonen and Lindström 2004). The large flowerpots were similar in size (and overall appearance when covered by sand) to a large natural nest constructed under a flat rock (Lehtonen and Lindström 2004). Altogether, we had 6 different setups (treatments): 1) large males, one with a small nest and other one with a large nest (n = 31), 2) small males, one with a small nest and other one with a large nest (n = 30), 3) a small and a large male with large nests (n = 29), 4) a small and a large male with small nests (n = 31), 5) a small male with a small nest and a large male with a large nest (n = 30), and 6) a small male with a large nest and a large male with a small nest (n = 33) (Figure 1). The male–nest combinations were randomly distributed to each side of the tank. The size of the fish did not differ between the setups (females: analysis of variance [ANOVA], F5,178 = 0.68, P = 0.64; small males: ANOVA, F4, 178 = 1.02, P = 0.40; large males: ANOVA, F4,180 = 1.14, P = 0.34).
Statistical analyses
Because the criteria of normality and heteroscedasticity were met after square root transformation, we proceeded analysing the effects of male size and nest size on female mating decisions with repeated-measures ANOVA using MIXED procedure in SAS 8.2 statistical package (SAS Institute Inc.). MIXED procedure generates general linear mixed models, which are based on restricted maximum likelihood methods (Littell et al. 1996). Female preference for the 2 males/nests in the tank was used as the dependent variable. The explanatory variables were male size and nest size. Repeated subject was each female. We also assessed pairwise differences between all the 4 possible male size–nest size combinations (small/large male x small/large nest). Type I error arising from the multiple paired comparisons was corrected using Tukey–Kramer method. Finally, we applied the multinomial logit model to test for differences in male courtship behavior among the treatments.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Male size did not have a direct effect on female choice independent of nest size (repeated-measures ANOVA, F1,183 = 0.087, P = 0.77). Similarly, nest size did not have a clear, independent effect (repeated-measures ANOVA, F1,183 = 2.73, P = 0.10). However, female preferences were based on these 2 traits together (repeated-measures ANOVA, male size x nest size interaction, F1,183 = 5.55, P = 0.020). The most popular combination of male and nest size was a large male possessing a large nest and the least popular combination a large male with a small nest (Figure 2). Combinations including a small male fell between these 2 extremes (Figure 2). In paired comparisons between the different combinations, the only significant difference was the higher attractiveness of a large male with a large nest than that of a large male with a small nest (Tukey–Kramer, t = 2.82, degrees of freedom [df] = 183, Padj = 0.027; all other pairwise comparisons: Padj > 0.10). Male courtship behavior did not significantly differ among the treatments (multinomial logit model,
2 = 7.93, df = 5, P = 0.16).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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In this study, we are among the first to experimentally demonstrate that female preferences are sometimes based more strongly on a simultaneous, combined effect of different cues than on each cue independently or additively (a review of interactions among multiple cues in Candolin 2003
). Sand goby females did not show a preference for male body size or size of the nest the male occupied, but the interaction of these 2 cues had a significant effect: a large male with a large nest was preferred to a large male with a small nest. Earlier laboratory studies on various fish species have revealed female choice for nest size or other nest characteristics (e.g., Bisazza et al. 1989; Candolin and Voigt 1998; Candolin and Reynolds 2001) or male body size (reviewed in Kodric-Brown 1990), but the combined effects of the 2 cues have not been assessed. Failures to reveal a significant role for either of these 2 (or some other) cues in female choice may in some cases have been due to not considering the combined effects, even when they might have existed. Indeed, our results may help to explain some of the contradictory results in empirical mate choice studies. For example, earlier work on sand gobies have suggested female preference for large males (Forsgren 1992; Kvarnemo and Forsgren 2000), indifferent mate choice in relation to body size (Magnhagen and Kvarnemo 1989; Lindström and Kangas 1996; Forsgren 1997), and a tendency to prefer small males (Lehtonen 2007). In each of the studies, females may really have preferred the combination of male size and nest characteristics, not male size independently; nest size relative to male size was not standardized between the studies. Our results also illustrate, why males should choose nest sites relative to their own body size even in the absence of male–male competition, as shown by Kvarnemo (1995).
Females of many bird as well as fish species prefer to lay their eggs in a nest that is well build or appropriately located (e.g., Candolin and Voigt 1998; Hansell 2000; Svensson and Kvarnemo 2005). A nest site has therefore a potential to act as a sexual male ornament (Kvarnemo et al. 1998; Barber et al. 2001). Moreover, nests that already contain eggs may be favored because in these nests predation on eggs is diluted or egg survival is otherwise enhanced (Jamieson 1995; Forsgren et al. 1996). If nest size physically limits the number of eggs that can fit in it, the dilution benefit may on average be higher in a large nest. Males, in turn, may adjust their care behavior according to nest size (Pampoulie et al. 2004; Lindström et al. 2006). It is not surprising then that in some species, females prefer to spawn in large nests even when these are guarded by small males (Bisazza et al. 1989; Marconato et al. 1989). However, many of the costs associated with egg fanning, nest maintenance, and defence may depend on nest size relative to male size. For example, a high-quality resource may attract both more competitors and competitors with higher fighting ability (Alcock 2000), and the consequent risk of a nest takeover may be higher for small than large males (Lindström and Pampoulie 2005). In addition, small stickleback males need to fan more intensively to compensate for their smaller pectoral fin size (Künzler and Bakker 2000), potentially compromising their ability to take care of a large nest. When the high maintenance costs or the increased risk of failure in nest defence affect egg survival, it should be beneficial for females to be able to choose a male that matches the size and quality of his nest.
Female preference for a match between male and nest size is exactly what we found in this study: sand goby females avoid large males occupying a small nest site. If the preference induces males to actively choose nest sites according their own properties (see Kvarnemo 1995), we may consider a male's propensity to choose a nest site as a trait under sexual selection, the benefit of which depends on body size. In such a case, a theory suggests that a correlation between the 2 traits will develop (Jennions et al. 2001). However, size-depended costs of nest maintenance and male–male competition for nest sites are also likely to contribute to the observed positive correlation between nest and male size in several species (e.g., Downhower and Brown 1980; Côte and Hunte 1989). This is also true for the sand goby: male size and nest size correlate more clearly in habitats where competition for nest sites is intense (Lehtonen and Lindström 2004). Indeed, nest site availability and competition between males may severely limit the scope for nest site choice. A mismatch situation, a large male occupying a small nest, may give a signal of inferior body condition or nest defence abilities of the male. The male may also be motivated to eventually abandon the small nest in order to look for a larger one. Moreover, because a small offspring number is known to be more valuable to small than large individuals (Galvani and Coleman 1998), small sand goby males may value the number of eggs that fit into a small nest more than large males. This relationship between male size and the male's expected reproductive output may, in turn, affect the quality of the care he provides; a large male occupying a small nest may be an inferior father.
In our mate preference tests, the 2 males were placed in the opposite ends of a test tank in order to facilitate the focal female's opportunity to assess them simultaneously (Figure 1). This setup does not completely rule out the effect of male–male competition on the results. However, we have several reasons to assume that, if present at all, male–male interactions did not significantly influence the results. 1) Water was pumped into the male compartments and flowed out from the female compartment. This should effectively have prevented exchange of any chemical signals between the males. 2) The males guarding their nests were separated by 2 Plexiglass dividers and a distance of approximately 50 cm. In the field, for example, males have been found to overlook alternative nest sites if they are dispersed by 50 cm or more suggesting that males are only concerned about their immediate vicinity (Lindström 1988). 3) Despite regular observations of male behavior, we did not notice any interactions between the 2 males in any of the replicates. 4) The statistical comparisons of female preference were conducted over the 6 different choice setups. Male courtship behavior did not significantly differ among these setups, suggesting that a systematic bias in male courtship, caused by male–male interactions or some other factor, does not explain our results.
In the current study, the effects of environmental or social variables, such as competition or predation pressure, were not considered. However, these factors may affect the optimal combination between male size and nest size. For example, if competition between males had been allowed, increased defence costs could have enlarged differences in attractiveness of the male/nest combinations. Hence, the lack of opportunity for male–male competition may explain why we did not find a difference in attractiveness of small males with different-sized nests. In addition, we only considered 2 cues (male size and nest size) attempting to eliminate or randomize all other factors that might affect female preferences. However, it is possible, if not likely, that there are also other cues that affect female mating decisions in interaction with the cues considered. In general, when sexual selection on male traits depends on these interactive effects between different male traits, or between male traits and environmental factors, benefit of any one male trait is not absolute and selection is therefore less likely to be directional (Jennions and Petrie 1997; Candolin 2003). Hence, when female preferences are based on combined effects of different cues rather than each of them additively, the erosion of genetic variation as a consequence of mate choice is likely to be slowed down.
To conclude, we revealed that sand goby females do not necessarily base their mate preferences on male body size or nest size as such, but rather on a combination of these 2 cues. The results suggest that the common practice of considering the effects of different mate choice cues independent of each other may result in a biased interpretation of sexual selection pressures operating in the population. Hence, we encourage future studies that focus on the interplay between different mate choice cues. These studies may also wish to explore effects of environmental parameters on these interactions.
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ACKNOWLEDGEMENTS |
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We would like to thank Anders Berglund, Veijo Jormalainen, Ola Svensson, Outi Vesakoski, and Bob Wong. The work was conducted at Tvärminne zoological station, and financial support was provided by the Academy of Finland and Walter and Andrée de Nottbeck's foundation (S.R.).
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