Behavioral Ecology Advance Access originally published online on September 29, 2005
Behavioral Ecology 2005 16(6):1042-1048; doi:10.1093/beheco/ari085
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The importance of sperm competition risk and nest appearance for male behavior and female choice in the sand goby, Pomatoschistus minutus
Department of Zoology, Stockholm University, SE-104 05 Stockholm, Sweden
Address correspondence to O. Svensson, who is now at the Department of Biological Sciences, University of Hull, Hull HU6 7RX, UK. E-mail: o.svensson{at}hull.ac.uk.
Received 25 November 2004; revised 28 July 2005; accepted 31 August 2005.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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To test if an increased sperm competition risk affects male behavior and mating decisions of both sexes, we performed two experiments using the sand goby, Pomatoschistus minutus, a nest-building fish with exclusive paternal care. In our first experiment, a nest-holding male, with a confined female, was sequentially exposed to a vial with a sneaker male or an empty vial. While male courtship, nest building, displacement fanning, and time outside the nest were unaffected, individual males showed a higher mucus preparation effort inside the nest in the presence of a sneaker male than when alone. We found such mucus to contain sperm, thus clearly suggesting an importance in sperm competition. In our second experiment, a female was free to spawn with two different males, one of which was exposed to a confined sneaker male. Male mating success was not affected by the presence of a sneaker male. However, the volume of sand the male had put on his nest was positively associated with female spawning decision, while nest-opening width was not. In a partial correlation of five traits thought to attract females (nest-opening width, sand volume, male courtship display, displacement fanning, and male size), males that fanned well were found to also build large nests or display intensely, but not both. This indicates that rather than being jacks-of-all-trades, individual males focus on a subset of traits for attracting females.
Key words: alternative reproductive tactics, courtship, mating decisions, signal honesty, sperm competition, sperm trail.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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From the male perspective, mate guarding serves to lessen the risk of sperm competition and to protect paternity (Birkhead and Møller, 1998
). Males investing in courtship and offspring survival are often reproductively "parasitized" by other males, and alternative reproductive tactics, in which one tactic invests whereas the other tactic parasitizes on the investment of the other male, are common (Birkhead and Møller, 1998; Taborsky, 2001). In fish with external fertilization, aggression of the investing male toward "parasitic" males trying to spawn simultaneously is very common (Taborsky, 1994), which can be seen as a form of mate guarding. When the risk of sperm competition is high, males sometimes refuse spawning (Alonzo and Warner, 1999), court less (Le Comber et al., 2003), or even attack females (Magnhagen, 1998). Apart from the lost paternity, other males may also decrease mating success by disrupted courtship (Saether et al., 1999; Trail and Koutnik, 1986) or female avoidance.
Females of some species prefer to spawn under sperm competition (Candolin and Reynolds, 2002; Oliveira et al., 2002; Widemo, 1998), whereas others avoid it (Alonzo and Warner, 1999), depending on whether or not it is beneficial to the females to have multiple males taking part in the mating. For instance, in the internally fertilizing guppy, Poecilia reticulata, multiple mating increases female fitness. Multiply mated females have larger broods after a shorter gestation period, and the offspring show more developed antipredator skills and schooling behavior, compared to singly mated females (Evans and Magurran, 2000). Other benefits of multiple mates include "good" genes, increased genetic diversity of the offspring, genetic compatibility (Olsson and Madsen, 2001), and increased fertilization success (Marconato and Shapiro, 1996), as well as getting access to resources such as nuptial gifts and paternal care (Griffith et al., 2002). In addition, when satellite males participate in nest defense, their presence serves females, and finally, females may copy the choice of satellite males (Oliveira et al., 2002). However, multiple males are not always beneficial to the females. In fishes where eggs are fertilized externally, parasitic spawning can resemble forced copulations in species with internal fertilization over which the females have no control. Without female control, sperm competition overrides female choice, and if fertilization rate is high also without parasitic spawners, the females do not receive any benefits in terms of increased fertilization rates either. Furthermore, if paternity affects paternal care (Neff and Gross, 2001; Sheldon, 2002) and if genetically low-quality males perform parasitic spawning, females would be predicted to avoid sperm competition from peripheral males.
With or without the presence of parasitic spawners, females are expected to be careful in their choice of mate. Traits assessed during mate choice that affect mating decisions are referred to as cues, and different cues can be used sequentially if they work at different distances (Candolin, 2003). Adaptive cues may decrease mate choice errors or cost of choice, and they can contain information that associates with different aspects of fitness such as direct and indirect benefits, which may or may not be correlated. For example, female choice of nest characteristics can generate direct benefits for the offspring, such as good environmental conditions, less predation, or better paternal care (Hansell, 2000; Svensson and Kvarnemo, 2003). However, through co-option the nest may also have ornamental functions advertising both direct and indirect benefits (Jones and Reynolds, 1999; Soler et al., 1998b). Nevertheless, this does not mean that there is a change in the nest's original function, only a shift in the optimal level of nest building (Lotem et al., 1999).
In the sand goby, Pomatoschistus minutus, females are known to use multiple cues in their choice of mate. Male display (Forsgren, 1997), displacement fanning (Pampoulie et al., 2004), male size (Forsgren, 1992; Kvarnemo and Forsgren, 2000), breeding coloration (Forsgren, 1992), and sound during nest inspection (Lindström and Lugli, 2000) are all documented choice criteria, or at least used in courtship. However, between individuals of the same species, different traits or resources preferred by the females can be positively correlated (Sikkel, 1995; Taylor et al., 1998), negatively correlated (Reynolds et al., 1993; Soler et al., 1998a), or uncorrelated (Candolin and Reynolds, 2001; Reynolds et al., 1993). Furthermore, the optimal level of courtship may differ among males due to unequal benefits (e.g., attractivity) and costs (e.g., predation), which may differ in different environments (e.g., light). For an attractive male or a male with high-quality resources, a single display may be sufficient to show his interest, and a female might choose him immediately (Reynolds, 1993).
In the present study, one aim was to test experimentally whether individual males alter their courtship behavior during increased sperm competition risk (i.e., in the presence of a sneaker male). We predicted that they would reduce their courtship or change it from "spectacular" displays into a less visual form of courtship, such as displacement fanning, to avoid attracting the attention of sneaker males. Another aim was to determine if males increase their mucus preparation effort during increased sperm competition risk. The mucus of gobiids has been found to protect the eggs from bacterial infection (Fishelson, 1991) and to contain pheromones (Colombo et al., 1980; Locatello et al., 2002) and spermatozoa (Marconato et al., 1996). Due to the latter, a role in sperm competition has been suggested (Ota et al., 1996). In the sand goby, P. minutus, inactive sperm have been found in the seminal vesicles in which the mucus is stored (Kvarnemo C and Svensson O, unpublished). Other aims included testing whether female spawning decisions and male mating success are affected by sperm competition risk. Furthermore, we know from previous work that males build smaller nest openings before spawning when exposed to sneaker males (Svensson and Kvarnemo, 2003). Therefore, we wanted to test whether high nest-building effort is correlated with a higher male mating success. In addition, to investigate whether males that perform well in, for instance, courtship display also build good nests, we performed a partial correlation on five male traits that have been suggested to be cues important for female spawning decision (Forsgren, 1992, 1997; Kvarnemo and Forsgren, 2000; Pampoulie et al., 2004).
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METHODS |
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The species
The sand goby, P. minutus (Pallas), is a small short-lived marine fish. Males build nests by covering empty mussel shells with sand and attract females by courtship display including erect fins and tail beats. Females show their spawning interest by exhibiting blackened eyes and by a characteristic hovering movement. The male alone tends the eggs until hatching. In the study area, sand gobies usually have one breeding season only, but during each of several brood cycles, the male may receive eggs from several females (Forsgren, 1999
). Parasitic spawnings are common in this species. In a field study, half of all nests contained eggs fertilized by another male than the nest-holding male, and one-tenth of all eggs were fertilized parasitically (Jones et al., 2001). Small males with rudimentary breeding coloration have been found to be sexually mature, with huge testes with viable sperm but only rudimentary or small seminal vesicles (involved in mucus secretion), thereby differing from males in full breeding coloration. When dissecting all sand goby males in catches early and late in the season no immature males were found (Kvarnemo C and Svensson O, unpublished).
General experimental procedure
The experiments were conducted at Klubban Biological Station and the nearby Kristineberg Marine Research Station (58° 15' N, 11° 28' E) on the west coast of Sweden, in May–June of 2002, 2003, and 2005. Fish were caught with a hand trawl in Bökevik bay, close to the stations, and kept in 130-l storage aquaria for at least 36 h before the trials. All experimental aquaria were provided with a 3-cm layer of sand and running natural seawater (temperature range 8°C–16°C). Light from fluorescent tube fittings was used in all aquaria. Halved flowerpots were used as artificial nest sites. The fish were fed mussel meat (Mytilus edulis), shrimp (Crangon crangon), and Alaska pollock (Theragra chalcogramma) every day during storage and every third day during the experimental procedure. In all experiments, a female was placed in a plastic vial to encourage nest building. Also, in some setups, a sneaker male in a vial was put into the aquarium. The vials (0.5 l) were provided with a net over the top and holes on the sides to enable water circulation. In the experiments described below, the female used to encourage nest building was not used in experiments with the same male. The males used as sneaker males were small and often with very little breeding coloration, therefore, not predicted to build nests or be seen as competitors over nest sites.
Male behavior experiment
To test if an increased sperm competition risk affects nest-holding male behavior, a behavior experiment was performed in which the nest-holding male first experienced a vial with a sneaker male and thereafter an empty vial (n = 14), first an empty vial and thereafter a vial with a sneaker male (n = 15), or, to control for effects of habituation, an empty vial two times (n = 8). The setup of the experiment also enables us to correlate traits used as cues in mate choice. Each 20-l aquarium (38 x 21 x 25 cm) contained one male (medium to large, size range 49–74 mm total length, mean ± SD 56 ± 5 mm) and a nest site. When a nest was built, an empty vial or a vial containing a sneaker male (range 35–43 mm, mean ± SD 41 ± 2 mm) was added, and 1 h later, a vial with a female was added as well (Figure 1A). A DV camera was placed in front of two aquaria, which were filmed at the same time. The acclimation period allowed the male to become aware of the sneaker male. Sneaker males of the black goby, Gobius niger, can squat for hours nearby a nest, apparently waiting for sneaking opportunities (personal observation), which is the situation we simulated. Fifteen minutes later, we started the recording which lasted for 45 min. Thereafter, the camera and the vial containing a female (not used with the same male again) were removed, and the empty vial was exchanged for one containing a sneaker male or vice versa. However, in the eight control trials, the empty vial was exchanged for another empty vial. One hour later, a vial with a new female was added, and the camera was placed in front of the two aquaria again. Fifteen minutes later the two aquaria were filmed for 45 min. After the experiment, the total length of all males was measured to the nearest millimeter.
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contained a gravid female and the other vial contained either a sneaker male (s
) during the first filming which was changed for an empty vial (e) for the second filming or in the opposite order, whereas some males were exposed to empty vials both times. (B) The setup in experiment 2, the mating success experiment. The female was allowed to spawn with either of two nest-building males, one of which was exposed to a sneaker male in a vial (sNest attributes used in the statistical analyses were measured at the start of the first film. However, any changes in nest appearance between the start of the first film and the end of the second (165 min later) were noted. The sand volume of each nest was estimated by comparing the filmed nests to photographed nests with measured volumes of sand using the same DV camera. The nest-opening width was calculated from markings on the front edge of the flowerpot.
Male behaviors used in the statistical analyses are the time the males spent (1) completely inside the nest, (2) with head visible in nest opening, (3) outside the nest, (4) fanning (with head visible in nest opening), and (5) displaying toward female (outside the nest); as well as the number of bouts the males performed (6) nest building from the inside of the nest, (7) nest building from the outside of the nest, and (8) rubbing the anal-urogenital area toward the ceiling inside the nest. The sand goby male prepares mucus trails by rubbing the anal-urogenital area (personal observation).
Comparing the first and the second recordings of males in the empty/empty treatment (n = 8), there was an order effect on displacement fanning (Wilcoxon matched-pairs test, z = 1.96, p = .050; first 151 ± 186 s, second 526 ± 554 s) and there tended to be one on mucus preparation as well (z = 1.68, p = .094; first 1.5 ± 1.7 times, second 2.8 ± 3.5 times), indicating habituation or an effect of the prolonged exposure to the female. However, we have controlled for this effect by randomizing the treatment order. All other behaviors showed no order effect (Wilcoxon matched-pairs test, time outside nest z = 1.26, p = .21; time completely inside nest z = 0.28, p = .78; total time displaying z = 0.17, p = .87; all bouts of nest building z = 1.07, p = .29).
To investigate whether male performance covaries across multiple traits that have been suggested to be cues for females in their mate choice, we used the films to quantify five such traits (nest-opening width, sand volume, male courtship display, displacement fanning, and male size). For fanning, both films from each replicate were used. Courtship display, however, we measured as display time during 5 min, starting when the male displayed for the first time. Of the two measurements of display in films one and two, we choose the highest to get each male's "personal best" record. Males that did not display at all were omitted. There was no difference in the 5 min of highest display between the three groups: sneaker/empty, empty/sneaker, and empty/empty (one-way ANOVA, F2,26 = 1.27, p = .30).
To confirm the existence of sperm in the mucus trails, two slides were attached inside the roof of a nest just before a confined female was released. When the male was observed to perform anal-urogenital rubbing toward the ceiling inside the nest, the two slides were exchanged for new ones (n = 3). When the female had spawned one to five eggs, the second set of slides was removed (n = 2). An artificial mucus trail was also created by gently moving the genital papilla of a euthanized male over a slide (n = 1). The mucus trails were protected with coverslips and observed under a light microscope (1000x).
Mating success experiment
To test if the presence of a sneaker male affects spawning decisions in the sand goby, a mating experiment was performed. The setup of the experiment also enables us to correlate nest attributes with female choice. Each 50-l aquarium (50 x 36 x 30 cm) was semidivided by an opaque screen, and a nest site was placed in each of the two compartments. The two nest sites were placed so that the males could not see each other from the nests (Figure 1B). To achieve as equal dominance relationships as possible, three males of the same size were released and were allowed to compete over the two nest sites. When both nests were built, the excess male that did not occupy a nest was removed. The next day it was noted if any nest had more sand on top than the other and if any of the nest openings was larger than the other. The nests were not experimentally manipulated. Thereafter, a vial with a sneaker male was placed in front of one of the nests, an empty vial was placed in front of the other, and a vial with a female was placed in the middle. One hour later the female was released. To see if the female was able to choose freely, the fish were observed during the first half hour and thereafter once every half hour until in most cases the female had spawned. Because no male chased the other male and because during spawning the nonspawning male paid very little attention to the spawning pair, female choice was likely to be fairly free. The next day, the presence of eggs in the nest was noted (N = 60).
Statistical analyses
In the first experiment, Wilcoxon matched-pairs tests were used when comparing the same males experiencing a sneaker male in a vial or not. However, due to the number of tests (k = 7), we corrected the p-values by sequential Bonferroni correction using the Dunn-Sidák method (Sokal and Rohlf, 1995) at 
-level .05 and .1. The correction severely reduces power, and therefore, we have refrained from doing tests on data with low sample sizes in either subsample. When correlating the five male traits with each other, we used a partial correlation. Before analysis, data on male length were (–1/x) transformed (two large males had to be excluded), nest-opening width and displacement fanning were cube root transformed, and the first 5 min of display were log transformed, whereas data on sand volume were untransformed. In the second experiment, binomial tests were used. All tests are two tailed. All means are given with ±SD.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Experiment 1: sperm competition risk and male behavior
In the pairwise analyses the nest-holding males spent more time completely inside their nests and performed mucus trail preparations by rubbing their anal-urogenital area toward the ceiling more often, when there was a sneaker male in the vial compared to when it was empty (Figure 2). However, time outside nest, total time displaying and fanning, did not differ between the treatments (Table 1). Most males constantly alternated between all or some of these activities. In addition, 11 out of 29 males attacked and tried to chase away the sneaker male in the vial. However, the amount of aggression was low (maximum of 14 attacks per 45 min).
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Nest building from the outside of the nest never changed the shape of the nest appearance markedly during the 90 min of filming. Yet, nest building from the inside sometimes decreased the width of the nest opening by up to 10 mm within seconds. However, the nest opening is very flexible and also increases, for example, when the male is swimming in and out of it trying to lead the female to the nest. Altogether 10 of 37 nest openings changed shape during the 165 min (increased, decreased, and also both), whereas the nest volume never changed. Three of 14 males with a sneaker male present during the first filming had decreased their nest openings 10 mm or more by the start of the second filming, while only 1 of 23 did so when they were alone (
2 = 2.63, p = .10, not significant after sequential Bonferroni correction at = .1). Combining the counts of nest building from the outside of the nest (sneak 2.1 ± 4.9 times, alone 5.0 ± 12 times) with nest building from the inside (sneak 0.48 ± 1.6 times, alone 0.89 ± 2.0 times), treatment had no effect (Table 1).
Nest appearance, male length, and courtship
Table 2 shows the result of the partial correlation on male length, display time during the first 5 min of displaying, fanning time, nest-opening width, and the volume of sand the nest consisted of. Of the 10 correlations, three are significantly positively correlated (and one tends to be so) and two are significantly negatively correlated with regard to how we may expect them to be preferred by females (Table 2).
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Sperm trails
In all six different sets of slides with mucus trails (from four males), both active sperm and inactive sperm were found. Active sperm were found both outside and within the mucus, inactive sperm only within.
Experiment 2: Sperm competition risk, nest appearance, and mating success
The females neither avoided nor preferred the male with a sneaker male close to his nest opening because 31 out of the 58 females that spawned in a single nest (two females spawned in both nests) did so in the nest next to the sneaker male (binomial test, p > .50).
Only including replicates in which the two nests a female could choose between differed; 10 out of 12 females spawned in the most well-covered nest (binomial test, p < .05). Among the best covered nests, eight nest openings were smaller, three were the same size, and one was larger than the opening of the less covered nests. In 25 aquaria the nest-opening width differed between the two nests. The females did not spawn more often in the nest with the smallest opening (14 out of 25 [8 out of 16 if those that also differed in coverage are deleted], binomial test, p > .50).
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DISCUSSION |
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The presence of a sneaker male affected the time the male spent inside his nest and the amount of mucus preparation but not male or female mating decision. Instead, males with larger volumes of sand over their nests had higher mating success. Males with well-covered nests also had small nest openings and showed much displacement fanning but little courtship display. The fact that all these traits may be related to male mating success suggests that individual males focus on a subset of traits for attracting females.
Sperm competition risk—the male perspective
In the male behavior experiment, the individual males increased their numbers of bouts of mucus trail preparations when they were exposed to a sneaker male. By observing mucus trails under a light microscope, we confirmed that they contain both active and inactive sperm, similar to what has been found previously for three other species of gobies (Marconato et al., 1996; Ota et al., 1996; Rasotto and Mazzoldi, 2002; Scaggiante et al., 1999). In these species the mucus trails have been documented to release sperm for hours, and hence, a role in sperm competition has been suggested. Thus, we find it very likely that the nest-holding males of the present study increased their mucus trail effort in the presence of sneaker males as a response to a perceived increase in sperm competition risk.
A possible alternative explanation of our result, however, is that the increased mucus preparation effort was a reaction to a perceived increase in mating competition from the small male. Yet, spawning G. niger males react with aggression but not with increased mucus preparation on foreign mucus trails (and they do not react at all on trails from sneaker males suggesting those to be chemically silent) (Locatello et al., 2002). Still, the mucus may contain sexual pheromones which attract females (Colombo et al., 1980). Consistent with this, the frequency of anal-urogenital rubbing in the grass goby, Zosterisessor ophiocephalus, has been shown to increase in the presence of females (Ota et al., 1996). The mucus may also protect the eggs from infection (Fishelson, 1991), and females may gain direct benefits from choosing a nest well prepared with mucus. In this context, it is also possible to hypothesize good gene or condition indicator mechanisms. However, if the main purpose of mucus trail preparation was to signal one or several of these traits to attract females, the males would have been expected to increase their courtship display and displacement fanning effort as well, which they did not. Furthermore, if there was a strong female preference for mucus-prepared nests, we would have predicted females in the mating success experiment to spawn most often in the nest next to the sneaker male (assuming that also these nest-holding males increased mucus preparation when exposed to sneakers), which they did not. Finally, if it was not for the fact that the males never once courted the sneaker males but instead were aggressive toward them, an alternative explanation of our result would have been that small males were regarded as females, so-called female mimics.
Males stayed completely inside their nest for a longer time when the sneaker males were present, but we have no reason to believe they were hiding. Firstly, males were engaged in as many less cryptic behaviors (fanning, being outside the nest, and displaying) when there was a sneaker male present compared to when there was not. Secondly, if males experiencing increased sperm competition risk were reluctant to spawn, we would have expected fewer spawnings in the presence of sneaker males in the mating success experiment, as found in the Mediterranean wrasse, Symphodus ocellatus (Alonzo and Warner, 1999), the three-spined stickleback, Gasterosteus aculeatus (Le Comber et al., 2003), and the common goby, Pomatoschistus microps (Magnhagen, 1998). Yet, this was clearly not the case in our study. However, in contrast to these species (Alonzo and Warner, 1999; Borg, 1985; Borg et al., 2002; Magnhagen, 1998; Rowland et al., 1991), sand goby males have been documented to mate with females rather unselectively (Kvarnemo and Forsgren, 2000) and females shown not to suffer any shortage of nest-holding males to choose among in the study area (Forsgren et al., 1996), suggesting that these males rarely face a situation when rejecting a spawning is beneficial, despite potential costs of sneaking.
In Svensson and Kvarnemo (2003), sand goby males built much smaller nest openings in the presence of sneaker males, suggesting that the nest opening may work as a defense or camouflage against sneaker males. However, we have found no behavioral or genetic support for this to be true (Svensson, 2004). Similarly, in the Azorean rock-pool blenny, Parablennius sanguinolentus parvicornis, nests in the field with associated satellite males did not have larger openings than nests without satellites. On the other hand, nests with two openings had an associate satellite male much more often than nests with one (Oliveira et al., 2002). In the present study, we hypothesized that males should be more engaged in nest building when experiencing a sneaker male compared to when not, which was not the case.
Sperm competition—the female perspective
In the mating success experiment, female spawning decisions seemed unaffected by the presence of sneaker males as similar numbers of females spawned in the nests with and without a sneaker male nearby. However, sand goby females might be predicted not to include the presence of sneaker males in their mate choice decision as it is hard to see any large benefit or cost of sneaking to them (except possibly disturbance, Svensson, 2004). Fertilization rate is close to 100% in the sand goby whether or not there are sneaker males present (personal observation). The pelagic larval stage (low philopatry) and huge population size (outbreeding population) make inbreeding avoidance and genetically variable offspring unlikely benefits. When sneaking occurs, the preferred nest-holding male still fertilizes the majority of her clutch (Malavasi et al., 2001; Svensson, 2004) and sand goby males do not increase their rate of filial cannibalism after sneak intrusion and fertilization (Svensson, 2004). Similarly, in the common goby, sneak intrusion had no effect on fanning, nest defense, or filial cannibalism (Svensson et al., 1998). Furthermore, due to the lack of female preference for sneaker males in the present study, we have presently no reason to believe that sneakers are of extraordinary genetic quality by having good or exclusive sneaker genes.
Mating success and mate choice cues
In the mating success experiment, the females spawned significantly more often in the nests covered by the most sand, whereas nest-opening width had no effect. A similar result has earlier been found in the common goby. In this case, females prefer to spawn in manipulated nests with a thick cover of sand and small nest openings, which were also discovered by egg predators less often (Jones and Reynolds, 1999). Even though the nests were not manipulated in our study, female choice based on sand cover makes sense. Nest building in Pomatoschistus is affected by body condition (Jackson et al., 2002; Kvarnemo et al., 1998) and dissolved oxygen (Lissåker et al., 2003), and by being costly, it fulfills some of the essential assumptions for being a sexually selected ornament (Kotiaho, 2001). Direct benefits by choosing well-covered nests include reduced adult predation by birds (Lindström and Ranta, 1992) and less filial cannibalism by egg-tending males (Kvarnemo et al., 1998). Sand cover may also be a more reliable estimate of male and nest quality than the highly variable nest-opening width, which may explain why male mating success was correlated with this one nest character but not with the other, even though the two were highly correlated.
Nest cover may very well covary with preferred traits. In the partial correlation on sand volume of the nest, nest-opening width, male length, displacement fanning during 90 min (no eggs in the nest), and the first 5 min of courtship display in the male behavior experiment, sand volume of the nest was positively correlated with displacement fanning but negatively correlated with display. Therefore, it is possible that displacement fanning (not measured in the mating success experiment) was the preferred trait rather than nest cover per se. The five traits correlated both positively and negatively with regard to what we expect females to prefer. Furthermore, males that fanned well also built large nests or displayed intensely (but not both). This result suggests trade-offs between different traits and that, rather than being jacks-of-all-trades, individual males focus on a subset of traits for attracting females. Possibly males are able to evaluate their own qualities and then use their best means to court the females, resulting in different courtship tactics. For example, small males displayed more, a negative correlation between male size and courtship that is found in other studies as well (Magnhagen, 1998; Reynolds, 1993). The many different criteria used by females in mate choice may provide different information, for example, about male condition, forthcoming care, or indirect genetic benefits. They may also function serially, as in the bitterling, Rhodeus sericeus, in which the initial decision by the female is based on male behavior and color, whereas the final decision is taken after inspection of the mussel in which the female places the eggs (Candolin and Reynolds, 2001). In our study, we had no or low level of male-male competition and did not measure any aspects of male breeding coloration. Therefore, it is likely that the inclusion of these factors would change the picture (Candolin, 2000) but not lessen the importance of our current findings.
In birds, traits associated with good genes and those associated with paternal care are not necessarily the same (Møller and Jennions, 2001; Soler et al., 1998a). In the sand goby, females do not invite sneaker males to sneak (Svensson, 2004), and they probably have no control over parasitic fertilizations. Therefore, in contrast to many birds, indirect benefits such as good genes or genetic compatibility have to be provided by the same individual as the direct benefits. This abolishes the potential intersexual conflict between females and nest-holding males over simultaneous parasitic spawnings.
To summarize, our main findings are that male mating success or female mating decision were not affected by the presence of sneaker males and that males showed higher mucus preparation effort inside the nest in the presence of a sneaker male than when alone, while visually spectacular behaviors such as courtship, nest building, and displacement fanning were unaffected. The mucus contains sperm, suggesting an importance in sperm competition. Interestingly, the volume of sand that males put on their nests was positively associated with female spawning decision, while nest-opening width was not. In the partial correlation, male traits were intercorrelated both positively and negatively with regard to how we may expect them to be preferred by females. Therefore, if only one of the traits is measured, there is a risk of drawing the wrong conclusions about male attractiveness.
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ACKNOWLEDGEMENTS |
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We thank Sigal Balshine, Bertil Borg, Ulrika Candolin, Jonathan Ready, Marlene Zuk, and two anonymous referees for valuable comments on the manuscript. We also thank Kristina Axelson, Laila Fröberg, Lotta Laurent, Maria Lissåker, and Daniel Simonsson for providing help in the field. Financial support was given by the Smitts Foundation (to O.S.) and the Swedish Research Council (to C.K.). A special gratitude goes to the friendly staff at Klubban Biological Station and Kristineberg Marine Research Station.
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