- Email: [email protected]
How do animals choose their mates?
REVIEWS 38 Teaford, M.F. (1991) Dental microwear: what can it tell us about diet and dental function? in Advances in Dental Anthropology (Kelley, M.A.and Larsen, C.S., eds), pp. 341-356, Alan R. Liss 39 Mallatt, J. Ventilalion and the origin of jawed vertebrates: a new mouth, Zool. J. Linn. Sot. (in press)
40 Peterson, K.J. (1994) The origiu and early evolution of the Craniata, in Major Features of Vertebrate Evolution (Prothero, D.R.and Schoch, R.M., eds), pp. 14-37, The Paleontological Society, and the University of Tennessee
Howdo animalschoosetheir mates? Robert M. Gibson and Tom A. Langen
S
How animals search for and evaluate ability24are also possible in some exual selection has been such an intensive focus of research prospective mates has, until recently, cases. Different cues may be used hierarchically* to narrow down been a neglected aspect of sexual over the past decade that selection. Theory and field data suggest one might expect there to be the search at each stage. Fiddler that discrimination varies with the costs a well-established answer to the crabs (&a annulipes), for examand benefits of choice, but a consensus ple, preferentially approach larger question posed in our title. On the has yet to be reached on the tactics by contrary, researchers have focused males but base subsequent choice their efforts primarily on determinwhich prospective mates are evaluated. on burrow dimension@. Female ing which mates are chosen and This intriguing issue may be clarified by sage grouse (Centrocercus urn why, largely ignoring the processes new studies that deal explicitly with the phasiunus) (Fig. 1) are attracted by by which prospective mates are process of information acquisition. vocal characteristics of male displays but choose among visited evaluated. It has been apparent for males using other cues, including well over a decade that studying Robert Gibson and Tom Langen are at the Dept of the process of mate choice would be display ratel7. These observations Biology, University of California, Los Angeles, instructive. Simply demonstrating imply that the number of prospecCA 90095-1606, USA. ([email protected]) tive males a female evaluates that mate choice involves complex ([email protected]) assessment provides convincing could substantially exceed the evidence for adaptive choice’. number that she visits. More-detailed analyses promise to sharpen understanding of the associated costs and benefits The economics of finding a mate of mate choice, clarify the ways in which mate choice affects Given active choice, are there any generalities that govthe evolution of a range of sexually selected characters and ern how choosy individuals will be; or the way in which illuminate general mechanisms of decision makingz. Yet prospective mates are evaluated? These two issues have until 1990, tactical aspects of mate choice were ignored by been addressed from a theoretical perspectivel!JJ5-27 and all but a handful of researcher+. Since then, interest in are beginning to be scrutinized empirically. We take up each in turn. this topic has been stimulated by new theory and data. Our purpose here is to highlight these developments, identify Optimal choosiness areas of debate, and point to some unanswered questions. In theory, the fitness gain from choice, and hence optiActive choice mal choosiness, should be affected by at least three variA starting premise of most work in this area is that ani- ables: the distribution of mate quality, the costs of mals are engaged in a process of active choice while searchsearching for mates, and the chooser’s qualitylJ5J8. Quality ing for mates’. They examine a number of prospects closely is used here synonymously with the fitness obtained when choosing a particular partner. The predictions are intuitive: and reject all but one, based on comparisons either among choosiness should increase with the variance in quality of the candidates or to an internal standard (threshold). This prospective mates and decrease as the costs of locating is an appealing idea, but mate choice may often entail much another mate or delaying choice increase. When both sexes simpler mechanisms, such as attraction to mates emitting choose their mates, low quality (less desirable) individuals more conspicuous or intense signals’. What is the evidence for active choice? should be less discriminating. This is because their options are limited to lower quality individuals of the opposite sex, Active choice has been inferred from the observation that individuals visit several prospective mates but choose capping their benefits and increasing search costs. Data relonly one (or a subset) of them, thus implicitly rejecting the evant to the first two predictions are beginning to accumulate, though choosiness based on individual quality remains remainder. Using this criterion, field workers have documented active choice of males by females in diverse taxa, in- unexplored. cluding insects7,8,crustaceag, fishlo-12,frog+, bird&4-19 and There is some evidence that animals can adaptively track changes in the distribution of mate quality. Female mamma@. Table 1 summarizes data from 11 well-studied species. In each case, data refer to one mating episode in pine engraver beetles (1~spini), searching for a mate in the which a female typically selects a single mate. field, discriminate more strongly in favor of unmated males as the proportion of such males on the log where they are Besides illustrating that active choice can be an important component of mate selection, the data also show that searching increasess; this preference probably increases larfemales of a number of species do not approach males at val viability. Bakker and MilinskP presented female threespined sticklebacks (Gasterosteusaculeutus) with three males random but rather visit a pre-selected subset. This suggests sequentially, the first and last of which had similar nuptial some initial assessment based on long-range cues, although simpler alternative processes such as differences in detectcoloration (a cue presumed to indicate male quality).
468
0
1996, Elsevier
Science
Ltd
PII: SO169-5347(96)10050-l
TREE
uol.
I I, no.
I I Nouember
1996
REVIEWS
Fig. 1. Female sage grouse (Centrocercus Photograph by M. Chappell.
urophasianus)
at a lek.
benefit obtained from choice depends on the way in which males are evaluated. He assumed that females encountered males sequentially and in a random order with respect to their quality, and were able to assess male quality accurately. For a given number of males examined, a ‘best-of-n’ (or pooled comparisons) tactic in which all options are examined, and the best chosen retrospectively, yielded a consistently higher quality mate than alternative thresholdbased rules (in which a female proceeds from male to male until encountering one whose quality exceeds a critical acceptance threshold). Subsequent work has revealed that the optimal sampling tactic changes when the costs as well as the benefits of choice are considered. Starting from the same assumptions as Janetos, Real25found that best-of-n search consistently yields a lower payoff than a threshold (or sequential search) tactic in which the female accepts or rejects an encountered male based on the fitness gain he provides relative to the expected net benefit of continued search. The latter takes into account both the cost of finding another mate and its expected quality. The threshold tactic yields a higher fitness because it enables a searcher to avoid further costs when an acceptable male is encountered early during a search. This work builds on theory developed by economists to solve the analogous problem of finding the ideal job candidate. Following a suggestion by Wittenbergerz, field workers have tried to discriminate between pooled comparison and threshold-based sampling rules by retrospectively examining observed sequences of visits to prospective mates in a variety of species. Thus, female pine engravers, which visit a series of different mates without repeats, could be employing a sequential searcha, while female cock-of-the-rock (Rupicolu rupicola), which repeatedly visit a small set of males before mating, may be following a pooled comparison tactics. Some other species exhibit rather variable visit sequences, which suggests that search tactics vary among individuals23. Two criticisms have been leveled at this approach. First, it is unlikely to yield clear answers because different tactics can produce similar search sequences. For example, best-of-n and sequential search with a falling response threshold should produce similar behavior14V34. According to this view, some studies provide evidence for sequential search, but none unequivocally supports pooled comparison. Second, search sequences, particularly those for birds, often exhibit greater flexibility than either bestof-n or sequential search models appear to predicG27. For instance, multiple visits to the same male and repeated visits followed by rejection are commonplace in the avian data. While such patterns might be dismissed as
Females were less sexually responsive to the last male if the previous one was brighter, and more responsive if it was duller, suggesting that response thresholds were tracking mean mate quality. Similar results have been reported for other fish30and birds31.Whether preferences also track the variance in mate quality has yet to be shown. Experiments with sticklebacks also provide evidence that search costs can affect choosiness. Females were more responsive to a male with dull nuptial coloration if they had expended energy swimming against a current since encountering the previous male than if they had not32. In theory, choosiness could also be lowered by other costs of mate searching, including predation risk, the possibility of losing an acceptable mate to competitors if choice is delayed, and physiological or ecological constraints on the timing of fertilization that limit mating to a finite time window25.Possible examples of each effect include decreased choosiness under perceived predation risk in guppies33, more rapid mate choice by female pied flycatchers (Ficedufa hypoleuca) when competition with other females increases22, and lowered discrimination by female three-spined sticklebacks as spawning time approacheGg. The preceding examples indicate that animals can respond to changes in either costs and benefits of choice in expected ways. Changes in preference observed in the field may also be linked to simultaneous changes in both benefits and costs. For example, field observations of the peacock wrasse (Symphodus thx) show that as the breeding season progresses females increasingly prefer males that will guard their eggs over non-guarding males. This shift is exDlained , by the combination’ of an Table 1. Mate-searching behavior by females in some intensively studied species increase in the survivorship of guarded, relative to unRandom Active Males visited Species encounter? choice? meanfso (n) Refs guarded, eggs, and a decrease in search costs as more males Pine engraver beetle (Ips pini) 2.8k1.5 (92) 8 yes yes defend nest+. Fiddler crab (Uca annulipes) no 7.5f6.0 (50) 9 The tactics of choice If active choice is a common phenomenon, are there any general rules by which potential mates are assessed? In the first theoretical exploration of this question, Janetos4 showed that the TREE DOI. II,
no.
II
November
Nattetjack toad (Bufo calamita) Barnacle goose (Branta leucopsis) Great snipe (Galjinago media) Sage grouse (Centrocercus urophasianus) Black grouse (Jetrao tetrix), Peacock (Pave cristatus) Cock-of-the-rock (Rupicola rupicola) Pied flycatcher (Ficedula hypdeuca) Great reed warbler (Acrocephalus arundinaceus)
I996
no ? ? no no
? no ? ?
yes no
yes yes yes yes
yes yes yes yes
1.7f1.1(33) 2.4f0.6 (14) 3.0f2.5 i33j 3.7f2.6 (40) 4.9f2.0 (31)
6 21 16 17 19
3.0f1.2 (11) 3.4f2.3 (88)
18 5
3.8f2.4 5.9f2.6
(30) (11)
15,22,23 14
469
REVIEWS recall errors34 they may also point to processes that the models omit. Luttbeg27has recently shown that re-sampling could be explained by relaxing the assumptions of random encounter and perfect information about mate quality employed in previous analyses. In his model, a female samples from a set of males each of whom provides a signal that probabilistically indicates his quality. The female has some prior information about each male and, at any stage before mating, she can choose to sample any male to update her estimate of his quality. The presumption is that repeated sampling provides a more accurate estimate of a male’s quality. She chooses a mate when this decision provides a greater expected fitness return than collecting additional information. In the face of imperfect information about mate quality, this strategy outperforms both best-of-n and threshold rules. By acknowledging that animals are unlikely to have perfect information about mate quality but must instead rely on imperfect cues35, Luttbeg’s analysis is an important step towards incorporating more realistic constraints into search models. It correctly predicts that animals (1) may selectively visit certain prospective mates, (2) sample some of these repeatedly (both reported in references cited above), and (3) prolong sampling when there is greater uncertainty36. It may also imply considerable cognitive complexity; whether the information processing abilities of animals are up to the task remains to be seen. Prospects Making sense of the tactics used by animals to evaluate prospective mates poses one of the more interesting unresolved challenges to students of sexual selection. Our survey suggests that two kinds of studies are likely to advance understanding of this topic. First, it would be useful to explore further how optimal search tactics are affected by proximate constraints on information acquisition and prc+ cessing. This will require explicit consideration of such issues as signal detection, discrimination and memory. Second, we need empirical studies that are designed to distinguish more clearly between alternative tactical model@. This will entail careful selection of study systems, since the process of choosing a mate is often hard to observe and relevant variables, such as benefits of choice, can be difficult to measure or manipulate. Useful insights may be provided by studying other more empirically tractable situations in which animals sample before choosing, such as prospecting for a nesting site, a breeding territory, or a food item to cache. Acknowledgements We appreciate the suggestions of Judy Stamps, Bob Warner and an anonymous reviewer. T.A.L. is supported by a National Research Fellowship from the NIH.
1 Parker, G.A.(1983)Mate quality and mating decisions, in Mare Choice (Bateson, P., ed.), pp. 141-166,CambridgeUniversity Press 2 Wittenberger, J.F. (1983) Tactics of mate choice, in Mate Choice (Bateson, P., ed.), pp. 435-447, Cambridge University Press 3 Brown, L. (1981) Patterns of female choice ln mottled sculpins (Cottidae, Teleostei), Anim. Behav. 29,375-382 4 Janetos, AC (1980) Strategies of female mate choice: a theoretical analysis, Behav. Ecol. Sociobiol. 7, 107-l 12 5 Trail, P.W. and Adams, P.S. (1989) Active mate choice at cock-of-the rock leksz tactics of sampling and comparison, Behav. 25, 283-292
6 Arak, A. (1988) Female mate selection in the nattejack toad: active choice or passive attraction? Behav. Ecol. Sociobiol. 22,317-327
470
(Burmeister) (Odonata: Libellulidae): III.Male density, OSR,and male and female mating behavior, Ethology 80,120-136 8 Reid, M.L.and Stamps, J.A. Mate tactics of female pine engravers (Coleoptera: Scolytidae): field tests of alternative models, Am. Nat (in press) 9 Backwell, P.R.Y.and Passmore, N.1.(1996) Time constralnts and multiple choice criteria in the sampling behavior and mate choice of the fiddler crab, Uca annulipes, Behau. Ecol. Sociobiol.38, 407-416 10 Gronell, A.M. (1989) Visiting behaviour by females of the sexually dichromatic damsel fish, Chrysiptera cyaneo (Teleostei: Pomacentidae): a probable method of assessing male quality, Ethology 81,89-122
11 Warner, R.R. et al. (1995) Dynamics of female choice for parental care in a fish spezies whm care is facultatlve,Behau. Ecol. 6,73-81 12 Sikkel, P.C. (1995) Die1periodicity of spawning activity in a permanently territorial damselfish: a test of adult feeding hypotheses, Environ. Biol. Fish. 42,241-251 13 Ryan, M.J. (1985) The T&guru Frog, University of Chicago Press 14 Bensch, S. and Hasselquist, D. (1992) Evidence for active female mate choice in a polygynous warbler, Anim. Behav. 44,301-311 15 Dale, S. et al. (1990) Mate sampling behavior of female pied flycatchers: evidence for active mate choice, Behav. Ecol. Sociobiol.
27,87-91
16 Fiske, P. and K%Is, J.A. (1995) Mate sampling and copulation behavlour of great snipe females, Anim. Behav. 49,209-219 17 Gibson, R.M. (1996) Female choice in sage grouse: the roles of attraction and active comparison, Behav. Ecol. Sociobiol. 39,55-59 18 Petrie, M., Halliday, T. and Sanders, C. (1991) Peahens prefer peacocks with elaborate trains, Anim. Behav. 41,323-331 19 RintamBki,P.T. et al. (1995) Mate sampling behavior of black grouse females (Tetrao tetrix), Behav. Ecol. Sociobiol. 37,209-215 20 Byers, J.A., Moodie, J.D. and Hall, N. (1994) Pronghom females choose vigorous mates, Anim. Behav. 47,33-43 21 Choudhury, S. and Black, J.M. (1993) Mate-selection behaviour and sampling strategies in geese, Anim. Behau. 46,747-757 22 Dale, S., Rinden, H. and Slagsvold, T. (1992) Competition for a mate restricts mate search of female pied flycatchers, Behav. Ecol. Sociobiol.
30, 165-176
23 Hovi, M. and Rltti, 0. (1994) Mate sampling and assessment procedures in female pied flycatchers (Ficedula hypoleucu), Ethology 96, 127-137
24 Forrest, T.G. and Raspet, R. (1994) Models of female choice in acoustic communication, Behav. Ecol. 5,293-303 25 Real, L. (1990) Search theory and mate choice. I. Models of single-sex discrimination, Am. Nat. 136,376-404 26 Dombrovsky, Y. and Perrin, N. (1994) On adaptive search and optimal stopping in sequential mate choice, Am. Nat. 144,355-361 27 Luttbeg, B. A comparative Bayes tactic for mate assessment and choice, Behav. Ecol. (in press) 28 Real, L. (1991) Search theory and mate choice. II. Mutual interaction, assortative mating, and equilibrium variation in male and female fitness, Am. Nat 138,901-917 29 Bakker, T.C. and Milinski, M. (1991) Sequential female choice and the previous male effect in sticklebacks, Behav. Ecol. Sociobiol. 29, 205-210
30 Downhower, J.F. and Lank, D.B. (1994)Effects of previous experience on mate choice by female mottled sculpins, Anim. Behav. 47,369-372
References
Ecol. Sociobiol.
7 Moore, A.J. (1989) The behavioral ecology of Libellulu luctuosu
31 Collins, S.A. (1995) The effect of recent experience on female choice in zebra finches, Anim. Behau. 49,479-486 32 Milinski, M. and Bakker, T.C. (1992) Costs influence sequential mate choice in sticklebacks, Gasterosteus aculeatus, hoc. R. Sot. London Ser. B 250,229-233
33 Godin, J-G. and Briggs, S.E. (1995) Female mate choice under predation risk in the guppy, Anim. Behau. 51,117-130 34 Weigmann, D.D.et al. (1996) Some distlngulshlng features of models of search behavior and mate choice, Am. Nat. 147,188-204 35 Getty, T. (1996) Mate selection by repeated inspection, Anim. Behav. 51,739-745
36 Dick, J.T.A. and Elwood, R.W. (1989) Assessment and decisions during mate choice in Gammarus pulex (Amphipoda), Behauiour 109,235-246 TREE
vol.
II,
no.
II
November
I996
40 Peterson, K.J. (1994) The origiu and early evolution of the Craniata, in Major Features of Vertebrate Evolution (Prothero, D.R.and Schoch, R.M., eds), pp. 14-37, The Paleontological Society, and the University of Tennessee
Howdo animalschoosetheir mates? Robert M. Gibson and Tom A. Langen
S
How animals search for and evaluate ability24are also possible in some exual selection has been such an intensive focus of research prospective mates has, until recently, cases. Different cues may be used hierarchically* to narrow down been a neglected aspect of sexual over the past decade that selection. Theory and field data suggest one might expect there to be the search at each stage. Fiddler that discrimination varies with the costs a well-established answer to the crabs (&a annulipes), for examand benefits of choice, but a consensus ple, preferentially approach larger question posed in our title. On the has yet to be reached on the tactics by contrary, researchers have focused males but base subsequent choice their efforts primarily on determinwhich prospective mates are evaluated. on burrow dimension@. Female ing which mates are chosen and This intriguing issue may be clarified by sage grouse (Centrocercus urn why, largely ignoring the processes new studies that deal explicitly with the phasiunus) (Fig. 1) are attracted by by which prospective mates are process of information acquisition. vocal characteristics of male displays but choose among visited evaluated. It has been apparent for males using other cues, including well over a decade that studying Robert Gibson and Tom Langen are at the Dept of the process of mate choice would be display ratel7. These observations Biology, University of California, Los Angeles, instructive. Simply demonstrating imply that the number of prospecCA 90095-1606, USA. ([email protected]) tive males a female evaluates that mate choice involves complex ([email protected]) assessment provides convincing could substantially exceed the evidence for adaptive choice’. number that she visits. More-detailed analyses promise to sharpen understanding of the associated costs and benefits The economics of finding a mate of mate choice, clarify the ways in which mate choice affects Given active choice, are there any generalities that govthe evolution of a range of sexually selected characters and ern how choosy individuals will be; or the way in which illuminate general mechanisms of decision makingz. Yet prospective mates are evaluated? These two issues have until 1990, tactical aspects of mate choice were ignored by been addressed from a theoretical perspectivel!JJ5-27 and all but a handful of researcher+. Since then, interest in are beginning to be scrutinized empirically. We take up each in turn. this topic has been stimulated by new theory and data. Our purpose here is to highlight these developments, identify Optimal choosiness areas of debate, and point to some unanswered questions. In theory, the fitness gain from choice, and hence optiActive choice mal choosiness, should be affected by at least three variA starting premise of most work in this area is that ani- ables: the distribution of mate quality, the costs of mals are engaged in a process of active choice while searchsearching for mates, and the chooser’s qualitylJ5J8. Quality ing for mates’. They examine a number of prospects closely is used here synonymously with the fitness obtained when choosing a particular partner. The predictions are intuitive: and reject all but one, based on comparisons either among choosiness should increase with the variance in quality of the candidates or to an internal standard (threshold). This prospective mates and decrease as the costs of locating is an appealing idea, but mate choice may often entail much another mate or delaying choice increase. When both sexes simpler mechanisms, such as attraction to mates emitting choose their mates, low quality (less desirable) individuals more conspicuous or intense signals’. What is the evidence for active choice? should be less discriminating. This is because their options are limited to lower quality individuals of the opposite sex, Active choice has been inferred from the observation that individuals visit several prospective mates but choose capping their benefits and increasing search costs. Data relonly one (or a subset) of them, thus implicitly rejecting the evant to the first two predictions are beginning to accumulate, though choosiness based on individual quality remains remainder. Using this criterion, field workers have documented active choice of males by females in diverse taxa, in- unexplored. cluding insects7,8,crustaceag, fishlo-12,frog+, bird&4-19 and There is some evidence that animals can adaptively track changes in the distribution of mate quality. Female mamma@. Table 1 summarizes data from 11 well-studied species. In each case, data refer to one mating episode in pine engraver beetles (1~spini), searching for a mate in the which a female typically selects a single mate. field, discriminate more strongly in favor of unmated males as the proportion of such males on the log where they are Besides illustrating that active choice can be an important component of mate selection, the data also show that searching increasess; this preference probably increases larfemales of a number of species do not approach males at val viability. Bakker and MilinskP presented female threespined sticklebacks (Gasterosteusaculeutus) with three males random but rather visit a pre-selected subset. This suggests sequentially, the first and last of which had similar nuptial some initial assessment based on long-range cues, although simpler alternative processes such as differences in detectcoloration (a cue presumed to indicate male quality).
468
0
1996, Elsevier
Science
Ltd
PII: SO169-5347(96)10050-l
TREE
uol.
I I, no.
I I Nouember
1996
REVIEWS
Fig. 1. Female sage grouse (Centrocercus Photograph by M. Chappell.
urophasianus)
at a lek.
benefit obtained from choice depends on the way in which males are evaluated. He assumed that females encountered males sequentially and in a random order with respect to their quality, and were able to assess male quality accurately. For a given number of males examined, a ‘best-of-n’ (or pooled comparisons) tactic in which all options are examined, and the best chosen retrospectively, yielded a consistently higher quality mate than alternative thresholdbased rules (in which a female proceeds from male to male until encountering one whose quality exceeds a critical acceptance threshold). Subsequent work has revealed that the optimal sampling tactic changes when the costs as well as the benefits of choice are considered. Starting from the same assumptions as Janetos, Real25found that best-of-n search consistently yields a lower payoff than a threshold (or sequential search) tactic in which the female accepts or rejects an encountered male based on the fitness gain he provides relative to the expected net benefit of continued search. The latter takes into account both the cost of finding another mate and its expected quality. The threshold tactic yields a higher fitness because it enables a searcher to avoid further costs when an acceptable male is encountered early during a search. This work builds on theory developed by economists to solve the analogous problem of finding the ideal job candidate. Following a suggestion by Wittenbergerz, field workers have tried to discriminate between pooled comparison and threshold-based sampling rules by retrospectively examining observed sequences of visits to prospective mates in a variety of species. Thus, female pine engravers, which visit a series of different mates without repeats, could be employing a sequential searcha, while female cock-of-the-rock (Rupicolu rupicola), which repeatedly visit a small set of males before mating, may be following a pooled comparison tactics. Some other species exhibit rather variable visit sequences, which suggests that search tactics vary among individuals23. Two criticisms have been leveled at this approach. First, it is unlikely to yield clear answers because different tactics can produce similar search sequences. For example, best-of-n and sequential search with a falling response threshold should produce similar behavior14V34. According to this view, some studies provide evidence for sequential search, but none unequivocally supports pooled comparison. Second, search sequences, particularly those for birds, often exhibit greater flexibility than either bestof-n or sequential search models appear to predicG27. For instance, multiple visits to the same male and repeated visits followed by rejection are commonplace in the avian data. While such patterns might be dismissed as
Females were less sexually responsive to the last male if the previous one was brighter, and more responsive if it was duller, suggesting that response thresholds were tracking mean mate quality. Similar results have been reported for other fish30and birds31.Whether preferences also track the variance in mate quality has yet to be shown. Experiments with sticklebacks also provide evidence that search costs can affect choosiness. Females were more responsive to a male with dull nuptial coloration if they had expended energy swimming against a current since encountering the previous male than if they had not32. In theory, choosiness could also be lowered by other costs of mate searching, including predation risk, the possibility of losing an acceptable mate to competitors if choice is delayed, and physiological or ecological constraints on the timing of fertilization that limit mating to a finite time window25.Possible examples of each effect include decreased choosiness under perceived predation risk in guppies33, more rapid mate choice by female pied flycatchers (Ficedufa hypoleuca) when competition with other females increases22, and lowered discrimination by female three-spined sticklebacks as spawning time approacheGg. The preceding examples indicate that animals can respond to changes in either costs and benefits of choice in expected ways. Changes in preference observed in the field may also be linked to simultaneous changes in both benefits and costs. For example, field observations of the peacock wrasse (Symphodus thx) show that as the breeding season progresses females increasingly prefer males that will guard their eggs over non-guarding males. This shift is exDlained , by the combination’ of an Table 1. Mate-searching behavior by females in some intensively studied species increase in the survivorship of guarded, relative to unRandom Active Males visited Species encounter? choice? meanfso (n) Refs guarded, eggs, and a decrease in search costs as more males Pine engraver beetle (Ips pini) 2.8k1.5 (92) 8 yes yes defend nest+. Fiddler crab (Uca annulipes) no 7.5f6.0 (50) 9 The tactics of choice If active choice is a common phenomenon, are there any general rules by which potential mates are assessed? In the first theoretical exploration of this question, Janetos4 showed that the TREE DOI. II,
no.
II
November
Nattetjack toad (Bufo calamita) Barnacle goose (Branta leucopsis) Great snipe (Galjinago media) Sage grouse (Centrocercus urophasianus) Black grouse (Jetrao tetrix), Peacock (Pave cristatus) Cock-of-the-rock (Rupicola rupicola) Pied flycatcher (Ficedula hypdeuca) Great reed warbler (Acrocephalus arundinaceus)
I996
no ? ? no no
? no ? ?
yes no
yes yes yes yes
yes yes yes yes
1.7f1.1(33) 2.4f0.6 (14) 3.0f2.5 i33j 3.7f2.6 (40) 4.9f2.0 (31)
6 21 16 17 19
3.0f1.2 (11) 3.4f2.3 (88)
18 5
3.8f2.4 5.9f2.6
(30) (11)
15,22,23 14
469
REVIEWS recall errors34 they may also point to processes that the models omit. Luttbeg27has recently shown that re-sampling could be explained by relaxing the assumptions of random encounter and perfect information about mate quality employed in previous analyses. In his model, a female samples from a set of males each of whom provides a signal that probabilistically indicates his quality. The female has some prior information about each male and, at any stage before mating, she can choose to sample any male to update her estimate of his quality. The presumption is that repeated sampling provides a more accurate estimate of a male’s quality. She chooses a mate when this decision provides a greater expected fitness return than collecting additional information. In the face of imperfect information about mate quality, this strategy outperforms both best-of-n and threshold rules. By acknowledging that animals are unlikely to have perfect information about mate quality but must instead rely on imperfect cues35, Luttbeg’s analysis is an important step towards incorporating more realistic constraints into search models. It correctly predicts that animals (1) may selectively visit certain prospective mates, (2) sample some of these repeatedly (both reported in references cited above), and (3) prolong sampling when there is greater uncertainty36. It may also imply considerable cognitive complexity; whether the information processing abilities of animals are up to the task remains to be seen. Prospects Making sense of the tactics used by animals to evaluate prospective mates poses one of the more interesting unresolved challenges to students of sexual selection. Our survey suggests that two kinds of studies are likely to advance understanding of this topic. First, it would be useful to explore further how optimal search tactics are affected by proximate constraints on information acquisition and prc+ cessing. This will require explicit consideration of such issues as signal detection, discrimination and memory. Second, we need empirical studies that are designed to distinguish more clearly between alternative tactical model@. This will entail careful selection of study systems, since the process of choosing a mate is often hard to observe and relevant variables, such as benefits of choice, can be difficult to measure or manipulate. Useful insights may be provided by studying other more empirically tractable situations in which animals sample before choosing, such as prospecting for a nesting site, a breeding territory, or a food item to cache. Acknowledgements We appreciate the suggestions of Judy Stamps, Bob Warner and an anonymous reviewer. T.A.L. is supported by a National Research Fellowship from the NIH.
1 Parker, G.A.(1983)Mate quality and mating decisions, in Mare Choice (Bateson, P., ed.), pp. 141-166,CambridgeUniversity Press 2 Wittenberger, J.F. (1983) Tactics of mate choice, in Mate Choice (Bateson, P., ed.), pp. 435-447, Cambridge University Press 3 Brown, L. (1981) Patterns of female choice ln mottled sculpins (Cottidae, Teleostei), Anim. Behav. 29,375-382 4 Janetos, AC (1980) Strategies of female mate choice: a theoretical analysis, Behav. Ecol. Sociobiol. 7, 107-l 12 5 Trail, P.W. and Adams, P.S. (1989) Active mate choice at cock-of-the rock leksz tactics of sampling and comparison, Behav. 25, 283-292
6 Arak, A. (1988) Female mate selection in the nattejack toad: active choice or passive attraction? Behav. Ecol. Sociobiol. 22,317-327
470
(Burmeister) (Odonata: Libellulidae): III.Male density, OSR,and male and female mating behavior, Ethology 80,120-136 8 Reid, M.L.and Stamps, J.A. Mate tactics of female pine engravers (Coleoptera: Scolytidae): field tests of alternative models, Am. Nat (in press) 9 Backwell, P.R.Y.and Passmore, N.1.(1996) Time constralnts and multiple choice criteria in the sampling behavior and mate choice of the fiddler crab, Uca annulipes, Behau. Ecol. Sociobiol.38, 407-416 10 Gronell, A.M. (1989) Visiting behaviour by females of the sexually dichromatic damsel fish, Chrysiptera cyaneo (Teleostei: Pomacentidae): a probable method of assessing male quality, Ethology 81,89-122
11 Warner, R.R. et al. (1995) Dynamics of female choice for parental care in a fish spezies whm care is facultatlve,Behau. Ecol. 6,73-81 12 Sikkel, P.C. (1995) Die1periodicity of spawning activity in a permanently territorial damselfish: a test of adult feeding hypotheses, Environ. Biol. Fish. 42,241-251 13 Ryan, M.J. (1985) The T&guru Frog, University of Chicago Press 14 Bensch, S. and Hasselquist, D. (1992) Evidence for active female mate choice in a polygynous warbler, Anim. Behav. 44,301-311 15 Dale, S. et al. (1990) Mate sampling behavior of female pied flycatchers: evidence for active mate choice, Behav. Ecol. Sociobiol.
27,87-91
16 Fiske, P. and K%Is, J.A. (1995) Mate sampling and copulation behavlour of great snipe females, Anim. Behav. 49,209-219 17 Gibson, R.M. (1996) Female choice in sage grouse: the roles of attraction and active comparison, Behav. Ecol. Sociobiol. 39,55-59 18 Petrie, M., Halliday, T. and Sanders, C. (1991) Peahens prefer peacocks with elaborate trains, Anim. Behav. 41,323-331 19 RintamBki,P.T. et al. (1995) Mate sampling behavior of black grouse females (Tetrao tetrix), Behav. Ecol. Sociobiol. 37,209-215 20 Byers, J.A., Moodie, J.D. and Hall, N. (1994) Pronghom females choose vigorous mates, Anim. Behav. 47,33-43 21 Choudhury, S. and Black, J.M. (1993) Mate-selection behaviour and sampling strategies in geese, Anim. Behau. 46,747-757 22 Dale, S., Rinden, H. and Slagsvold, T. (1992) Competition for a mate restricts mate search of female pied flycatchers, Behav. Ecol. Sociobiol.
30, 165-176
23 Hovi, M. and Rltti, 0. (1994) Mate sampling and assessment procedures in female pied flycatchers (Ficedula hypoleucu), Ethology 96, 127-137
24 Forrest, T.G. and Raspet, R. (1994) Models of female choice in acoustic communication, Behav. Ecol. 5,293-303 25 Real, L. (1990) Search theory and mate choice. I. Models of single-sex discrimination, Am. Nat. 136,376-404 26 Dombrovsky, Y. and Perrin, N. (1994) On adaptive search and optimal stopping in sequential mate choice, Am. Nat. 144,355-361 27 Luttbeg, B. A comparative Bayes tactic for mate assessment and choice, Behav. Ecol. (in press) 28 Real, L. (1991) Search theory and mate choice. II. Mutual interaction, assortative mating, and equilibrium variation in male and female fitness, Am. Nat 138,901-917 29 Bakker, T.C. and Milinski, M. (1991) Sequential female choice and the previous male effect in sticklebacks, Behav. Ecol. Sociobiol. 29, 205-210
30 Downhower, J.F. and Lank, D.B. (1994)Effects of previous experience on mate choice by female mottled sculpins, Anim. Behav. 47,369-372
References
Ecol. Sociobiol.
7 Moore, A.J. (1989) The behavioral ecology of Libellulu luctuosu
31 Collins, S.A. (1995) The effect of recent experience on female choice in zebra finches, Anim. Behau. 49,479-486 32 Milinski, M. and Bakker, T.C. (1992) Costs influence sequential mate choice in sticklebacks, Gasterosteus aculeatus, hoc. R. Sot. London Ser. B 250,229-233
33 Godin, J-G. and Briggs, S.E. (1995) Female mate choice under predation risk in the guppy, Anim. Behau. 51,117-130 34 Weigmann, D.D.et al. (1996) Some distlngulshlng features of models of search behavior and mate choice, Am. Nat. 147,188-204 35 Getty, T. (1996) Mate selection by repeated inspection, Anim. Behav. 51,739-745
36 Dick, J.T.A. and Elwood, R.W. (1989) Assessment and decisions during mate choice in Gammarus pulex (Amphipoda), Behauiour 109,235-246 TREE
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