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Behavioral Ecology Vol. 14 No. 1: 63-67
© 2003 International Society for Behavioral Ecology
Tests of the mate-guarding hypothesis for social monogamy: male snapping shrimp prefer to associate with high-value females
Department of Biology, University of Louisiana at Lafayette, Lafayette, LA 70504, USA
Address correspondence to L.M. Mathews, who is now at the Department of Medicine, Division of Molecular Medicine, Columbia University, 630 West 168th Street, New York, NY 10032, USA. E-mail: lm2023{at}columbia.edu.
Received 28 July 2001; revised 19 March 2002; accepted 17 April 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Social monogamy without biparental care has evolved in many taxa, and a number of hypotheses have been developed to explain this phenomenon. Several authors have suggested the importance of male mate-guarding behavior in the evolution of social monogamy, although empirical support for this hypothesis is lacking. In the caridean shrimp genus Alpheus, social monogamy may result from selection on males for long-term guarding of females because mating is temporally restricted to a short time after the female's molt. I used Alpheus angulatus to test two predictions of the extended mate-guarding hypothesis: Males should (1) be physiologically capable of predicting the timing of female sexual receptivity, and (2) prefer to associate with (guard) females that are closer to sexual receptivity. Data from a Y-maze experiment testing for distance chemical communication showed that males of A. angulatus were attracted to water treated by exposure to premolt females, repulsed by water treated by exposure to intermolt males and females, and did not appear to respond in either direction to water treated by exposure to premolt males. In mate choice experiments, significantly more males paired with premolt females than with postmolt females. These data suggest that males of A. angulatus engage in precopulatory mate-guarding behavior. Other factors (population density, sex ratio) may have played a role in the temporal extension of mate guarding to social monogamy.
Key words: Alpheus, mate guarding, snapping shrimp, social monogamy.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The phenomenon of social monogamy has presented a dilemma for evolutionary ecologists. Parental investment theory (Trivers, 1972
) predicts monogamous associations to be rare, as at least one sex is likely to benefit by being polygamous. Fitness benefits through shared parental care are thought to contribute to the evolution of partner-exclusive behavior (e.g., mammals: Kleiman, 1977; birds: Lack, 1968), but social monogamy has evolved in the absence of biparental care in some mammals (Brotherton and Manser, 1997; Kishimoto and Kawamichi, 1996), coral reef fishes (Reavis and Barlow, 1998; Roberts and Ormond, 1992), decapod crustaceans (Huber, 1987; Johnson, 1969; Nolan and Salmon, 1970; Seibt and Wickler, 1979), and reptiles and amphibians (Bull et al., 1998; Gillette et al., 2000).
For these taxa, at least two hypotheses for the evolution of social monogamy are applicable: the territorial cooperation and the extended mate-guarding hypotheses. Hixon (1987) and Brown (1982) suggested that the evolution of social behavior may often be correlated to territoriality, and the majority of socially monogamous taxa are also territorial (see Mathews, 2002a), suggesting that individuals in pairs may benefit by sharing territorial maintenance (Fricke, 1986; Takegaki and Nakazono, 1999).
Selection for male mate guarding of females may play a role in the evolution of social monogamy (Brotherton and Manser, 1997; Bull et al., 1998; Reavis and Barlow, 1998; Seibt and Wickler, 1979), although, to my knowledge, direct experimental evidence is lacking. Male mate guarding is predicted to evolve whenever the guarding sex benefits by restricting a mate or potential mate's access to other opposite-sex conspecifics, and it may lead to pairing relationships if males are unable to monopolize multiple females at one time because of female–female aggression (Brotherton and Manser, 1997; Gillette et al., 2000) or female dispersion (Herold and Clark, 1993; Seibt and Wickler, 1979). Furthermore, pairing relationships may be extended in time if males are under selection to guard females for long periods before,during, and/or after female sexual receptivity (the extended mate-guarding hypothesis), resulting in females being guarded throughout their reproductive cycles. Such selection could result from physiological factors, such as cryptic orconcealed ovulation (Burley, 1979), ecological factors thatincrease a male's search time per female (Parker, 1974), such as low population densities (Wickler and Seibt, 1981) or a male-biased sex ratio (Grafen and Ridley, 1983), or behavioral factors, such as a high cost of initial pairing interactions in a highly aggressive taxon.
Social monogamy in the caridean shrimp genus Alpheus (snapping shrimp) may be a result of selection for territorial cooperation between partners (Mathews, 2002a), selection for extended male mate guarding of females, or both. Social monogamy is characteristic of the highly speciose genus Alpheus (Knowlton, 1980; Nolan and Salmon, 1970; Schein, 1975), and also occurs in the closely related genus Synalpheus, for which it may be the ancestral condition leading to more complex assemblages, including eusociality (Duffy, 1992, 1996). I have used A. angulatus, a species that occurs in constructed burrows in shallow subtidal and intertidal rubble habitats in the subtropical northwestern Atlantic, as a model for the genus. Snapping shrimp are territorial, with male and female partners codefending a constructed burrow from intruders (Knowlton, 1980; Knowlton and Keller, 1982; Schein, 1975). Previous research has shown that paired females are significantly less likely to be evicted from a burrow by conspecific females than are solitary females (Mathews, 2002a); therefore, the benefits of territorial cooperation may have contributed to the evolution of socially monogamous behavior in females. However, males of A. angulatus do not appear to benefit from territorial cooperation as females do. Though paired males were less likely to be evicted by conspecific males than were solitary males, this difference was not statistically significant (Mathews, 2002a). Although other factors related to territoriality may have shaped social evolution in this group (i.e., burrow construction and maintenance; Mathews, 2002a), it is prudent to consider the potential influence of female reproductive physiology, which can potentially select for pre- and/or postcopulatory mate guarding, on male behavior.
Snapping shrimp are likely candidates for extended mate-guarding social monogamy. The evolution of social monogamy as a form of extended mate guarding is a two-step evolutionary process: first, the evolution of mate-guarding behavior in males and second, the temporal extension of male mate guarding to encompass females' entire reproductive periods. The models of Grafen and Ridley (1983) predicted the evolution of male precopulatory mate guarding for crustacean taxa in which mating is restricted to a short period of female receptivity after the female molt, as is the case for caridean shrimp (Nelson, 1991). Any male that predicted the timing of female receptivity and selectively guarded prereceptive females would have higher copulation rates than nonguarding males. The mate-guarding hypothesis predicts (1) that males should be physiologically capable of predicting female sexual receptivity and (2) that they should use this ability to pair selectively with (guard) females that are relatively closer to sexual receptivity. Here I report results of my tests of these two predictions.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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I collected individuals of A. angulatus in a rubble intertidal habitat in Fort Pierce Inlet, Fort Pierce, Florida, USA, in the summers of 1999 and 2000 by digging 20–30 cm into the substrate and removing pairs (<5 cm apart) or single individuals by hand. Test shrimp were measured (carapace length and major chela length), sexed, and housed individually or in pairs as collected, before use in an experiment. At the Smithsonian Marine Station in Fort Pierce (SMSFP), I maintained shrimp in a recirculating seawater system at 24°C, 32–34 parts per thousand, and a natural day : night cycle. At The University of Louisiana at Lafayette (UL), I maintained shrimp in the Department of Biology's aquatics laboratory at 24°C, 32–34 parts per thousand, and a 14 : 10 h day:night cycle in recirculating seawater tables. I fed shrimp daily a diet of commercial shrimp pellets (Wardley) or homemade omnivore food (chicken livers, penaeid shrimp, catfish, spinach, carrots, and gelatin). For all experiments, I used natural seawater transported from offshore sites in Florida (SMSFP) or the Gulf of Mexico (UL).
Y-maze experiment for chemical communication of sexual status
To test for distance communication of sexual status, I used a Y-maze experimental design with a clear glass tube as a test chamber (Figure 1). The two forward arms of the test chamber were connected to two elevated water sources (source containers) with plastic aquarium tubing (6-mm diam). Water flowed from the source containers into the forward arms of the test chamber, mixed in the center of the chamber, and flowed out the outflow arm. During trials, I controlled flow rate at approximately 7 l/10-min trial period. Pilot runs with water colored with commercial food coloring showed that, at this flow rate, water from the two source arms mixed in the center of the tube, but water in the two forward arms remained unmixed (Figure 1). Stopcocks on both lengths of connecting tubes prevented water flow during acclimation periods and regulated flow rates during testing.
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Before each trial, I rinsed the two source containers for 5min with tapwater and then twice with small volumes of untreated, filtered seawater (this procedure hereafter referred to as "cleaning"). Then, I filled the test chamber with untreated, filtered seawater and placed a male test shrimp inside to explore the Y-maze undisturbed for 10 min, after which I released the stopcocks and recorded the position of the test shrimp for 12 min. I considered the first 2 min of data as acclimation to flow and did not include them in the analyses. The test shrimp entered a region of the chamber whenever its eyes crossed a line drawn on the arms of the tube that delineated regions of the chamber (Figure 1). After the 10-min trial period, I removed the test male and cleaned (as above) the test chamber, connecting tubes, and source containers. I tested each male once, although I used some test males in the preparation of treatment water.
I prepared source water for each trial by placing a treatment shrimp into a clean bucket with approximately 10 l of filtered natural seawater and a clean cover object for 24 h. Then, I transferred the treatment water to one of the two clean source chambers. I filled the other source chamber with approximately 10 l of control water, which was treated in the same way as treatment water except that no treatment shrimp was added. I switched the position (left or right) of the treatment water between each trial to control for any side preferences. There were seven treatments in this experiment (Table 1). A premolt treatment shrimp had molted within 3 days after being used in the preparation of treatment water; an intermolt treatment shrimp had not molted 3 days before or 7 days after being used in the preparation of treatment water; and a molted treatment shrimp had molted in the treatment water during the 24-h preparation period. In all trials, the treatment shrimp and test shrimp were not partners.
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For all treatment types, I presented test males with a choice between water treated by a male or female conspecific and control water, such that their behavior could be interpreted as attraction to or repulsion from a stimulus. For each trial, I calculated total time in seconds spent in the treatment water arm minus the total time spent in the control water arm. For the control treatment (untreated water in both arms), the time for one forward arm was randomly assigned to be subtracted from the time for the other. Time spent in the outflow arm and time in the central portion of the test chamber were considered time in neutral area.
I performed approximately half of the replicates in each treatment group at SMSFP (summer 1999). I performed the other half at UL (summer 2000) using shrimp that had been collected at SMSFP, with an identical experimental design, pooling data for analyses. The data were non-normally distributed and thus were analyzed with a randomization procedure (Adams and Anthony, 1996), using the SAS program (SAS Institute, 1989) that was employed by Gillette et al. (2000). This program calculated an artificial mean value for each treatment by multiplying each value in a treatment group randomly by 1 or –1. This artificial mean was calculated to approximate what the observed mean would be if the shrimp were behaving randomly toward source waters. A large number (n = 6000 iterations) of these artificial means was generated, and then these means were compared to the observed mean of that treatment group. The p value for each treatment is then the percentage of randomly generated means that was larger than a positive observed mean or smaller than a negative observed mean.
Time spent in neutral areas of the test chamber and data from all trials in which males were unresponsive (i.e., no movement for the entire test period) were excluded from randomization analyses. I analyzed for differences between treatments in the time males spent in areas of the chamber defined as neutral with a Kruskal-Wallis one-way ANOVA (Siegel and Castellan, 1988) and for differences between treatments in the number of trials in which males were unresponsive with a chi-square goodness-of-fit test. For all statistical tests, I set 
= 0.05.
Mate choice experiment
To determine if males prefer to pair with females relatively closer to sexual receptivity, I performed a laboratory mate-choice experiment at UL in the summer of 2000. I prepared test chambers (38 x 25 x 13 cm) in seawater tables with two artificial burrows (200 ml clear plastic containers) sunk into a 10-cm deep layer of cleaned, crushed oyster shells. I placed two female shrimp, size matched to within 0.5 mm carapace length, into each test chamber and allowed them to acclimate for 24 h. In each trial, one of the two females was a ``high-value,'' premolt female, and the other was a ``low-value,'' postmolt female. Females with no brooding embryos and highly developed ovaries were categorized as premolt; these females molted and were sexually receptive 1–3 days after being used in a trial. Females brooding embryos in the two- to four-cell stage and with little or no ovarian development were categorized as postmolt; these females had molted and mated 2–4 days before being used in an experiment (total molt cycle = 21–24 days, unpublished data). After the 24-h acclimation period, I added a single, size-matched, unfamiliar male to the chamber. I recorded the positions of all three shrimp after 24h, judging that the male had paired with a female if he wasresiding in a burrow with a female at the end of the test period. Because snapping shrimp are rarely outside their burrows during the day (Mathews, personal observation), the daytime positions of the three test shrimp represent pairing relationships among them. The data were analyzed for statistical significance with a one-tailed binomial test with = 0.05.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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In the Y-maze experiment, males spent significantly less time in water treated by intermolt male or female conspecifics than in control water, but significantly more time in water treated by premolt females than in control water (Table 1, Figure 2). There were no significant differences in the time that males spent in water treated by premolt males or molted males or females and control water. There was also no significant difference among treatments in the amount of time males spent in neutral areas of the test chamber (Kruskal-Wallis = 12.22, 6 df, p >.05). Test males were unresponsive in 36 trials (total n = 247 trials), and there was no significant difference among treatments in the number of trials in which males were unresponsive (
2 = 2.17, 6 df, p >.90).
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Out of 55 trials in the mate choice experiment, males paired with premolt females 26 times, postmolt females 12 times, and did not pair with either female 8 times. In another nine trials, the premolt female molted during the trial; these were not included in the analyses. In all trials in which the male did not pair with either female, one female was evicted from her burrow by the male, who then established residence in the burrow. Significantly more males paired with premolt females than with postmolt females (z = 2.11, p =.0174).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Males of A. angulatus may engage in precopulatory mate guarding; they were attracted by chemical signals to premolt females, and they preferred to pair with females closer to sexual receptivity when offered a choice. Similar behavior has been reported in other crustaceans for which male mate-guarding behavior has been documented. Gleeson (1980
, 1991) reported that males of Callinectes sapidus perform courtship behavior in response to water treated by prepubertal females, but not in response to water treated by postreceptive females or males. Kelly et al. (1998) reported evidence that males of Tigriopus japonicus assess female sexual receptivity with a contact pheromone and prefer to associate with more developmentally advanced females. Borowsky and Borowsky (1987) also reported a contact pheromone communicating female receptivity to males in the mate-guarding amphipod Gammarus palustris.
Dunham (1978, 1988) pointed out that female chemical cues that elicit male responses do not necessarily function as sex pheromones. For example, males might respond to female cues as cannibalistic predators toward potential prey. However, my data on A. angulatus suggest that males responding to chemical cues from female conspecifics treat them as signals from potential mates. Because males were significantly attracted to premolt females and were not significantly attracted to premolt males, female chemical cues were probably eliciting mate-searching behavior, rather than cannibalistic foraging behavior.
However, males did respond differently to premolt males than they did to intermolt males. Males were repulsed by water from intermolt males, but I found no evidence that males were either repulsed by or attracted to water from premolt males. Because males responded differently to premolt males than to either premolt females or intermolt males, this suggests that males use different chemical cues to gather information about a conspecific's gender and molt status, showing negative responses to male signals, but positive responses to premolt signals. The significant negative response that males showed toward signals from intermolt conspecifics of either gender is consistent with high initial levels of aggression between unfamiliar shrimp (Schein, 1975, 1977), which escalates or results in escape behavior by one shrimp in intrasexual encounters (Knowlton and Keller, 1982) and gives way to pairing behavior in intersexual encounters (Nolan and Salmon, 1970).
In my Y-maze experiment, males were not significantly attracted to or repulsed by molted conspecifics of either sex. Upon physically contacting a molted female, males respond by increasing general activity, repeatedly contacting the female with antennae and antennules, and mating with the female, usually within several minutes of first contact (Mathews, personal observation). This suggests the presence of a contact chemical by which males assess females' immediate sexual receptivity, as reported by Bauer (1979) for another caridean shrimp, Heptacarpus paludicola.
Data from the mate choice experiment demonstrate that chemical communication of female molt stage may be translated into mate choice decisions by males. However, the design of this experiment did not control for other potentially interacting factors, particularly the influence of female behavior on pairing. There are no obvious differences in the behavior of intermolt and premolt females, and males appear to pair at equal rates with intermolt and premolt females when not offered a choice between multiple females (i.e., male encounters a single female in a test chamber; unpublished data). However, the possibility that female behavior may influence male pairing decisions cannot be discounted and therefore the proximate mechanism by which males make pairing decisions cannot be determined through this experiment. Yet the ultimate effect of pairing with premolt females over intermolt females is an increase in male fitness, regardless of the mechanism males use to evaluate female receptivity.
Although male preferences for prereceptive females have been demonstrated in a number of crustacean taxa (Borowsky and Borowsky, 1987; Gleeson, 1980, 1991; Kelly et al., 1998), these data for A. angulatus are unique for two reasons. First, this is the first reported demonstration of distance communication of sexual status in a caridean shrimp. Second, this is the first empirical support for the hypothesis that social monogamy may evolve at least in part as a result of selection on one sex for engaging in mate-guarding behavior. Further experimentation to examine factors that may have contributed to the temporal extension of mate guarding to social monogamy suggest a possible role for operational sex ratio in male pairing behavior (Mathews, 2002b).
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ACKNOWLEDGEMENTS |
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I thank M. Rice and the staff of the Smithsonian Marine Station in Fort Pierce, Florida, for logistic support, and R. T. Bauer and R. G. Jaeger for advice and comments on an earlier version of this manuscript. This research was funded by Louisiana Board of Regents Doctoral Fellowship grant LEQSF(1996–01)-GF-30 through R. G. Jaeger; Link Foundation/Smithsonian Institution Graduate Student Fellowships, 1998 and 1999; American Museum of Natural History Lerner-Gray Fund grants, 1998 and 1999; and a Sigma Xi Grant-in-Aid of Research, 1998. This is Smithsonian Marine Station at Fort Pierce contribution no. 520, and contribution no. 82 of the Laboratory for Crustacean Research.
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