- Email: [email protected]
Studying paternity and paternal care: pitfalls and problems
Anim. Behav., 1997, 53, 423–427
COMMENTARIES Studying paternity and paternal care: pitfalls and problems BART KEMPENAERS* & BEN C. SHELDON† *Konrad Lorenz Institute for Comparative Ethology, Vienna †Institute of Cell, Animal & Population Biology, University of Edinburgh (Received 15 August 1996; initial acceptance 6 September 1996; final acceptance 12 November 1996; MS. number: -1086)
Theoretical treatments of the relationship between paternity (or certainty of paternity) and paternal care predict, under certain conditions, that individual males should invest less in paternal care if their paternity is reduced (Whittingham et al. 1992; Westneat & Sherman 1993). Several recent papers have addressed this question using information about males’ genetic paternity from unmanipulated breeding attempts together with measures of those males’ contributions to some components of parental care (Table I). The general picture that emerges from these studies is that there is no positive relationship between paternity and paternal effort (although in some studies the sample size was small, and statistical power limited). However, we argue here that it is inappropriate to use data of this kind to test models relating paternity to paternal care. We discuss the sort of data that can provide a better test. Models of optimal paternal care in response to variation in paternity are based on the effects of trade-offs between current reproductive effort and future reproductive success (Westneat & Sargent 1996). They ask, in effect, what the optimal response in terms of parental effort would be for an individual male responding to a change in paternity. Individuals may lie at different positions along a trade-off between current and future reproduction, and may also experience qualitatively different trade-offs because of (for example) differences in resource availability (van Noordwijk & de Jong 1986). As a consequence, one cannot assume that all males within a Correspondence: B. C. Sheldon, Department of Zoology, Uppsala University, Villava¨gen 9 S-752 36 Uppsala, Sweden (email: [email protected]). Bart Kempenaers is at KLIVV, Savoyenstrasse 1a, A-1160 Vienna, Austria. 0003–3472/97/020423+05 $25.00/0/ar960377
?
population will be subject to the same rules relating paternity to paternal effort. We illustrate this argument and its consequences by considering three different cases that are likely to obscure relationships between paternity and paternal care at the population level. These can be summarized as resulting from (1) different optimal levels of care for different individuals, (2) the interdependence of paternal and maternal care and (3) differing trade-offs between paternal care and mating opportunities faced by different individuals. The points that we make here are simple, have general applicability to many problems in behavioural ecology, and similar points have been made many times before in different contexts (for example in discussions of the pros and cons of nonexperimental studies of the costs of reproduction: Partridge & Harvey 1985; Lessells 1991). Nevertheless, it is our impression that they are not given adequate consideration in most of the studies referred to in Table I. Experimental studies of birds have demonstrated that paternal care may be costly, in terms of reduced survival, breeding or mating opportunities (reviewed in Clutton-Brock 1991). As a consequence, allocation of resources to paternal care is expected to be individually optimized, as with other life-history traits such as clutch size. For example, males in poor condition might reduce their parental care, if the cost of a single ‘unit’ of parental care was greater for males in poor condition. An increasing number of studies have related parentage in natural populations to the relative magnitude of condition-dependent secondary sexual characters (Smith et al. 1991; Hasselquist et al. 1996; Sundberg & Dixon 1996), and there are good reasons to expect such relationships to be rather common (Møller 1992). 1997 The Association for the Study of Animal Behaviour
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Table I. Published studies investigating the relationship between genetic parentage and level of parental care by male birds Species Bobolink, Dolichonyx oryzivorus* Indigo bunting, Passerina cyanea† Purple martin, Progne subis* Great tit, Parus major‡ Tree swallow, Tachycineta bicolor* Hooded warbler, Wilsonia citrina* Red-winged blackbird, Agelaius phoenicus§ House martin, Delichon urbica** Purple martin**
Sample size
Relationship
Study
7 41 21 15 12 12 Variable (up to 93) 10 15
r=0.59, P=0.01 rS =0.42 rS =0.08
Gavin & Bollinger 1985 Westneat 1988 Morton et al. 1990 Lubjuhn et al. 1993 Lifjeld et al. 1993 Stutchbury et al. 1994 Westneat 1995
"0.31¦rS¦0.03 "0.15¦rS¦0.16
Whittingham & Lifjeld 1995 Wagner et al. 1996
Sample size is the number of nests for which information on paternity and paternal care was available; with the exception of Lubjuhn et al. (1993), no relationships are statistically significant (P>0.05). *Share of nestling feeding by male. †Measure of care by male was whether the male fed nestlings. ‡Index of nest defence by male. §Several different relationships examined. **Three different measures of paternal care.
Hence, both paternity and the extent of paternal care may be causally related to a third variable, in this case condition. The simplest expectation is that males in poor condition will make a small contribution to parental care, and achieve low paternity, whereas the reverse will be true for males in good condition. This would generate a positive correlation between paternity and paternal care, although the relationship would not be causal. It is also possible however, that a male in poor condition might be selected to increase his share of parental care, if his future prospects were very low (e.g. in cases of ‘terminal investment’: Clutton-Brock 1984). In this case, the correlation between paternity and paternal care might disappear, or even become negative. The potential benefits of parental care may also vary, for example in relation to timing of breeding: in many bird species reproductive success declines with breeding date, and there is evidence that this relationship is causal (e.g. Verhulst & Tinbergen 1991). As a consequence, one might expect lower levels of parental care in broods that are worth less. If there were also a tendency for later broods to contain more extra-pair young, as Møller (1992) has suggested may be the case, one might also expect a positive relationship between paternity and paternal care, but again not the result of a direct effect of paternity on paternal care. The proportion of care that one member of a pair makes will depend upon the contribution that
the other pair member makes (Chase 1980; Wright & Cuthill 1990). The division of parental effort between mates can be understood as an evolutionarily stable strategy whose equilibrium depends upon the relative costs and benefits of investment to the male and female (Houston & Davies 1985; Winkler 1987). Above, we argue that variation in condition between males may affect the extent to which they invest in the current breeding attempt; the same applies to females, which can potentially affect the share of parental care performed by males. For example, imagine a species in which females compete for settlement with the most attractive males, so that females in poorer condition are more likely to pair with unattractive males, with the result that they are also more likely to engage in extra-pair copulations. In this case, lower investment by females, and compensation by males, could lead to a negative relationship between paternity and paternal care, or obscure the males’ response to lowered paternity. Burley (1986) proposed that a female might be prepared to invest more in care for offspring if mated to an attractive male, and evidence from Burley’s study and others (e.g. de Lope & Møller 1993; Petrie & Williams 1993; Møller 1994) supports this suggestion. The interpretation of Burley’s differential investment model is that (1) male attractiveness acts as an indicator of heritable fitness differences and (2), as a consequence,
Commentaries offspring sired by attractive males are of greater value to a female than those sired by unattractive males, and hence worth greater parental investment by the female. Therefore, a female may make a greater share of parental effort when mated to an attractive male (with the result that the male’s share declines), while at the same time being less likely to engage in extra-pair copulations with other males. Hence, differential investment by females might be responsible for a negative correlation between paternity and paternal care. Further complication is added when one considers how a female should respond when mated to a relatively unattractive male, when some of her offspring have been sired by an attractive extra-pair male. In this case, a prediction of the differential allocation hypothesis is that these females would provide relatively more care to the brood as a whole (since discrimination of chicks based upon paternity is unlikely: Davies et al. 1992; Kempenaers & Sheldon 1996), which would potentially affect the strength and sign of any correlation between paternity and paternal care resulting from differential allocation by females. In some of the earlier models that investigated the relationship between paternity and optimal levels of paternal care, the costs of paternal care were expressed in terms of lost mating opportunities (e.g. Werren et al. 1980). In species with multiple breeding attempts within a season, or with a high degree of breeding asynchrony, a male might face a trade-off between investing in the current breeding attempt and pursuing other mating opportunities, either through polygyny or extra-pair copulation. However, this trade-off may not be the same for all males. It is not unreasonable to expect that the extent to which males pursue extra mating opportunities will be partly determined by their likelihood of gaining extra matings. Thus attractive males, or males in good physiological condition, may be able to expend more effort in gaining extra mating opportunities, at the expense of investment in the current brood. If the factors that determine a male’s pursuit of extra matings are related to those that determine a male’s paternity, there may exist a negative correlation between paternity and paternal effort. Similarly, in polygynous species, a trade-off may exist between investing in paternal care and guarding another female. Whittingham (1994)
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showed experimentally that male red-winged blackbirds did not feed offspring if they had an additional mate in her fertile period breeding on their territory (see also Lifjeld & Slagsvold 1989). This might influence the relationship between paternity and paternal care if, for example, males that were more successful in attracting multiple females were also less likely to lose paternity. We have outlined three ways in which relationships may exist between paternity and paternal care, without there being a causal link between the two, and other scenarios could doubtless be suggested. For example, some models of the evolution of male sexual ornaments postulate that they have evolved partly as a reliable signal of male parental care ability (e.g. Hoelzer 1989; Price et al. 1993), in which case paternity and paternal care may be further confounded. In two of the cases above, one can construct plausible arguments for the expected correlation between paternity and paternal care to be either positive or negative. It does not seem likely that quantitative predictions about the relative importance of the three cases that we have described above can be made in even the best studied systems at present. As a consequence, we argue that it is currently impossible to predict what relationship may be uncovered between paternity and paternal care in studies relying on correlations across individuals. It is quite possible that in all of the studies listed in Table I, a causal relationship between paternity and paternal care is masked by the influence of other variables. Therefore, there is little to be achieved by reporting relationships between paternity and paternal care in natural populations as a test of models of optimal levels of paternal care, since there can be no clear expectation of the form of the relationship, and even a positive relationship may result entirely from the influence of other variables. Carefully designed experiments provide one means to avoid the numerous problems associated with confounding variables affecting both paternity and paternal care. However, one difficulty empirical studies face is that it does not seem possible that males can directly measure their own paternity; rather, paternity and paternal care must be linked by a third variable, ‘certainty of paternity’. An experiment aiming to uncover a relationship between paternity and paternal care can only reasonably be expected to work if it also affects a male’s certainty of paternity, and in fact the latter
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is the only quantity that such an experiment needs to affect. Unfortunately, this quantity is at present unmeasurable, so that an experimenter must assume that an experiment has manipulated certainty of paternity. This assumption is most likely to be justifiable in cases where experiments mimic as closely as possible what happens when paternity is naturally reduced. For example, studies of several species demonstrate that females actively seek extra-pair copulations by visiting the territories of other males (Kempenaers et al. 1992; Sheldon 1994; Gray 1996). Thus, in these species at least, experiments involving male removal may not be good models for this process (Gowaty, in press), whereas removing a female for a short period might be more effective (e.g. Wright & Cotton 1994; Sheldon et al., in press). It is also important that experiments attempt, as far as is possible, to control for variation in date at which they are performed, relative to fertilization of eggs, since the timing of extra-pair copulations may affect their success (Birkhead et al. 1988; Colegrave et al. 1995). An alternative approach, which has proved fruitful (Dixon et al. 1994; Freeman-Gallant 1996), is to restrict comparisons of paternity and paternal care to successive breeding attempts by the same pair. By doing this one potentially controls for many (but conceivably not all) sources of variation between individual breeding attempts. In conclusion, we believe that there is little to be learnt from the reporting of relationships between paternity and paternal care in unmanipulated populations as tests of models of optimal paternal care. Further testing of models relating paternity to paternal care requires careful consideration of potentially confounding variables and the behavioural mechanisms that relate paternity to paternal care. We are grateful to Tim Birkhead, Nick Davies, Jan Lifjeld, Josephine Pemberton, Hans Winkler and an anonymous referee for comments. B.C.S. was supported by a research fellowship from NERC (UK). REFERENCES Birkhead, T. R., Pellatt, J. E. & Hunter, F. M. 1988. Extra-pair copulation and sperm competition in the zebra finch. Nature, Lond., 334, 60–62. Burley, N. 1986. Sexual selection for aesthetic traits in species with biparental care. Am. Nat., 127, 415–445. Chase, I. D. 1980. Cooperative and non-cooperative behavior in animals. Am. Nat., 115, 827–857.
Clutton-Brock, T. H. 1984. Reproductive effort and terminal investment in iteroparous animals. Am. Nat., 123, 212–229. Clutton-Brock, T. H. 1991. The Evolution of Parental Care. Princeton: Princeton University Press. Colegrave, N., Birkhead, T. R. & Lessells, C. M. 1995. Sperm precedence in zebra finches does not require special mechanisms of sperm competition. Proc. R. Soc. Lond. Ser. B, 259, 223–228. Davies, N. B., Hatchwell, B. J., Robson, T. & Burke, T. 1992. Paternity and parental effort in dunnocks, Prunella modularis: how good are male chick-feeding rules? Anim. Behav., 43, 729–745. de Lope, F. & Møller, A. P. 1993. Female reproductive effort depends on the degree of ornamentation of their mates. Evolution, 47, 1152–1160. Dixon, A., Ross, D., O’Malley, S. L. C. & Burke, T. 1994. Paternal investment inversely related to degree of extra-pair paternity in the reed bunting. Nature, Lond., 371, 698–700. Freeman-Gallant, C. R. 1996. DNA fingerprinting reveals female preference for male parental care in savannah sparrows. Proc. R. Soc. Lond. Ser. B, 263, 157–160. Gavin, T. A. & Bollinger, E. K. 1985. Multiple paternity in a territorial passerine: the bobolink. Auk, 102, 550–555. Gowaty, P. A. In press. Field studies of parental care in birds: new data focus questions on variation among females. Adv. Study Behav. Gray, E. M. 1996. Female control of offspring paternity in a western population of red-winged blackbirds (Agelaius phoeniceus). Behav. Ecol. Sociobiol., 38, 267–278. Hasselquist, D., Bensch, S. & von Schantz, T. 1996. Correlation between male song repertoire, extra-pair paternity and offspring survival in the great reed warbler. Nature, Lond., 381, 229–232. Hoelzer, G. A. 1989. The good parent process of sexual selection. Anim. Behav., 38, 1067–1078. Houston, A. I. & Davies, N. B. 1985. The evolution of cooperation and life history in the dunnock Prunella modularis. In: Behavioural Ecology: Ecological Consequences of Adaptive Behaviour (Ed. by R. M. Sibley & R. H. Smith), pp. 471–487. Oxford: Blackwell Scientific Publications. Kempenaers, B. & Sheldon, B. C. 1996. Why do male birds not discriminate between their own and extrapair offspring? Anim. Behav., 51, 1165–1173. Kempenaers, B., Verheyen, G. R., Van den Broeck, M., Burke, T., Van Broeckhoven, C. & Dhondt, A. A. 1992. Extra-pair paternity results from female preference for high-quality males in the blue tit. Nature, Lond., 357, 494–496. Lessells, C. M. 1991. The evolution of life-histories. In: Behavioural Ecology. 3rd edn (Ed. by J. R. Krebs & N. B. Davies), pp. 32–68. Oxford: Blackwell. Lifjeld, J. T. & Slagsvold, T. 1989. Allocation of parental investment by polgynous pied flycatcher males. Ornis Fenn., 66, 3–14. Lifjeld, J. T., Dunn, P. O., Robertson, R. J. & Boag, P. T. 1993. Extra-pair paternity in monogamous tree swallows. Anim. Behav., 45, 213–229.
Commentaries Lubjuhn, T., Curio, E., Muth, S. C., Brün, J. & Epplen, J. T. 1993. Influence of extra-pair paternity on parental care in great tits Parus major. In: DNA Fingerprinting: State of the Science (Ed. by S. D. J. Pena, R. Chakraborty, J. T. Epplen & A. J. Jeffreys), pp. 379– 385. Basel: Birkhaüser. Møller, A. P. 1992. Frequency of copulations with multiple males and sexual selection. Am. Nat., 139, 1089–1101. Møller, A. P. 1994. Symmetrical male sexual ornaments, paternal care, and offspring quality. Behav. Ecol., 5, 188–194. Morton, E. S., Forman, L. & Braun, M. 1990. Extrapair fertilizations and the evolution of colonial breeding in purple martins. Auk, 107, 275–283. van Noordwijk, A. J. & de Jong, G. 1986. Acquisition and allocation of resources: their influence on variation in life history tactics. Am. Nat., 128, 137–142. Partridge, L. & Harvey, P. H. 1985. Costs of reproduction. Nature, Lond., 316, 20. Petrie, M. & Williams, A. 1993. Peahens lay more eggs for peacocks with larger trains. Proc. R. Soc. Lond. Ser. B, 251, 127–131. Price, T., Schluter, D. & Heckman, N. E. 1993. Sexual selection when the female directly benefits. Biol. J. Linn. Soc., 48, 187–211. Sheldon, B. C. 1994. Sperm competition in the chaffinch: the role of the female. Anim. Behav., 47, 163–173. Sheldon, B. C., Räsänen, K. & Dias, P. C. In press. Certainty of paternity and paternal effort in the collared flycatcher. Behav. Ecol. Smith, H. G., Montgomerie, R., Poldmaa, T., White, B. N. & Boag, P. T. 1991. DNA fingerprinting reveals relation between tail ornament and cuckoldry in barn swallows. Behav. Ecol., 2, 90–98. Stutchbury, B. J., Rhymer, J. M. & Morton, E. S. 1994. Extrapair paternity in hooded warblers. Behav. Ecol., 5, 384–392. Sundberg, J. & Dixon, A. 1996. Old, colourful male yellowhammers, Emberiza citrinella, benefit from extra-pair copulations. Anim. Behav., 52, 113–122.
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Verhulst, S. & Tinbergen, J. M. 1991. Experimental evidence for a causal relationship between timing and success of reproduction in the great tit Parus m. major. J. Anim. Ecol., 60, 269–282. Wagner, R. H., Schug, M. D. & Morton, E. S. 1996. Confidence of paternity, actual paternity and parental effort by purple martins. Anim. Behav., 52, 123–132. Werren, J. H., Gross, M. R. & Shine, R. 1980. Paternity and the evolution of male parental care. J. theor. Biol., 82, 619–631. Westneat, D. F. 1988. Parental care and extra-pair copulations in the indigo bunting. Auk, 105, 149–160. Westneat, D. F. 1995. Paternity and paternal behaviour in the red-winged blackbird, Agelaius phoeniceus. Anim. Behav., 49, 21–35. Westneat, D. F. & Sargent, R. C. 1996. Sex and parenting: the effects of sexual conflict and parentage on parental strategies. Trends Ecol. Evol., 11, 87–91. Westneat, D. F. & Sherman, P. W. 1993. Parentage and the evolution of parental behavior. Behav. Ecol., 4, 66–77. Whittingham, L. A. 1994. Additional mating opportunities and male parental care in red-winged blackbirds. Anim. Behav., 48, 875–883. Whittingham, L. A. & Lifjeld, J. T. 1995. High parental investment in unrelated young: extra-pair paternity and male parental care in house martins. Behav. Ecol. Sociobiol., 37, 103–108. Whittingham, L. A., Taylor, P. D. & Robertson, R. J. 1992. Confidence in paternity and male paternal care. Am. Nat., 139, 1115–1125. Winkler, D. W. 1987. A general model for parental care. Am. Nat., 130, 526–543. Wright, J. & Cotton, P. A. 1994. Experimentally induced differences in parental care: an effect of certainty of paternity. Anim. Behav., 47, 1311–1322. Wright, J. & Cuthill, I. 1990. Biparental care: short term manipulation of partner contribution and brood size in the starling, Sturnus vulgaris. Behav. Ecol., 1, 116–124.
COMMENTARIES Studying paternity and paternal care: pitfalls and problems BART KEMPENAERS* & BEN C. SHELDON† *Konrad Lorenz Institute for Comparative Ethology, Vienna †Institute of Cell, Animal & Population Biology, University of Edinburgh (Received 15 August 1996; initial acceptance 6 September 1996; final acceptance 12 November 1996; MS. number: -1086)
Theoretical treatments of the relationship between paternity (or certainty of paternity) and paternal care predict, under certain conditions, that individual males should invest less in paternal care if their paternity is reduced (Whittingham et al. 1992; Westneat & Sherman 1993). Several recent papers have addressed this question using information about males’ genetic paternity from unmanipulated breeding attempts together with measures of those males’ contributions to some components of parental care (Table I). The general picture that emerges from these studies is that there is no positive relationship between paternity and paternal effort (although in some studies the sample size was small, and statistical power limited). However, we argue here that it is inappropriate to use data of this kind to test models relating paternity to paternal care. We discuss the sort of data that can provide a better test. Models of optimal paternal care in response to variation in paternity are based on the effects of trade-offs between current reproductive effort and future reproductive success (Westneat & Sargent 1996). They ask, in effect, what the optimal response in terms of parental effort would be for an individual male responding to a change in paternity. Individuals may lie at different positions along a trade-off between current and future reproduction, and may also experience qualitatively different trade-offs because of (for example) differences in resource availability (van Noordwijk & de Jong 1986). As a consequence, one cannot assume that all males within a Correspondence: B. C. Sheldon, Department of Zoology, Uppsala University, Villava¨gen 9 S-752 36 Uppsala, Sweden (email: [email protected]). Bart Kempenaers is at KLIVV, Savoyenstrasse 1a, A-1160 Vienna, Austria. 0003–3472/97/020423+05 $25.00/0/ar960377
?
population will be subject to the same rules relating paternity to paternal effort. We illustrate this argument and its consequences by considering three different cases that are likely to obscure relationships between paternity and paternal care at the population level. These can be summarized as resulting from (1) different optimal levels of care for different individuals, (2) the interdependence of paternal and maternal care and (3) differing trade-offs between paternal care and mating opportunities faced by different individuals. The points that we make here are simple, have general applicability to many problems in behavioural ecology, and similar points have been made many times before in different contexts (for example in discussions of the pros and cons of nonexperimental studies of the costs of reproduction: Partridge & Harvey 1985; Lessells 1991). Nevertheless, it is our impression that they are not given adequate consideration in most of the studies referred to in Table I. Experimental studies of birds have demonstrated that paternal care may be costly, in terms of reduced survival, breeding or mating opportunities (reviewed in Clutton-Brock 1991). As a consequence, allocation of resources to paternal care is expected to be individually optimized, as with other life-history traits such as clutch size. For example, males in poor condition might reduce their parental care, if the cost of a single ‘unit’ of parental care was greater for males in poor condition. An increasing number of studies have related parentage in natural populations to the relative magnitude of condition-dependent secondary sexual characters (Smith et al. 1991; Hasselquist et al. 1996; Sundberg & Dixon 1996), and there are good reasons to expect such relationships to be rather common (Møller 1992). 1997 The Association for the Study of Animal Behaviour
423
424
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Table I. Published studies investigating the relationship between genetic parentage and level of parental care by male birds Species Bobolink, Dolichonyx oryzivorus* Indigo bunting, Passerina cyanea† Purple martin, Progne subis* Great tit, Parus major‡ Tree swallow, Tachycineta bicolor* Hooded warbler, Wilsonia citrina* Red-winged blackbird, Agelaius phoenicus§ House martin, Delichon urbica** Purple martin**
Sample size
Relationship
Study
7 41 21 15 12 12 Variable (up to 93) 10 15
r=0.59, P=0.01 rS =0.42 rS =0.08
Gavin & Bollinger 1985 Westneat 1988 Morton et al. 1990 Lubjuhn et al. 1993 Lifjeld et al. 1993 Stutchbury et al. 1994 Westneat 1995
"0.31¦rS¦0.03 "0.15¦rS¦0.16
Whittingham & Lifjeld 1995 Wagner et al. 1996
Sample size is the number of nests for which information on paternity and paternal care was available; with the exception of Lubjuhn et al. (1993), no relationships are statistically significant (P>0.05). *Share of nestling feeding by male. †Measure of care by male was whether the male fed nestlings. ‡Index of nest defence by male. §Several different relationships examined. **Three different measures of paternal care.
Hence, both paternity and the extent of paternal care may be causally related to a third variable, in this case condition. The simplest expectation is that males in poor condition will make a small contribution to parental care, and achieve low paternity, whereas the reverse will be true for males in good condition. This would generate a positive correlation between paternity and paternal care, although the relationship would not be causal. It is also possible however, that a male in poor condition might be selected to increase his share of parental care, if his future prospects were very low (e.g. in cases of ‘terminal investment’: Clutton-Brock 1984). In this case, the correlation between paternity and paternal care might disappear, or even become negative. The potential benefits of parental care may also vary, for example in relation to timing of breeding: in many bird species reproductive success declines with breeding date, and there is evidence that this relationship is causal (e.g. Verhulst & Tinbergen 1991). As a consequence, one might expect lower levels of parental care in broods that are worth less. If there were also a tendency for later broods to contain more extra-pair young, as Møller (1992) has suggested may be the case, one might also expect a positive relationship between paternity and paternal care, but again not the result of a direct effect of paternity on paternal care. The proportion of care that one member of a pair makes will depend upon the contribution that
the other pair member makes (Chase 1980; Wright & Cuthill 1990). The division of parental effort between mates can be understood as an evolutionarily stable strategy whose equilibrium depends upon the relative costs and benefits of investment to the male and female (Houston & Davies 1985; Winkler 1987). Above, we argue that variation in condition between males may affect the extent to which they invest in the current breeding attempt; the same applies to females, which can potentially affect the share of parental care performed by males. For example, imagine a species in which females compete for settlement with the most attractive males, so that females in poorer condition are more likely to pair with unattractive males, with the result that they are also more likely to engage in extra-pair copulations. In this case, lower investment by females, and compensation by males, could lead to a negative relationship between paternity and paternal care, or obscure the males’ response to lowered paternity. Burley (1986) proposed that a female might be prepared to invest more in care for offspring if mated to an attractive male, and evidence from Burley’s study and others (e.g. de Lope & Møller 1993; Petrie & Williams 1993; Møller 1994) supports this suggestion. The interpretation of Burley’s differential investment model is that (1) male attractiveness acts as an indicator of heritable fitness differences and (2), as a consequence,
Commentaries offspring sired by attractive males are of greater value to a female than those sired by unattractive males, and hence worth greater parental investment by the female. Therefore, a female may make a greater share of parental effort when mated to an attractive male (with the result that the male’s share declines), while at the same time being less likely to engage in extra-pair copulations with other males. Hence, differential investment by females might be responsible for a negative correlation between paternity and paternal care. Further complication is added when one considers how a female should respond when mated to a relatively unattractive male, when some of her offspring have been sired by an attractive extra-pair male. In this case, a prediction of the differential allocation hypothesis is that these females would provide relatively more care to the brood as a whole (since discrimination of chicks based upon paternity is unlikely: Davies et al. 1992; Kempenaers & Sheldon 1996), which would potentially affect the strength and sign of any correlation between paternity and paternal care resulting from differential allocation by females. In some of the earlier models that investigated the relationship between paternity and optimal levels of paternal care, the costs of paternal care were expressed in terms of lost mating opportunities (e.g. Werren et al. 1980). In species with multiple breeding attempts within a season, or with a high degree of breeding asynchrony, a male might face a trade-off between investing in the current breeding attempt and pursuing other mating opportunities, either through polygyny or extra-pair copulation. However, this trade-off may not be the same for all males. It is not unreasonable to expect that the extent to which males pursue extra mating opportunities will be partly determined by their likelihood of gaining extra matings. Thus attractive males, or males in good physiological condition, may be able to expend more effort in gaining extra mating opportunities, at the expense of investment in the current brood. If the factors that determine a male’s pursuit of extra matings are related to those that determine a male’s paternity, there may exist a negative correlation between paternity and paternal effort. Similarly, in polygynous species, a trade-off may exist between investing in paternal care and guarding another female. Whittingham (1994)
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showed experimentally that male red-winged blackbirds did not feed offspring if they had an additional mate in her fertile period breeding on their territory (see also Lifjeld & Slagsvold 1989). This might influence the relationship between paternity and paternal care if, for example, males that were more successful in attracting multiple females were also less likely to lose paternity. We have outlined three ways in which relationships may exist between paternity and paternal care, without there being a causal link between the two, and other scenarios could doubtless be suggested. For example, some models of the evolution of male sexual ornaments postulate that they have evolved partly as a reliable signal of male parental care ability (e.g. Hoelzer 1989; Price et al. 1993), in which case paternity and paternal care may be further confounded. In two of the cases above, one can construct plausible arguments for the expected correlation between paternity and paternal care to be either positive or negative. It does not seem likely that quantitative predictions about the relative importance of the three cases that we have described above can be made in even the best studied systems at present. As a consequence, we argue that it is currently impossible to predict what relationship may be uncovered between paternity and paternal care in studies relying on correlations across individuals. It is quite possible that in all of the studies listed in Table I, a causal relationship between paternity and paternal care is masked by the influence of other variables. Therefore, there is little to be achieved by reporting relationships between paternity and paternal care in natural populations as a test of models of optimal levels of paternal care, since there can be no clear expectation of the form of the relationship, and even a positive relationship may result entirely from the influence of other variables. Carefully designed experiments provide one means to avoid the numerous problems associated with confounding variables affecting both paternity and paternal care. However, one difficulty empirical studies face is that it does not seem possible that males can directly measure their own paternity; rather, paternity and paternal care must be linked by a third variable, ‘certainty of paternity’. An experiment aiming to uncover a relationship between paternity and paternal care can only reasonably be expected to work if it also affects a male’s certainty of paternity, and in fact the latter
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is the only quantity that such an experiment needs to affect. Unfortunately, this quantity is at present unmeasurable, so that an experimenter must assume that an experiment has manipulated certainty of paternity. This assumption is most likely to be justifiable in cases where experiments mimic as closely as possible what happens when paternity is naturally reduced. For example, studies of several species demonstrate that females actively seek extra-pair copulations by visiting the territories of other males (Kempenaers et al. 1992; Sheldon 1994; Gray 1996). Thus, in these species at least, experiments involving male removal may not be good models for this process (Gowaty, in press), whereas removing a female for a short period might be more effective (e.g. Wright & Cotton 1994; Sheldon et al., in press). It is also important that experiments attempt, as far as is possible, to control for variation in date at which they are performed, relative to fertilization of eggs, since the timing of extra-pair copulations may affect their success (Birkhead et al. 1988; Colegrave et al. 1995). An alternative approach, which has proved fruitful (Dixon et al. 1994; Freeman-Gallant 1996), is to restrict comparisons of paternity and paternal care to successive breeding attempts by the same pair. By doing this one potentially controls for many (but conceivably not all) sources of variation between individual breeding attempts. In conclusion, we believe that there is little to be learnt from the reporting of relationships between paternity and paternal care in unmanipulated populations as tests of models of optimal paternal care. Further testing of models relating paternity to paternal care requires careful consideration of potentially confounding variables and the behavioural mechanisms that relate paternity to paternal care. We are grateful to Tim Birkhead, Nick Davies, Jan Lifjeld, Josephine Pemberton, Hans Winkler and an anonymous referee for comments. B.C.S. was supported by a research fellowship from NERC (UK). REFERENCES Birkhead, T. R., Pellatt, J. E. & Hunter, F. M. 1988. Extra-pair copulation and sperm competition in the zebra finch. Nature, Lond., 334, 60–62. Burley, N. 1986. Sexual selection for aesthetic traits in species with biparental care. Am. Nat., 127, 415–445. Chase, I. D. 1980. Cooperative and non-cooperative behavior in animals. Am. Nat., 115, 827–857.
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