ELSEVIER
Behavioural
Processes 36 (1996) 99- 102
Short Report ‘
Copying mate choice’: Which phenomena deserve this term? Sarah ELM. Kraak Zoological
Laboratory,
University
of Groningen,
’
P.O. Box 14.9750
AA Haren,
The Netherlands
Accepted 2 March 1995
Keywords:
Copying mate choice; Proximate/ultimate
causes
Recently several theoretical and empirical studies have been published on ‘female mate choice 1990; Dugatkin, 1992; Gibson and Hbglund, copying’ (Losey et al., 1986; Wade and Pruett-Jones,
1992; Pruett-Jones, 1992; Goldschmidt et al., 1993; Kirkpatrick and Dugatkin, 1994). A common interpretation of this phenomenon is that some variation in male quality exists in a population, and at least some females are able to discriminate and choose the higher quality males. Other females avoid the cost of assessing these quality differences, and rely on choices made by the former: they copy other females’ mate choice. This copying behaviour may play an important role in sexual selection (Losey et al., 1986; Wade and Pruett-Jones, 1990; Gibson and Hiiglund, 1992; Pruett-Jones, 1992; Kirkpatrick and Dugatkin, 1994). Although Pruett-Jones (1992) intended to clarify the definition of female copying because of the confusion existing in the literature, my purpose here is to identify situations where confusion still occurs and to suggest when the term ‘copying’ should and should not be applied. This is not a mere semantic discussion. Instead, I believe that future research will benefit if the distinction between separate behavioural phenomena and their underlying proximate and ultimate causes is not blurred by inaccurate terminology. My discussion concerns a phenomenon in fish that is commonly cited in relation to female copying: in many fish with male parental care, females prefer to spawn with males that already have eggs in their nest (e.g. Ridley and Rechten, 1981; Marconato and Bisazza, 1986; Unger and Sargent, 1988; Knapp and Sargent, 1989; Kraak and Videler, 1991; Goldschmidt et al., 1993). My first point concerns the definition of ‘copying’. Losey et al. (1986, page 653) stated that “for copying to exist, females must be able to observe other females’ mating choices.” Pruett-Jones ( 1992, page 1002) elaborated on this by stating that we should refer to copying “if it is the action, and not
’ Present Switzerland.
address:
Abteilung
VerhaltenGkologie,
Universitit
0376-6357/96/$15.00 0 1996 Elsevier Science B.V. All rights reserved SSDI 0376-6357(95)00020-S
Bern,
Wohlenstrasse
50a, CH-3032
Hinterkappelen,
loo
S.B.M. Kruuk/
Behouiourol
Proce.we.~ 36 (1996) 99-102
the consequence, of the choice of one female that influences the decision of another female.” For example, “if, after mating, a male’s behaviour changes (e.g. he displays more vigorously or guards eggs more carefully) and he becomes more ‘attractive’ to successively choosing females, then the absolute probability of choice of this male by females may increase, but this is not an example of copying”. So far, I agree with Pruett-Jones. It is inconsistent, however, that Pruett-Jones (1992, page 1003) also includes cases in which females base their choice on “physical evidence of mating (e.g. eggs) remaining in the territories of mated males” under his definition of copying. The presence of eggs is clearly a consequence, and not the action, of a female’s choice. The presence of eggs is comparable to changed male behaviour: both are consequences of mating, by which the attractiveness of a male may have increased. Therefore, if we follow Pruett-Jones’ reasoning (of page 1002) consistently, females that base their choice on the presence of eggs are not copying. Pruett-Jones is not the only one who refers to females preferring nests with eggs as copying, Gibson and Hiiglund (1992, page 230) do so as well. Goldschmidt et al. (1993) also conclude from their study that female sticklebacks base their choice on the presence of eggs in the nest, and call this copying. I prefer the definition of the phenomenon copying sensu strictu that Dugatkin (1992) uses. Copying should refer exclusively to the situation in which the female bases her choice of mate on her direct observation of the action of other females mating with a particular male, as observed by Dugatkin (1992). In none of the studies in which females were more likely to spawn in nests containing eggs (including Goldschmidt et al., 1993) has the phenomenon of copying sensu strictu been studied. A second source of confusion in the literature on female copying is that the cue on which females base their choice and the benefit that females may gain from making this choice (i.e. proximate and ultimate causes, the ‘how’ and the ‘why’) are sometimes mixed up. In the case of female preference for males with eggs, a number of cues and functions can be distinguished. Possible cues which may trigger the female’s decision are: (1) her observation of increased male courtship display, (2) her observation of increased male parental behaviour, (3) her observation of a certain number of eggs present in the nest, (4) her observation of other females in the act of mating (i.e. copying sensu strictu). The adaptive significance or function, i.e. the selective advantage of this preference (based on any of these cues), may be: (I) dilution of the risk of predation or cannibalism with increasing brood size (Rohwer, 1978), (II) increased paternal care with larger broods (Sargent, 1988), (III) increased chance of choosing a male of good parental quality (the eggs are proof of the male’s ability to care for them so far) (Ridley, 1978), (IV) increased chance of choosing a male that has been attractive to other females (the eggs are proof that the male has already attracted females) (Ridley, 1978). These possible benefits are not mutually exclusive. By all four effects female fitness may be enhanced through better chances of survival of her eggs in the nest. The last two effects (III and IV) may constitute a benefit if such apparently attractive males produce offspring of good genetic quality or ‘sexy sons’. It is important to note that in theory, any of the four benefits (I-IV) could accrue to females choosing males based on any of the four cues (l-4). The last benefit (IV), i.e. the increased chance of picking a male that has been attractive to other females, is most commonly discussed in relation to copying 1 son and Hoglund, 1992; Pruett-Jones, 1992). However, the term ‘copying’ (Losey et al., 1986; G’b sensu strictu refers to the cue on which females base their mate choice, i.e. the observation of other females mating with a particular male (4). Sometimes proximate and ultimate causes are treated as if they are alternative explanations. For example, Pruett-Jones (1992, page 1004) states that “Preference by females for males with eggs could result from copying, changes in male display or parental-care behaviour, or a reduction in the risk of
S.B.M. Kruuk/
Behaviourul
Processrs
36 (1996) 99-102
101
predation with increasing clutch size”. This is incorrect because copying and changes in display refer to the cues that females use for choosing particular males (4 and 1 respectively). On the other hand, reduction of predation risk refers to the benefit that females may gain from such a preference (I). Changes in paternal care may refer to both the cue that females use as well as the benefit that females gain (2 and II respectively). Dugatkin (1992) also mixes proximate and ultimate causes when he refers to female fish preferring males that are already guarding eggs (page 1387): “these results are ambiguous with respect to copying behaviour, as females may prefer nests with eggs because this ‘dilutes’ the risk of predation”. While Dugatkin’s own experiments focus entirely on the proximate mechanism, his argument here is based on ultimate causes. It is important that studies of the mechanism controlling a behaviour and the function of that behaviour go hand in hand, but one must remember that they are separate questions. Mixing up of the two creates confusion. My last point concerns the discussion of the adaptive significance of copying. In the theoretical models of copying (Losey et al., 1986; Wade and Pruett-Jones, 1990; Pruett-Jones, 1992) the authors refer to a fitness benefit which comes about because copying females are likely to mate with males whose good quality has been assessed by other females (IV). These models investigate whether copying can be an evolutionary stable strategy by this benefit alone. Other benefits, such as a higher hatching success of eggs laid in a nest that already contains eggs, independent of the male’s inherent quality, (I and II), do not play a role in their models. In theory this could apply to situations where the females copy sensu strictu as well as to situations where the females base their choice on any indirect evidence of other females’ choices. However, one of the assumptions made in these models is that choosing a mate is costly and copying is not (Losey et al., 1986; Wade and Pruett-Jones, 1990; Pruett-Jones, 1992): choosing females have costs when they are assessing male quality, which copying females do not have because they rely on the assessment made by other females, Obviously, this assumption does not hold in cases in which females base their choice on the number of eggs present in the nest. Field studies (Gronell, 1989; Kraak and Videler, 1991; Goldschmidt et al., 1993) suggest that visiting nests in order to check whether or not eggs are present, costs as much as assessing male quality on the basis of physical or behavioural traits of the male. In either case, females spend time searching, visiting, and assessing males or nests. When a female visits a nest, a behavioural interaction occurs during which male traits can be judged by the female as well. Hence, the theoretical models on the evolutionary stability of copying are inappropriate in this case. In summary, I want to suggest that the term ‘copying’ be used more carefully. The term sensu strictu refers to the phenomenon that females base their choice on what they have observed other females doing. This is a proximate mechanism. The adaptive significance and evolutionary consequences of this and related phenomena should be investigated as a separate question. Furthermore, one must bear in mind that the models on the evolutionary stability of copying assume that copying females avoid the cost of choosing, which is not the case when females make their choice after having checked the contents of the nest.
Acknowledgements I want to acknowledge Dr. J.P. Kruijt and Dr. Ton Groothuis, who helped me think clearly about this matter. The manuscript has also benefitted from the comments of anonymous referees.
102
S.B.M. Krauk/
Brhaoioural
Processes 36 (1996) 99-102
References Dugatkin, L.A., 1992. Sexual selection and imitation: females copy the mate choice of others. Am. Nat. 139: 1384-1389. Gibson, R.M. and Hiiglund, J., 1992. Copying and sexual selection. TREE 7: 229-231. Goldschmidt, T., Bakker, T.C.M. and Feuth-de Bruijn, E., 1993. Selective copying in mate choice of female sticklebacks. Anim. Behav. 45: 541-547. Gronell, A.M., 1989. Visiting behaviour by females of the sexually dichromatic damselfish, Chrypsipreru cyanea (Teleostei: Pomacentridae): a probable method of assessing male quality. Ethology 8 1: 89- 122. Kirkpatrick, M. and Dugatkin, L.A., 1994. Sexual selection and the evolutionary effects of copying mate choice. Behav. Ecol. Sociobiol. 34: 443-449. Knapp, R.A. and Sargent, R.C., 1989. Egg mimicry as a mating strategy in the fantail darter, Ethiostomaflabelfare: females prefer males with eggs. Behav. Ecol. Sociobiol. 25: 321-326. Kraak, S.B.M. and Videler, J.J., 1991. Mate choice in Aidablennius sphynx (Teleostei, Blenniidae); females prefer nests containing more eggs. Behaviour 119: 243-266. Losey, G.S., Stanton, F.G., Telecky, T.M., Tyler, W.A., III and the Zoology 691 Graduate Seminar Class, 1986. Copying others, an evolutionarily stable strategy for mate choice: a model. Am. Nat. 128: 653-664. Marconato, A. and Bisazza, A., 1986. Males whose nests contain eggs are preferred by female Cottus gobio L. (Pisces, Cottidae). Anim. Behav. 34: 1580-1582. Pruett-Jones, S., 1992. Independent versus nonindependent mate choice: do females copy eachother?. Am. Nat. 140: 1000-1009. Ridley, M., 1978. Paternal care. Anim. Behav. 26: 904-932. Ridley, M. and Rechten, C., 198 1. Female sticklebacks prefer to spawn with males whose nests contain eggs. Behaviour 76: 152-161. Rohwer, S., 1978. Parental cannibalism of offspring and egg raiding as a courtship strategy. Am. Nat. 112: 429-440. Sargent, R.C., 1988. Paternal care and egg survival both increase with clutch size in the fathead minnow, Pimephales promelas. Behav. Ecol. Sociobiol. 23: 33-37. Unger, L.M. and Sargent, R.C., 1988, Allopatemal care in the fathead minnow, Pimephales promefas: females prefer males with eggs. Behav. Ecol. Sociobiol. 23: 27-32. Wade, M.J. and Pruett-Jones, S.G., 1990. Female copying increases the variance in male mating success. Proc. Nat]. Acad. Sci. USA 87: 5749-5753.
Behavioural
Processes 36 (1996) 99- 102
Short Report ‘
Copying mate choice’: Which phenomena deserve this term? Sarah ELM. Kraak Zoological
Laboratory,
University
of Groningen,
’
P.O. Box 14.9750
AA Haren,
The Netherlands
Accepted 2 March 1995
Keywords:
Copying mate choice; Proximate/ultimate
causes
Recently several theoretical and empirical studies have been published on ‘female mate choice 1990; Dugatkin, 1992; Gibson and Hbglund, copying’ (Losey et al., 1986; Wade and Pruett-Jones,
1992; Pruett-Jones, 1992; Goldschmidt et al., 1993; Kirkpatrick and Dugatkin, 1994). A common interpretation of this phenomenon is that some variation in male quality exists in a population, and at least some females are able to discriminate and choose the higher quality males. Other females avoid the cost of assessing these quality differences, and rely on choices made by the former: they copy other females’ mate choice. This copying behaviour may play an important role in sexual selection (Losey et al., 1986; Wade and Pruett-Jones, 1990; Gibson and Hiiglund, 1992; Pruett-Jones, 1992; Kirkpatrick and Dugatkin, 1994). Although Pruett-Jones (1992) intended to clarify the definition of female copying because of the confusion existing in the literature, my purpose here is to identify situations where confusion still occurs and to suggest when the term ‘copying’ should and should not be applied. This is not a mere semantic discussion. Instead, I believe that future research will benefit if the distinction between separate behavioural phenomena and their underlying proximate and ultimate causes is not blurred by inaccurate terminology. My discussion concerns a phenomenon in fish that is commonly cited in relation to female copying: in many fish with male parental care, females prefer to spawn with males that already have eggs in their nest (e.g. Ridley and Rechten, 1981; Marconato and Bisazza, 1986; Unger and Sargent, 1988; Knapp and Sargent, 1989; Kraak and Videler, 1991; Goldschmidt et al., 1993). My first point concerns the definition of ‘copying’. Losey et al. (1986, page 653) stated that “for copying to exist, females must be able to observe other females’ mating choices.” Pruett-Jones ( 1992, page 1002) elaborated on this by stating that we should refer to copying “if it is the action, and not
’ Present Switzerland.
address:
Abteilung
VerhaltenGkologie,
Universitit
0376-6357/96/$15.00 0 1996 Elsevier Science B.V. All rights reserved SSDI 0376-6357(95)00020-S
Bern,
Wohlenstrasse
50a, CH-3032
Hinterkappelen,
loo
S.B.M. Kruuk/
Behouiourol
Proce.we.~ 36 (1996) 99-102
the consequence, of the choice of one female that influences the decision of another female.” For example, “if, after mating, a male’s behaviour changes (e.g. he displays more vigorously or guards eggs more carefully) and he becomes more ‘attractive’ to successively choosing females, then the absolute probability of choice of this male by females may increase, but this is not an example of copying”. So far, I agree with Pruett-Jones. It is inconsistent, however, that Pruett-Jones (1992, page 1003) also includes cases in which females base their choice on “physical evidence of mating (e.g. eggs) remaining in the territories of mated males” under his definition of copying. The presence of eggs is clearly a consequence, and not the action, of a female’s choice. The presence of eggs is comparable to changed male behaviour: both are consequences of mating, by which the attractiveness of a male may have increased. Therefore, if we follow Pruett-Jones’ reasoning (of page 1002) consistently, females that base their choice on the presence of eggs are not copying. Pruett-Jones is not the only one who refers to females preferring nests with eggs as copying, Gibson and Hiiglund (1992, page 230) do so as well. Goldschmidt et al. (1993) also conclude from their study that female sticklebacks base their choice on the presence of eggs in the nest, and call this copying. I prefer the definition of the phenomenon copying sensu strictu that Dugatkin (1992) uses. Copying should refer exclusively to the situation in which the female bases her choice of mate on her direct observation of the action of other females mating with a particular male, as observed by Dugatkin (1992). In none of the studies in which females were more likely to spawn in nests containing eggs (including Goldschmidt et al., 1993) has the phenomenon of copying sensu strictu been studied. A second source of confusion in the literature on female copying is that the cue on which females base their choice and the benefit that females may gain from making this choice (i.e. proximate and ultimate causes, the ‘how’ and the ‘why’) are sometimes mixed up. In the case of female preference for males with eggs, a number of cues and functions can be distinguished. Possible cues which may trigger the female’s decision are: (1) her observation of increased male courtship display, (2) her observation of increased male parental behaviour, (3) her observation of a certain number of eggs present in the nest, (4) her observation of other females in the act of mating (i.e. copying sensu strictu). The adaptive significance or function, i.e. the selective advantage of this preference (based on any of these cues), may be: (I) dilution of the risk of predation or cannibalism with increasing brood size (Rohwer, 1978), (II) increased paternal care with larger broods (Sargent, 1988), (III) increased chance of choosing a male of good parental quality (the eggs are proof of the male’s ability to care for them so far) (Ridley, 1978), (IV) increased chance of choosing a male that has been attractive to other females (the eggs are proof that the male has already attracted females) (Ridley, 1978). These possible benefits are not mutually exclusive. By all four effects female fitness may be enhanced through better chances of survival of her eggs in the nest. The last two effects (III and IV) may constitute a benefit if such apparently attractive males produce offspring of good genetic quality or ‘sexy sons’. It is important to note that in theory, any of the four benefits (I-IV) could accrue to females choosing males based on any of the four cues (l-4). The last benefit (IV), i.e. the increased chance of picking a male that has been attractive to other females, is most commonly discussed in relation to copying 1 son and Hoglund, 1992; Pruett-Jones, 1992). However, the term ‘copying’ (Losey et al., 1986; G’b sensu strictu refers to the cue on which females base their mate choice, i.e. the observation of other females mating with a particular male (4). Sometimes proximate and ultimate causes are treated as if they are alternative explanations. For example, Pruett-Jones (1992, page 1004) states that “Preference by females for males with eggs could result from copying, changes in male display or parental-care behaviour, or a reduction in the risk of
S.B.M. Kruuk/
Behaviourul
Processrs
36 (1996) 99-102
101
predation with increasing clutch size”. This is incorrect because copying and changes in display refer to the cues that females use for choosing particular males (4 and 1 respectively). On the other hand, reduction of predation risk refers to the benefit that females may gain from such a preference (I). Changes in paternal care may refer to both the cue that females use as well as the benefit that females gain (2 and II respectively). Dugatkin (1992) also mixes proximate and ultimate causes when he refers to female fish preferring males that are already guarding eggs (page 1387): “these results are ambiguous with respect to copying behaviour, as females may prefer nests with eggs because this ‘dilutes’ the risk of predation”. While Dugatkin’s own experiments focus entirely on the proximate mechanism, his argument here is based on ultimate causes. It is important that studies of the mechanism controlling a behaviour and the function of that behaviour go hand in hand, but one must remember that they are separate questions. Mixing up of the two creates confusion. My last point concerns the discussion of the adaptive significance of copying. In the theoretical models of copying (Losey et al., 1986; Wade and Pruett-Jones, 1990; Pruett-Jones, 1992) the authors refer to a fitness benefit which comes about because copying females are likely to mate with males whose good quality has been assessed by other females (IV). These models investigate whether copying can be an evolutionary stable strategy by this benefit alone. Other benefits, such as a higher hatching success of eggs laid in a nest that already contains eggs, independent of the male’s inherent quality, (I and II), do not play a role in their models. In theory this could apply to situations where the females copy sensu strictu as well as to situations where the females base their choice on any indirect evidence of other females’ choices. However, one of the assumptions made in these models is that choosing a mate is costly and copying is not (Losey et al., 1986; Wade and Pruett-Jones, 1990; Pruett-Jones, 1992): choosing females have costs when they are assessing male quality, which copying females do not have because they rely on the assessment made by other females, Obviously, this assumption does not hold in cases in which females base their choice on the number of eggs present in the nest. Field studies (Gronell, 1989; Kraak and Videler, 1991; Goldschmidt et al., 1993) suggest that visiting nests in order to check whether or not eggs are present, costs as much as assessing male quality on the basis of physical or behavioural traits of the male. In either case, females spend time searching, visiting, and assessing males or nests. When a female visits a nest, a behavioural interaction occurs during which male traits can be judged by the female as well. Hence, the theoretical models on the evolutionary stability of copying are inappropriate in this case. In summary, I want to suggest that the term ‘copying’ be used more carefully. The term sensu strictu refers to the phenomenon that females base their choice on what they have observed other females doing. This is a proximate mechanism. The adaptive significance and evolutionary consequences of this and related phenomena should be investigated as a separate question. Furthermore, one must bear in mind that the models on the evolutionary stability of copying assume that copying females avoid the cost of choosing, which is not the case when females make their choice after having checked the contents of the nest.
Acknowledgements I want to acknowledge Dr. J.P. Kruijt and Dr. Ton Groothuis, who helped me think clearly about this matter. The manuscript has also benefitted from the comments of anonymous referees.
102
S.B.M. Krauk/
Brhaoioural
Processes 36 (1996) 99-102
References Dugatkin, L.A., 1992. Sexual selection and imitation: females copy the mate choice of others. Am. Nat. 139: 1384-1389. Gibson, R.M. and Hiiglund, J., 1992. Copying and sexual selection. TREE 7: 229-231. Goldschmidt, T., Bakker, T.C.M. and Feuth-de Bruijn, E., 1993. Selective copying in mate choice of female sticklebacks. Anim. Behav. 45: 541-547. Gronell, A.M., 1989. Visiting behaviour by females of the sexually dichromatic damselfish, Chrypsipreru cyanea (Teleostei: Pomacentridae): a probable method of assessing male quality. Ethology 8 1: 89- 122. Kirkpatrick, M. and Dugatkin, L.A., 1994. Sexual selection and the evolutionary effects of copying mate choice. Behav. Ecol. Sociobiol. 34: 443-449. Knapp, R.A. and Sargent, R.C., 1989. Egg mimicry as a mating strategy in the fantail darter, Ethiostomaflabelfare: females prefer males with eggs. Behav. Ecol. Sociobiol. 25: 321-326. Kraak, S.B.M. and Videler, J.J., 1991. Mate choice in Aidablennius sphynx (Teleostei, Blenniidae); females prefer nests containing more eggs. Behaviour 119: 243-266. Losey, G.S., Stanton, F.G., Telecky, T.M., Tyler, W.A., III and the Zoology 691 Graduate Seminar Class, 1986. Copying others, an evolutionarily stable strategy for mate choice: a model. Am. Nat. 128: 653-664. Marconato, A. and Bisazza, A., 1986. Males whose nests contain eggs are preferred by female Cottus gobio L. (Pisces, Cottidae). Anim. Behav. 34: 1580-1582. Pruett-Jones, S., 1992. Independent versus nonindependent mate choice: do females copy eachother?. Am. Nat. 140: 1000-1009. Ridley, M., 1978. Paternal care. Anim. Behav. 26: 904-932. Ridley, M. and Rechten, C., 198 1. Female sticklebacks prefer to spawn with males whose nests contain eggs. Behaviour 76: 152-161. Rohwer, S., 1978. Parental cannibalism of offspring and egg raiding as a courtship strategy. Am. Nat. 112: 429-440. Sargent, R.C., 1988. Paternal care and egg survival both increase with clutch size in the fathead minnow, Pimephales promelas. Behav. Ecol. Sociobiol. 23: 33-37. Unger, L.M. and Sargent, R.C., 1988, Allopatemal care in the fathead minnow, Pimephales promefas: females prefer males with eggs. Behav. Ecol. Sociobiol. 23: 27-32. Wade, M.J. and Pruett-Jones, S.G., 1990. Female copying increases the variance in male mating success. Proc. Nat]. Acad. Sci. USA 87: 5749-5753.
