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Can older males deliver the good genes?
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Can older males deliver the good genes? Robert Brooks and Darrell J. Kemp Females of many species choose to mate with old rather than young males, possibly because older males pass superior genes on to their offspring. Recent theoretical and empirical investigations have rejuvenated interest in the evolution of mating preferences based on age, and in the relationship between longevity and fitness. If the cost of signalling is a reduction in future survival and reproduction, mate choice based on age is one possible outcome when males signal their genetic quality.These recent investigations highlight the importance of understanding sexual selection from a life-history perspective.
Females often obtain direct benefits from their chosen mate1. However, the idea that females can also benefit from mate choice indirectly, because attractive males bequeath superior genes to the offspring, has been controversial from the start1,2 (Box 1). It has been argued that, merely by surviving, older males provide the simplest possible demonstration of their high genetic quality for viability3,4. By contrast, cohorts of young males include males of both high and of low viability. Older males are, therefore, on average, a better bet as mates, and should be preferred by females. It is an idea that is intuitively appealing, but, until recently, it has avoided the rigorous theoretical exploration
and zealous empirical testing that have otherwise been hallmarks of the study of sexual selection. Our review focuses on the idea at the centre of this agebased indicator mechanism (AIM): whether older males are adaptively superior to younger ones, and, therefore, whether they confer genetic benefits on their offspring. This idea is important, not only because of what it tells us about mate choice, but also because it is the key to an exciting new synthesis between two mainstays of modern evolutionary ecology: sexual selection and life-history theory5–8. In an early verbal formulation of the AIM, Manning4 argued that, as a cohort of males ages, individuals carrying deleterious prezygotic mutations, and those that are poorly adapted to current environmental conditions, will be gradually eliminated by viability selection. Older individuals that have survived such selection should, therefore, be of higher average genetic quality than are younger individuals that have not3,4. Trivers, one of the earliest proponents of the idea, stressed that this mechanism only works ‘all other things being equal’3. However, other things are seldom, if ever, equal. For example,
Box 1.The evolution of mating preferences by direct and indirect selection
Robert Brooks School of Biological Science,The University of New South Wales, Sydney, NSW 2052, Australia. Darrell J. Kemp* School ofTropical Biology, James Cook University, Cairns, QLD 4870, Australia. *e-mail: [email protected]
A mating preference might evolve and/or be maintained by one (or a combination) of three processes: (1) Historic selection on aspects of the psychosensory system not necessarily associated originally with mate choicea; (2) Direct selection because chosen males provide resources or ameliorate the costs and risks of mating; and (3) Indirect selection that occurs when preference alleles become positively associated with other fitness alleles. The operation of sensory drive and direct selection are relatively straightforwarda–c. However, the importance of indirect selectionb and the process by which fitness and mate choice become genetically correlatedc–e are far more controversial. Genes for female preference might become genetically correlated with genes for attractive male display as a consequence of mate choice itself e, resulting in a self-reinforcing cycle of preference–display coevolution known as the Fisher process. Alternatively, if male displays indicate
additive genetic variation in other fitness components, such as viability, then the build up of a genetic correlation between preference and fitness component indirectly favours preference when the fitness component is exposed to natural selection.This type of process is known generally as the good-genes or indicator mechanismc.The age-based indicator mechanism (AIM) and viability-indicator mechanisms are special cases thereof. According to the AIM, females prefer to mate with older males because of the demonstrated longevity of the males (and thus, implicitly, their genes for viability). References a Endler, J.A. and Basolo, A. (1998) Sensory ecology, receiver biases and sexual selection. Trends Ecol. Evol. 13, 415–420 b Kirkpatrick, M. and Ryan, M.J. (1991) The evolution of mating preferences and the paradox of the lek. Nature 350, 33–38 c Andersson, M. (1994) Sexual Selection, Princeton University Press d Rowe, L. and Houle, D. (1996) The lek paradox and the capture of genetic variance by condition dependent traits. Proc. R. Soc. London B Biol. Sci. 263, 1415–1421 e Lande, R. (1981) Models of speciation by sexual selection on polygenic traits. Proc. Natl. Acad. Sci. U. S. A. 78, 3721–3725
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Box 2. Potential influences on the relationship between age and mate quality Factors promoting a positive relationship • Older males might provide higher-quality ejaculatesa, invest more in current offspringb or otherwise serve as better parentsb,c than do younger males. • Age might signal genetic quality (fewer deleterious prezygotic mutations and better adapted to current conditions) because older males have proven their viability by survivingd–f. Factors promoting a negative relationship • The accumulation of spontaneous germ-line mutations throughout the lifetime of an individual could see older males more likely to carry unconditionally deleterious viability mutationsg. • Late age viability and/or fertility might be negatively genetically correlated negatively with early adult viability and/or fertilityg. • In continually evolving populations, younger males might represent more viable mates because they are born from a better adapted gene poolf,g. • In resource-based (gift-givingh) mating systems in which male ejaculates contribute to female reproductive success, old (previously mated) males might be less able to produce high-quality ejaculatese,i. References a Zuk, M. (1988) Parasite load, body size, and age of wild-caught male field crickets (Orthoptera: Gryllidae): effects on sexual selection. Evolution 42, 969–976 b Curio, E. (1982) Why do young birds reproduce less well? Ibis 125, 400–404 c Komers, P.E. and Dhindsa, M.S. (1989) Influence of dominance and age on mate choice in black-billed magpies: an experimental study. Anim. Behav. 37, 645–655 d Trivers, R.L. (1972) Parental Investment and Sexual Selection; In Sexual Selection and the Descent of Man 1871–1971 (Campbell, B, ed.), pp. 136–179, Heinemann e Manning, J.T. (1985) Choosy females and correlates of male age. J. Theor. Biol. 116, 349–354 f Kokko, H. and Lindström, J. (1996) Evolution of female preference for old mates. Proc. R. Soc. London B Biol. Sci. 263, 1533–1538 g Hansen, T.F. and Price, D.K. (1995) Good genes and old age: Do old mates provide superior genes? J. Evol. Biol. 8, 759–778 h Savalli, U.M. and Fox, C.W. (1999) The effect of male mating history on paternal investment, fecundity and remating in the seed beetle Callobruchus maculatus. Func. Ecol. 13, 169–177 i Fox, C.W. et al. (1995) Male body size affects female lifetime reproductive success in a seed beetle. Anim. Behav. 50, 281–284
both Trivers3 and Manning4 realized that the oldest males are often the least fertile, which suggests a direct fitness cost to females that choose such males. Exactly how unequal other things (i.e. the differences between old and young males) are has rarely been addressed, but it is probably the key to the generality of the AIM. In one of the first attempts to model the relationship between age and good genes, Hansen and Price9 drew on quantitative genetic and life-history principles to argue that older individuals need not be genetically superior mates, but that the opposite should often prevail. Their argument was four pronged: (1) negative genetic correlations between early- and late-life fitness components are common if not the norm; (2) younger males are likely to have higher breeding values for fertility; (3) younger cohorts might be better adapted to current conditions because their parents were exposed to selection more recently than were those of older cohorts; and http://tree.trends.com
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(4) deleterious germ-line mutations occur over the lifetime of a male, significantly reducing the breeding value for fitness of older males (Box 2). For the first time in discussions about the AIM, the assertion that age indicates fitness was seriously challenged. Sexual attractiveness is a life-history issue
The fitness of an individual is a function of both survival and mating success. In most cases, however, these two fitness components cannot be maximized simultaneously10. Conditionally expressed traits that enhance competitive mating abilities, such as flashy ornaments, aggressive behaviours and sexual displays, often do so at the expense of other fitness components, including longevity11,12. In general terms, this is an example of the tradeoff between the allocation of resources to current reproductive effort, and residual reproductive value (RRV), which is a cornerstone of life-history theory7,10. The realization that sexual advertisement is functionally analogous to other forms of reproductive investment, and is subject to similar life-history tradeoffs7,9,12, is fundamental to recent progress in understanding the AIM (Refs 5,6,13,14). The most important point that Hansen and Price9 made was that adult survival might not be strongly, or even positively, correlated with total fitness. The ability to survive to maturity, attract mates and mate with them successfully might be more important determinants of lifetime reproductive success than is longevity. Male longevity will be correlated with fitness only if most of the genetic variation in fitness is attributable to alleles that are uniformly deleterious or beneficial across the lifetime of an individual. Genes that have antagonistic effects on early and late fitness components, and deleterious mutations that act only in older individuals will weaken any such correlation and, in the case of antagonistic genes, might even reverse it9. Determinants of condition: resource allocation versus acquisition
Under Hansen and Price’s model9, the only circumstance under which older males would bestow genetic advantages on their offspring is if fertility increases steeply with age: a situation that Hansen and Price judged to be generally uncommon. Their approach assumed that variation in important fitness components was largely a problem of how resources are allocated throughout the lifetime of an organism (i.e. the allocation to current versus future reproductive effort). The issue of resource allocation can be conveniently thought of as ‘dividing up a pie’, because devoting some of the pie to a particular trait necessarily means that there is less of the pie for other traits10. Hence, where variation in fitness is determined by allocation of resources among fitness components, tradeoffs between these components are likely to prevail10,15. However, there is a growing appreciation that positive genetic correlations among fitness components to which resources have to be allocated might be generated if there is additive
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Box 3. Evolutionary game theory and its relevance to age-based sexual advertisement Originally devised to model economic systems, the ‘theory of games’ was first explicitly applied in the context of individual optimization in biology by Maynard Smith and Pricea. Game theory recognizes the importance of frequency dependence in evolution, and is based on the premise that the ‘best’ strategy (behaviour and/or morphology) will depend on the strategies played by other members of the population. Game theoretic models seek to define evolutionarily stable strategies (ESSs) for particular situations. An ESS is defined as a strategy that renders a population of individuals playing that strategy incapable of being invaded by a mutant individual playing a different strategyb. ESSs can be
pure, where different individuals in the population only ever play one of several available tactics, or mixed, where individuals switch between available tactics conditionally with an ESSprescribed probability. Whereas classic life-history theory deals with maximization of fitness rather than with evolutionary stabilityc, game theory is crucial to studies linking sexual selection with life-history processes. Individuals are expected to maximize their inclusive fitness according to life-history tradeoffs, but the social environment will ultimately determine the nature and course of these tradeoffsc. Evolutionary game theory has proved particularly relevant to studies of intrasexual conflict, but can be equally
genetic variation in resource acquisition10,17 (metaphorically, where some individuals have relatively bigger ‘pies’ to divide in the first place). A simulation study by Kokko and Lindström13, in which males differed only in condition (which is largely analogous to resource acquisition18) and not in patterns of resource allocation, predicted that highquality (condition and/or acquisition) males would survive longer and provide genetic fitness benefits to their offspring. A similar study by Beck and Powell14 reiterated that old-age preference is possible in principle, but will depend on how survival is determined from genes for viability. Where adult survival is relatively important as a determinant of fitness, preferences for older males can evolve by a good-genes process13,14, whereas if juvenile survival is relatively important then females should prefer younger and intermediate-age mature males14. Mathematical simulation is valuable because it provides insights that are not possible from verbal arguments alone, particularly regarding the action and importance of individual variables to evolutionary processes. The models of Kokko and Lindström13 and Beck and Powell14 suggest that, in addition to how fitness components co-vary genetically, the pattern of age-dependent survival will influence the benefits of mate choice based on age, and thus the evolution of preferences. This might manifest itself as consistent differences among taxa in the importance of age-based mate choice resulting from differences in longevity, life history and the relative contributions of juvenile and adult survival to fitness. Age-dependent sexual advertisement
In reality, there is probably variation among individuals both in overall condition18 and in the way that condition is allocated to current reproductive effort, future survival and reproduction19. Kokko6 built a model in which males varied genetically in condition, http://tree.trends.com
applied to model optimal male display (ornamentation and behaviour) in the context of female choice. Kokko’s modeld employs an explicit ESS approach to determining the optimum levels of agespecific male display when mating success depends upon the level of advertisement by rivals, and where the costs of such display are paid in a life-historical currency. References a Maynard Smith, J. and Price, G.R. (1973) The logic of animal conflict. Nature 246, 15–18 b Maynard Smith, J. (1982) Evolution and the Theory of Games, Cambridge University Press c Svensson, E. and Sheldon, B.C. (1998) The social context of life history evolution. Oikos 83, 466–477 d Kokko, H. (1997) Evolutionary stable strategies of age-dependent sexual advertisement. Behav. Ecol. Sociobiol. 41, 99–107
which they allocated to fecundity (including sexual advertisement) and survival in a way that was optimal for their age. In this model, under many (but not all) circumstances, early and late fecundity and survival can all be positively correlated with one another, with overall fitness and with condition. This result lends new plausibility to the evolution of preferences for older males by a good-genes process, because condition-dependent sexual advertisement can reliably indicate longevity and overall fitness. In a separate model, Kokko5 explored the optimal strategy for males of differing quality (either high or low) to advertisement over time, accounting both for life-history tradeoffs between sexual advertisement and RRV, and for the level at which competitors advertise. This model was based on the principles of evolutionary game theory (Box 3), and hence searched for evolutionarily stable strategies (ESSs) of lifetime sexual advertisement. Most ESSs in this ‘sexual advertisement game’ resulted in males increasing their level of advertisement over time. Under some conditions, low-quality cohort members advertised at a higher level than did high-quality individuals (primarily because low-quality males might suffer a lower RRV cost to advertisement20), with the result that sexual advertisement was not always strictly honest. However, such cheating males always paid for it in later years such that advertisement across age classes was honest on average5. Viability costs in the model could be imposed by increased mortality from predation (on the basis of increased visual and/or acoustic conspicuousness), loss of energetic reserves, or social costs and the risk of injury in male–male contests. The model, therefore, has broad appeal and could be extended (in principle) to encompass age-related delays in other aspects of male reproductive investment, such as fighting and lekking behaviour and advertising parental care21. Previous theoretical
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treatments have also suggested that, on the basis of lifetime changes in RRV, males should delay potentially dangerous aggressive behaviours until later in life22. Clear empirical evaluation of this idea has proven notoriously difficult because of concomitant age-based changes in relative competitive ‘abilities’23. Is the AIM really useful?
The two theoretical treatments by Kokko5,6 demonstrate that females can derive a good-genes benefit from mating with old rather than with young males under a wide range of conditions. The correlation between male attractiveness and age is mediated by an increased investment in costly sexual advertisement with age, and is highly consistent with evidence that males of several species increase their level of sexual ornamentation and display as they get older24–27. Here, the age indicator mechanism becomes indistinguishable from the standard viability indicator model5. This leads us to ask: do we really need the AIM? It is less general than the viability indicator model in which females prefer signals of male breeding value for survival irrespective of whether they are correlated with age. Both viability-indicator models and the AIM suffer from a further lack of generality as a result of the fallacy of equating longevity with fitness. In essence, the goodgenes process requires only that sexual attractiveness and breeding value for lifetime fitness are reliably and positively correlated. As Kokko’s model shows, however, there are situations in which optimal levels of honest sexual advertisement are not correlated with age5, and thus preferences that evolve by the good-genes process will not favour older males. In fact, several authors have pointed out that, under some circumstances, males of high genetic quality might invest so much in advertisement that they live shorter lives than do low-quality males, yet still make the best mates6,28–30. Thus, viability-indicator models (including the AIM) have less explanatory power than do more general good-genes models. From a practical point of view, a negative (or null) correlation between age and male attractiveness would falsify the AIM and viabilityindicator models, but not the good-genes process30. Critically testing the good-genes process requires exhaustive quantitative genetic study (under field conditions) in which the genetic correlation between attractiveness and lifetime fitness is estimated. Despite our claim that the AIM is of limited use as a model of preference evolution, it has served a valuable heuristic purpose. Attempts to model it5,6,9 have forced the explicit realization that the costs that enforce honesty (on average) of sexual advertisement are in RRV and can be observed via age-dependent changes in sexual advertisement5,6. Cheating is possible5,6, but is kept to a low level because only high-quality males can advertise at a consistently high level without paying unacceptable penalties in other fitness components (e.g. survival11, caring for offspring19,20 and social dominance12). This applies both to signals of http://tree.trends.com
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indirect and direct benefits and suggests that the most generally reliable indicators of male quality will be those that draw upon cumulative lifetime investments20,31. Do females prefer older males?
Several studies report positive correlations between male age and male attractiveness to females (Table 1; Refs 6,13,32). Such a correlation is necessary evidence for the AIM, but it is not sufficient because genetic quality is not the only potential correlate of male age. In resource-based mating systems, females could gain direct benefits from old mates: if RRV declines with age then older males are expected to invest relatively more effort in current broods33 and thus to be harder-working mates33,34. Furthermore, male parental ability could increase with age because of accumulated experience in specific parental duties, or as a result of increased foraging efficiency33,35. Other male traits, such as territory-defending ability and ejaculate quality might co-vary with age; however, in many groups, paternal investment in the form of ejaculate quality declines with successive matings36 and hence, possibly, with age37. The presence of direct benefits might, therefore, obscure a clear empirical evaluation of ‘good-genes’ explanations and, in particular, the AIM. Support for the AIM should include demonstrations of age-dependent choice in the absence of any direct benefits. Such evidence exists for several species (Table 1), but the correlative evidence is by no means unanimous. There are several counterexamples of no age-based preference and of preference for intermediate or younger males (Table 1)32. Evidence from extra-pair copulations (EPCs) in birds make particularly good tests because females are thought to engage in EPCs primarily to gain genetic benefits24,25,38–40. If female choice is for good genes (rather than for attractive, diverse or compatible genes), then male success through EPCs should increase with age. Recent empirical studies of cuckoldry provide both supporting and opposing evidence for this prediction (Table 1). A recent meta-analysis of 22 such studies41 also reports a weak positive correlation between age and own-nest paternity. Male age, therefore, appears generally related to extra-pair paternity in the direction suggested by the AIM, but this effect is far from unequivocal. Based on the evidence, it is therefore prudent to reject the AIM and the viability-indicator model as general hypotheses of the evolution of mate choice by indirect selection. However, null and negative correlations between age and sexual attractiveness remain consistent with more general good-genes models5,6,9,28–30, and an important challenge is now to test these more inclusive formulations. Delivering the good genes
Our rejection of the AIM and viability-indicator hypotheses as general models is not a statement that females derive no indirect benefits from mating with older or more long-lived males. It merely reflects the
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Table 1. Summary of recent evidence potentially relevant to the age-based indicator mechanism Key recent examples Nature of evidence
Supporta
Species
Choice contextb
Refs
Females prefer older males: (a) When male age is potentially correlated with resources
(b) When male age is not
+
European starling, Sturnus vulgaris
TP
26
+
Field crickets, Gryllus bimaculatus, G. veletis, G. pennsylvanicus
T
43,44
+
Great reed warbler, Acrocephalus arundinaceus
TP
45
+
Redlip blenny, Ophioblennius atlanticus
T
46
+
Blue tit, Parus caeruleus
EPC
40
+
Bullock's oriole, Icterus galbula bullockii
EPC
27
–
Red-winged blackbirds, Agelaius phoeniceus
EPC
47
+
Fallow deer, Dama dama
TE
48
–
Hooded warbler, Wilsonia citrina
EPC
49
+
House sparrow, Passer domesticus
EPC
24
+
Purple martins, Progne subis
EPC
39
–
Sandfly, Lutzomyia longipalpis
LEK
32
+
Yellowhammer, Emberiza citrinella
EPC
25
–
Yellow warbler, Dendroica petechia
EPC
50
better than do those of younger
–
Fruit fly, Drosophila melanogaster
NA
42
males
–
Sandfly, L. longipalpis
NA
32
correlated with resources
Offspring of older males perform
aKey:+
indicates positive support for the evidence; – indicates contradiction.
bAbbreviations:
EPC, choice of extrapair mate; LEK, choice of lekking mate; TE, choice inferred by timing of estrus; TP, choice of territorial
partner (with pair-bonds); T, choice of territorial mate (no pair bonds); NA, no choice mating experiment.
fact that these hypotheses hold up only as long as age and longevity are positively correlated with fitness, a somewhat arbitrary restriction. In evaluating more inclusive good-genes models, it is still worthwhile to ask whether females derive genetic benefits when they mate with older males. The indirect benefit of mate choice (including preferring older males) is the genetic inheritance of fitness by the mutual offspring. Testing of the mechanism, therefore, requires quantitative genetic evidence that the offspring of preferred older males are fitter than are those of other males. Although such tests require experimental designs that are so large as to be prohibitive in many animal systems, two recent laboratory studies of this nature have been attempted. In the first example, five-week-old male Drosophila melanogaster were found to sire offspring that were slightly less likely to survive to maturity than were those sired by two-day-old and two-week-old males42. There were no significant differences among the sire types in the mating ability of sons or the fecundity of daughters. Thus, if anything, younger males sire fitter offspring than extremely old males, but the effects of sire age on offspring fitness appear to be weak – perhaps too weak to provide a fitness benefit to females that discriminate among males based on their age. It is important to note, however, that there is no evidence of a natural correlation between male attractiveness and age in D. melanogaster, making it a potentially poor model for testing the benefits of preferring older mates. http://tree.trends.com
In the second example, Jones et al.32 showed that females of the lekking sandfly Lutzomyia longipalpis preferred to mate with males of intermediate age (four to six days old) over young (zero to two days old) or old (eight to ten days old) males. None of the measures of female reproductive success from these matings, including the number and proportion of eggs hatched, varied significantly in relation to the age class of the mate. However, when virgin females were mated at random to a male from one of the three age groups, hatching success of eggs sired by older males was significantly lower. This might be because of a negative genetic correlation between male longevity and offspring survival to hatching, or it might represent lower sperm number or performance in older males. Unfortunately, post-hatching performance of offspring is not reported and so it is impossible to tell whether sire age influenced further important components of offspring fitness. Thus, although the insights gained from these studies are limited, they do take an important step towards directly quantifying the fitness consequences of mate choice based on age. Conclusion
Females that mate with old rather than with young males might receive indirect (genetic) fitness benefits under many circumstances, but such benefits are not universal. This is reflected empirically in the findings that females often prefer old males, but that they can also prefer younger or intermediate-aged males or even disregard age entirely. The AIM, and viability-indicator
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Acknowledgements The authors would like to thank Michael Jennions, Hanna Kokko and the anonymous referees for helpful discussions and comments on the article. RB was supported by an Australian Postdoctoral Fellowship and an ARC Large grant. DJK was supported by an Australian Postgraduate Research Award.
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models of indirect benefits are falsified by these latter findings. In their place is now a more inclusive understanding of what ‘good genes’ are. The usefulness of the AIM is its historic role in shaping the realization that sexually selected traits should be viewed within a lifehistory context because it is here that the costs of these traits are exacted. Just as behavioural ecologists have rarely considered life-history constraints explicitly7, life historians have traditionally ignored the influences of a social environment on life-history evolution8. Clearly, workers in both fields will benefit from more explicit consideration of the interplay between them7,8. Empirically isolating the effect of age per se on female choice is a difficult assignment, given the
References 1 Andersson, M. (1994) Sexual Selection, Princeton University Press 2 Kirkpatrick, M. and Ryan, M.J. (1991) The evolution of mating preferences and the paradox of the lek. Nature 350, 33–38 3 Trivers, R.L. (1972) Parental investment and sexual selection. In Sexual Selection and the Descent of Man 1871–1971 (Campbell, B., ed.), pp. 136–179, Heinemann 4 Manning, J.T. (1985) Choosy females and correlates of male age. J. Theor. Biol. 116, 349–354 5 Kokko, H. (1997) Evolutionary stable strategies of age-dependent sexual advertisement. Behav. Ecol. Sociobiol. 41, 99–107 6 Kokko, H. (1998) Good genes, old age and lifehistory trade-offs. Evol. Ecol. 12, 739–750 7 Höglund, J. and Sheldon, B.C. (1998) The cost of reproduction and sexual selection. Oikos 83, 478–483 8 Svensson, E. and Sheldon, B.C. (1998) The social context of life history evolution. Oikos 83, 466–477 9 Hansen, T.F. and Price, D.K. (1995) Good genes and old age: Do old mates provide superior genes? J. Evol. Biol. 8, 759–778 10 Reznick, D. et al. (2000) Big houses, big cars, superfleas and the costs of reproduction. Trends Ecol. Evol. 15, 421–425 11 Cordts, R. and Partridge, L. (1996) Courtship reduces longevity of male Drosophila melanogaster. Anim. Behav. 52, 269–278 12 Gosling, L.M. et al. (2000) Life history costs of olfactory status signalling in mice. Behav. Ecol. Sociobiol. 48, 328–332 13 Kokko, H. and Lindström, J. (1996) Evolution of female preference for old mates. Proc. R. Soc. London B Biol. Sci. 263, 1533–1538 14 Beck, C.W. and Powell, L.A. (2000) Evolution of female mate choice based on male age: are older males better mates? Evol. Ecol. Research 2, 107–118 15 Houle, D. (1991) Genetic covariance of fitness correlates: what genetic correlations are made of and why it matters. Evolution 45, 630–648 16 van Noordwijk, A.J. and de Jong, G. (1986) Acquisition and allocation of resources: their influence on variation in life history tactics. Am. Nat. 128, 137–142 17 Glazier, D.S. (2000) Trade-offs between reproductive and somatic (storage) investments in animals: a comparative test of the van Noordwijk and de Jong model. Evol. Ecol. 13, 539–555 18 Rowe, L. and Houle, D. (1996) The lek paradox and the capture of genetic variance by condition dependent traits. Proc. R. Soc. London B Biol. Sci. 263, 1415–1421 http://tree.trends.com
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added complications inherent in separating direct and indirect benefits of choice. It might pay empiricists to switch focus from documenting the relationship between age, attractiveness, display and offspring performance to understanding how these traits trade off. Comparative and interpopulation studies might address how age-dependent mortality influences investment in sexual signalling and other costly reproductive behaviours. Within populations, attempts to partition the relative importance of the acquisition of condition and the allocation of condition to sexual display and survival promise to significantly advance our understanding of the genetic benefits of mate choice.
19 Gustafsson, L. et al. (1995) Trade-offs between lifehistory traits and a secondary sexual character in male collared flycatchers. Nature 375, 311–313 20 Candolin, U. (2000) Increased signalling effort when survival prospects decrease: male–male competition ensures honesty. Anim. Behav. 60, 417–422 21 Kokko, H. (1998) Should advertising parental care be honest? Proc. R. Soc. London B Biol. Sci. 265, 1871–1878 22 Parker, G.A. (1974) Assessment strategy and the evolution of fighting behaviour. J. Theor. Biol. 47, 223–243 23 Komers, P.E. et al. (1997) Age at first reproduction in male fallow deer: age-specific versus dominancespecific behaviors. Behav. Ecol. 8, 456–462 24 Wetton, J.H. et al. (1995) Single-locus DNA fingerprinting reveals that male reproductive success increases with age through extra-pair paternity in the house sparrow (Passer domesticus). Proc. R. Soc. London B Biol. Sci. 260, 91–98 25 Sundberg, J. and Dixon, A. (1996) Old, colourful male yellowhammers, Emberiza citrinella, benefit from extra-pair copulations. Anim. Behav. 52, 113–122 26 Mountjoy, D.J. and Lemon, R.E. (1996) Female choice for complex song in the European starling: a field experiment. Behav. Ecol. Sociobiol. 65, 65–71 27 Richardson, D.S. and Burke, T. (1999) Extra-pair paternity in relation to male age in Bullock’s orioles. Mol. Ecol. 8, 2115–2126 28 Grafen, A. (1990) Biological signals as handicaps. J. Theor. Biol. 144, 517–546 29 Eshel, I. et al. (2000) On Fisher–Zahavi’s handicapped sexy son. Evol. Ecol. Research 2, 509–523 30 Kokko, H. Fisherian vs. ‘good genes’ mate preference: what is the crucial test? Ecol. Lett. (in press) 31 Kokko, H. et al. (1999) Female choice selects for lifetime lekking performance in black grouse males. Proc. R. Soc. London B Biol. Sci. 266, 2109–2115 32 Jones, T.M. et al. (2000) Adaptive female choice for middle-aged mates in a lekking sandfly. Proc. R. Soc. London B Biol. Sci. 267, 681–686 33 Curio, E. (1983) Why do young birds reproduce less well? Ibis 125, 400–404 34 Komers, P.E. and Dhindsa, M.S. (1989) Influence of dominance and age on mate choice in blackbilled magpies: an experimental study. Anim. Behav. 37, 645–655 35 Sætre, G-P. et al. (1995) Food provisioning in the pied flycatcher: do females gain direct benefits from choosing bright-coloured males? J. Anim. Ecol. 64, 21–30
36 Savalli, U.M. and Fox,C.W. (1999) The effect of male mating history on paternal investment, fecundity and remating in the seed beetle Callobruchus maculatus. Func. Ecol. 13, 169–177 37 Fox, C.W. et al. (1995) Male body size affects female lifetime reproductive success in a seed beetle. Anim. Behav. 50, 281–284 38 Hasselquist, D. et al. (1996) Correlation between male song repertoire, extra-pair paternity and offspring survival in the great reed warbler. Nature 381, 229–233 39 Wagner, R.H. et al. (1996) Condition-dependent control of paternity by female purple martins: implications for coloniality. Behav. Ecol. Sociobiol. 38, 379–389 40 Kempenaers, B. et al. (1997) Extrapair paternity in the blue tit (Parus caeruleus): female choice, male characteristics and offspring quality. Behav. Ecol. 8, 481–492 41 Møller, A.P. and Ninni, P. (1998) Sperm competition and sexual selection: a meta-analysis of paternity studies in birds. Behav. Ecol. Sociobiol. 43, 345–358 42 Price, D.K. and Hansen, T.F. (1998) How does offspring quality change with age in male Drosophila melanogaster? Behav. Genet. 28, 395–402 43 Simmons, L.W. and Zuk, M. (1992) Variability in call structure and pairing success of male field crickets, Gryllus bimaculatus: the effects of age, size and parasite load. Anim. Behav. 44, 1145–1152 44 Zuk, M. (1988) Parasite load, body size, and age of wild-caught male fields crickets (Orthoptera: Gryllidae): effects on sexual selection. Evolution 42, 969–976 45 Hasselquist, D. (1998) Polygyny in great reed warblers: a long term study of factors contributing to male fitness. Ecology 79, 2376–2390 46 Côté, I.M. and Hunte, W. (1993) Female redlip blennies prefer older males. Anim. Behav. 46, 203–205 47 Westneat, D.F. (1993) Polygyny and extrapair fertilizations in eastern red-winged blackbirds (Agelaius phoeniceus). Behav. Ecol. 4, 49–60 48 Komers, P.E. et al. (1999) Timing of estrus in fallow deer is adjusted to the age of available mates. Am. Nat. 153, 431–436 49 Stutchbury, B.J.M. et al. (1997) Correlates of extrapair fertilization success in hooded warblers. Behav. Ecol. Sociobiol. 40, 119–126 50 Yezerinac, S.M. and Weatherhead, P.J. (1997) Extra-pair mating, male plumage coloration and sexual selection in yellow warblers (Dendroica petechia). Proc. R. Soc. London B Biol. Sci. 264, 527–532
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Can older males deliver the good genes? Robert Brooks and Darrell J. Kemp Females of many species choose to mate with old rather than young males, possibly because older males pass superior genes on to their offspring. Recent theoretical and empirical investigations have rejuvenated interest in the evolution of mating preferences based on age, and in the relationship between longevity and fitness. If the cost of signalling is a reduction in future survival and reproduction, mate choice based on age is one possible outcome when males signal their genetic quality.These recent investigations highlight the importance of understanding sexual selection from a life-history perspective.
Females often obtain direct benefits from their chosen mate1. However, the idea that females can also benefit from mate choice indirectly, because attractive males bequeath superior genes to the offspring, has been controversial from the start1,2 (Box 1). It has been argued that, merely by surviving, older males provide the simplest possible demonstration of their high genetic quality for viability3,4. By contrast, cohorts of young males include males of both high and of low viability. Older males are, therefore, on average, a better bet as mates, and should be preferred by females. It is an idea that is intuitively appealing, but, until recently, it has avoided the rigorous theoretical exploration
and zealous empirical testing that have otherwise been hallmarks of the study of sexual selection. Our review focuses on the idea at the centre of this agebased indicator mechanism (AIM): whether older males are adaptively superior to younger ones, and, therefore, whether they confer genetic benefits on their offspring. This idea is important, not only because of what it tells us about mate choice, but also because it is the key to an exciting new synthesis between two mainstays of modern evolutionary ecology: sexual selection and life-history theory5–8. In an early verbal formulation of the AIM, Manning4 argued that, as a cohort of males ages, individuals carrying deleterious prezygotic mutations, and those that are poorly adapted to current environmental conditions, will be gradually eliminated by viability selection. Older individuals that have survived such selection should, therefore, be of higher average genetic quality than are younger individuals that have not3,4. Trivers, one of the earliest proponents of the idea, stressed that this mechanism only works ‘all other things being equal’3. However, other things are seldom, if ever, equal. For example,
Box 1.The evolution of mating preferences by direct and indirect selection
Robert Brooks School of Biological Science,The University of New South Wales, Sydney, NSW 2052, Australia. Darrell J. Kemp* School ofTropical Biology, James Cook University, Cairns, QLD 4870, Australia. *e-mail: [email protected]
A mating preference might evolve and/or be maintained by one (or a combination) of three processes: (1) Historic selection on aspects of the psychosensory system not necessarily associated originally with mate choicea; (2) Direct selection because chosen males provide resources or ameliorate the costs and risks of mating; and (3) Indirect selection that occurs when preference alleles become positively associated with other fitness alleles. The operation of sensory drive and direct selection are relatively straightforwarda–c. However, the importance of indirect selectionb and the process by which fitness and mate choice become genetically correlatedc–e are far more controversial. Genes for female preference might become genetically correlated with genes for attractive male display as a consequence of mate choice itself e, resulting in a self-reinforcing cycle of preference–display coevolution known as the Fisher process. Alternatively, if male displays indicate
additive genetic variation in other fitness components, such as viability, then the build up of a genetic correlation between preference and fitness component indirectly favours preference when the fitness component is exposed to natural selection.This type of process is known generally as the good-genes or indicator mechanismc.The age-based indicator mechanism (AIM) and viability-indicator mechanisms are special cases thereof. According to the AIM, females prefer to mate with older males because of the demonstrated longevity of the males (and thus, implicitly, their genes for viability). References a Endler, J.A. and Basolo, A. (1998) Sensory ecology, receiver biases and sexual selection. Trends Ecol. Evol. 13, 415–420 b Kirkpatrick, M. and Ryan, M.J. (1991) The evolution of mating preferences and the paradox of the lek. Nature 350, 33–38 c Andersson, M. (1994) Sexual Selection, Princeton University Press d Rowe, L. and Houle, D. (1996) The lek paradox and the capture of genetic variance by condition dependent traits. Proc. R. Soc. London B Biol. Sci. 263, 1415–1421 e Lande, R. (1981) Models of speciation by sexual selection on polygenic traits. Proc. Natl. Acad. Sci. U. S. A. 78, 3721–3725
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Box 2. Potential influences on the relationship between age and mate quality Factors promoting a positive relationship • Older males might provide higher-quality ejaculatesa, invest more in current offspringb or otherwise serve as better parentsb,c than do younger males. • Age might signal genetic quality (fewer deleterious prezygotic mutations and better adapted to current conditions) because older males have proven their viability by survivingd–f. Factors promoting a negative relationship • The accumulation of spontaneous germ-line mutations throughout the lifetime of an individual could see older males more likely to carry unconditionally deleterious viability mutationsg. • Late age viability and/or fertility might be negatively genetically correlated negatively with early adult viability and/or fertilityg. • In continually evolving populations, younger males might represent more viable mates because they are born from a better adapted gene poolf,g. • In resource-based (gift-givingh) mating systems in which male ejaculates contribute to female reproductive success, old (previously mated) males might be less able to produce high-quality ejaculatese,i. References a Zuk, M. (1988) Parasite load, body size, and age of wild-caught male field crickets (Orthoptera: Gryllidae): effects on sexual selection. Evolution 42, 969–976 b Curio, E. (1982) Why do young birds reproduce less well? Ibis 125, 400–404 c Komers, P.E. and Dhindsa, M.S. (1989) Influence of dominance and age on mate choice in black-billed magpies: an experimental study. Anim. Behav. 37, 645–655 d Trivers, R.L. (1972) Parental Investment and Sexual Selection; In Sexual Selection and the Descent of Man 1871–1971 (Campbell, B, ed.), pp. 136–179, Heinemann e Manning, J.T. (1985) Choosy females and correlates of male age. J. Theor. Biol. 116, 349–354 f Kokko, H. and Lindström, J. (1996) Evolution of female preference for old mates. Proc. R. Soc. London B Biol. Sci. 263, 1533–1538 g Hansen, T.F. and Price, D.K. (1995) Good genes and old age: Do old mates provide superior genes? J. Evol. Biol. 8, 759–778 h Savalli, U.M. and Fox, C.W. (1999) The effect of male mating history on paternal investment, fecundity and remating in the seed beetle Callobruchus maculatus. Func. Ecol. 13, 169–177 i Fox, C.W. et al. (1995) Male body size affects female lifetime reproductive success in a seed beetle. Anim. Behav. 50, 281–284
both Trivers3 and Manning4 realized that the oldest males are often the least fertile, which suggests a direct fitness cost to females that choose such males. Exactly how unequal other things (i.e. the differences between old and young males) are has rarely been addressed, but it is probably the key to the generality of the AIM. In one of the first attempts to model the relationship between age and good genes, Hansen and Price9 drew on quantitative genetic and life-history principles to argue that older individuals need not be genetically superior mates, but that the opposite should often prevail. Their argument was four pronged: (1) negative genetic correlations between early- and late-life fitness components are common if not the norm; (2) younger males are likely to have higher breeding values for fertility; (3) younger cohorts might be better adapted to current conditions because their parents were exposed to selection more recently than were those of older cohorts; and http://tree.trends.com
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(4) deleterious germ-line mutations occur over the lifetime of a male, significantly reducing the breeding value for fitness of older males (Box 2). For the first time in discussions about the AIM, the assertion that age indicates fitness was seriously challenged. Sexual attractiveness is a life-history issue
The fitness of an individual is a function of both survival and mating success. In most cases, however, these two fitness components cannot be maximized simultaneously10. Conditionally expressed traits that enhance competitive mating abilities, such as flashy ornaments, aggressive behaviours and sexual displays, often do so at the expense of other fitness components, including longevity11,12. In general terms, this is an example of the tradeoff between the allocation of resources to current reproductive effort, and residual reproductive value (RRV), which is a cornerstone of life-history theory7,10. The realization that sexual advertisement is functionally analogous to other forms of reproductive investment, and is subject to similar life-history tradeoffs7,9,12, is fundamental to recent progress in understanding the AIM (Refs 5,6,13,14). The most important point that Hansen and Price9 made was that adult survival might not be strongly, or even positively, correlated with total fitness. The ability to survive to maturity, attract mates and mate with them successfully might be more important determinants of lifetime reproductive success than is longevity. Male longevity will be correlated with fitness only if most of the genetic variation in fitness is attributable to alleles that are uniformly deleterious or beneficial across the lifetime of an individual. Genes that have antagonistic effects on early and late fitness components, and deleterious mutations that act only in older individuals will weaken any such correlation and, in the case of antagonistic genes, might even reverse it9. Determinants of condition: resource allocation versus acquisition
Under Hansen and Price’s model9, the only circumstance under which older males would bestow genetic advantages on their offspring is if fertility increases steeply with age: a situation that Hansen and Price judged to be generally uncommon. Their approach assumed that variation in important fitness components was largely a problem of how resources are allocated throughout the lifetime of an organism (i.e. the allocation to current versus future reproductive effort). The issue of resource allocation can be conveniently thought of as ‘dividing up a pie’, because devoting some of the pie to a particular trait necessarily means that there is less of the pie for other traits10. Hence, where variation in fitness is determined by allocation of resources among fitness components, tradeoffs between these components are likely to prevail10,15. However, there is a growing appreciation that positive genetic correlations among fitness components to which resources have to be allocated might be generated if there is additive
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Box 3. Evolutionary game theory and its relevance to age-based sexual advertisement Originally devised to model economic systems, the ‘theory of games’ was first explicitly applied in the context of individual optimization in biology by Maynard Smith and Pricea. Game theory recognizes the importance of frequency dependence in evolution, and is based on the premise that the ‘best’ strategy (behaviour and/or morphology) will depend on the strategies played by other members of the population. Game theoretic models seek to define evolutionarily stable strategies (ESSs) for particular situations. An ESS is defined as a strategy that renders a population of individuals playing that strategy incapable of being invaded by a mutant individual playing a different strategyb. ESSs can be
pure, where different individuals in the population only ever play one of several available tactics, or mixed, where individuals switch between available tactics conditionally with an ESSprescribed probability. Whereas classic life-history theory deals with maximization of fitness rather than with evolutionary stabilityc, game theory is crucial to studies linking sexual selection with life-history processes. Individuals are expected to maximize their inclusive fitness according to life-history tradeoffs, but the social environment will ultimately determine the nature and course of these tradeoffsc. Evolutionary game theory has proved particularly relevant to studies of intrasexual conflict, but can be equally
genetic variation in resource acquisition10,17 (metaphorically, where some individuals have relatively bigger ‘pies’ to divide in the first place). A simulation study by Kokko and Lindström13, in which males differed only in condition (which is largely analogous to resource acquisition18) and not in patterns of resource allocation, predicted that highquality (condition and/or acquisition) males would survive longer and provide genetic fitness benefits to their offspring. A similar study by Beck and Powell14 reiterated that old-age preference is possible in principle, but will depend on how survival is determined from genes for viability. Where adult survival is relatively important as a determinant of fitness, preferences for older males can evolve by a good-genes process13,14, whereas if juvenile survival is relatively important then females should prefer younger and intermediate-age mature males14. Mathematical simulation is valuable because it provides insights that are not possible from verbal arguments alone, particularly regarding the action and importance of individual variables to evolutionary processes. The models of Kokko and Lindström13 and Beck and Powell14 suggest that, in addition to how fitness components co-vary genetically, the pattern of age-dependent survival will influence the benefits of mate choice based on age, and thus the evolution of preferences. This might manifest itself as consistent differences among taxa in the importance of age-based mate choice resulting from differences in longevity, life history and the relative contributions of juvenile and adult survival to fitness. Age-dependent sexual advertisement
In reality, there is probably variation among individuals both in overall condition18 and in the way that condition is allocated to current reproductive effort, future survival and reproduction19. Kokko6 built a model in which males varied genetically in condition, http://tree.trends.com
applied to model optimal male display (ornamentation and behaviour) in the context of female choice. Kokko’s modeld employs an explicit ESS approach to determining the optimum levels of agespecific male display when mating success depends upon the level of advertisement by rivals, and where the costs of such display are paid in a life-historical currency. References a Maynard Smith, J. and Price, G.R. (1973) The logic of animal conflict. Nature 246, 15–18 b Maynard Smith, J. (1982) Evolution and the Theory of Games, Cambridge University Press c Svensson, E. and Sheldon, B.C. (1998) The social context of life history evolution. Oikos 83, 466–477 d Kokko, H. (1997) Evolutionary stable strategies of age-dependent sexual advertisement. Behav. Ecol. Sociobiol. 41, 99–107
which they allocated to fecundity (including sexual advertisement) and survival in a way that was optimal for their age. In this model, under many (but not all) circumstances, early and late fecundity and survival can all be positively correlated with one another, with overall fitness and with condition. This result lends new plausibility to the evolution of preferences for older males by a good-genes process, because condition-dependent sexual advertisement can reliably indicate longevity and overall fitness. In a separate model, Kokko5 explored the optimal strategy for males of differing quality (either high or low) to advertisement over time, accounting both for life-history tradeoffs between sexual advertisement and RRV, and for the level at which competitors advertise. This model was based on the principles of evolutionary game theory (Box 3), and hence searched for evolutionarily stable strategies (ESSs) of lifetime sexual advertisement. Most ESSs in this ‘sexual advertisement game’ resulted in males increasing their level of advertisement over time. Under some conditions, low-quality cohort members advertised at a higher level than did high-quality individuals (primarily because low-quality males might suffer a lower RRV cost to advertisement20), with the result that sexual advertisement was not always strictly honest. However, such cheating males always paid for it in later years such that advertisement across age classes was honest on average5. Viability costs in the model could be imposed by increased mortality from predation (on the basis of increased visual and/or acoustic conspicuousness), loss of energetic reserves, or social costs and the risk of injury in male–male contests. The model, therefore, has broad appeal and could be extended (in principle) to encompass age-related delays in other aspects of male reproductive investment, such as fighting and lekking behaviour and advertising parental care21. Previous theoretical
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treatments have also suggested that, on the basis of lifetime changes in RRV, males should delay potentially dangerous aggressive behaviours until later in life22. Clear empirical evaluation of this idea has proven notoriously difficult because of concomitant age-based changes in relative competitive ‘abilities’23. Is the AIM really useful?
The two theoretical treatments by Kokko5,6 demonstrate that females can derive a good-genes benefit from mating with old rather than with young males under a wide range of conditions. The correlation between male attractiveness and age is mediated by an increased investment in costly sexual advertisement with age, and is highly consistent with evidence that males of several species increase their level of sexual ornamentation and display as they get older24–27. Here, the age indicator mechanism becomes indistinguishable from the standard viability indicator model5. This leads us to ask: do we really need the AIM? It is less general than the viability indicator model in which females prefer signals of male breeding value for survival irrespective of whether they are correlated with age. Both viability-indicator models and the AIM suffer from a further lack of generality as a result of the fallacy of equating longevity with fitness. In essence, the goodgenes process requires only that sexual attractiveness and breeding value for lifetime fitness are reliably and positively correlated. As Kokko’s model shows, however, there are situations in which optimal levels of honest sexual advertisement are not correlated with age5, and thus preferences that evolve by the good-genes process will not favour older males. In fact, several authors have pointed out that, under some circumstances, males of high genetic quality might invest so much in advertisement that they live shorter lives than do low-quality males, yet still make the best mates6,28–30. Thus, viability-indicator models (including the AIM) have less explanatory power than do more general good-genes models. From a practical point of view, a negative (or null) correlation between age and male attractiveness would falsify the AIM and viabilityindicator models, but not the good-genes process30. Critically testing the good-genes process requires exhaustive quantitative genetic study (under field conditions) in which the genetic correlation between attractiveness and lifetime fitness is estimated. Despite our claim that the AIM is of limited use as a model of preference evolution, it has served a valuable heuristic purpose. Attempts to model it5,6,9 have forced the explicit realization that the costs that enforce honesty (on average) of sexual advertisement are in RRV and can be observed via age-dependent changes in sexual advertisement5,6. Cheating is possible5,6, but is kept to a low level because only high-quality males can advertise at a consistently high level without paying unacceptable penalties in other fitness components (e.g. survival11, caring for offspring19,20 and social dominance12). This applies both to signals of http://tree.trends.com
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indirect and direct benefits and suggests that the most generally reliable indicators of male quality will be those that draw upon cumulative lifetime investments20,31. Do females prefer older males?
Several studies report positive correlations between male age and male attractiveness to females (Table 1; Refs 6,13,32). Such a correlation is necessary evidence for the AIM, but it is not sufficient because genetic quality is not the only potential correlate of male age. In resource-based mating systems, females could gain direct benefits from old mates: if RRV declines with age then older males are expected to invest relatively more effort in current broods33 and thus to be harder-working mates33,34. Furthermore, male parental ability could increase with age because of accumulated experience in specific parental duties, or as a result of increased foraging efficiency33,35. Other male traits, such as territory-defending ability and ejaculate quality might co-vary with age; however, in many groups, paternal investment in the form of ejaculate quality declines with successive matings36 and hence, possibly, with age37. The presence of direct benefits might, therefore, obscure a clear empirical evaluation of ‘good-genes’ explanations and, in particular, the AIM. Support for the AIM should include demonstrations of age-dependent choice in the absence of any direct benefits. Such evidence exists for several species (Table 1), but the correlative evidence is by no means unanimous. There are several counterexamples of no age-based preference and of preference for intermediate or younger males (Table 1)32. Evidence from extra-pair copulations (EPCs) in birds make particularly good tests because females are thought to engage in EPCs primarily to gain genetic benefits24,25,38–40. If female choice is for good genes (rather than for attractive, diverse or compatible genes), then male success through EPCs should increase with age. Recent empirical studies of cuckoldry provide both supporting and opposing evidence for this prediction (Table 1). A recent meta-analysis of 22 such studies41 also reports a weak positive correlation between age and own-nest paternity. Male age, therefore, appears generally related to extra-pair paternity in the direction suggested by the AIM, but this effect is far from unequivocal. Based on the evidence, it is therefore prudent to reject the AIM and the viability-indicator model as general hypotheses of the evolution of mate choice by indirect selection. However, null and negative correlations between age and sexual attractiveness remain consistent with more general good-genes models5,6,9,28–30, and an important challenge is now to test these more inclusive formulations. Delivering the good genes
Our rejection of the AIM and viability-indicator hypotheses as general models is not a statement that females derive no indirect benefits from mating with older or more long-lived males. It merely reflects the
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Table 1. Summary of recent evidence potentially relevant to the age-based indicator mechanism Key recent examples Nature of evidence
Supporta
Species
Choice contextb
Refs
Females prefer older males: (a) When male age is potentially correlated with resources
(b) When male age is not
+
European starling, Sturnus vulgaris
TP
26
+
Field crickets, Gryllus bimaculatus, G. veletis, G. pennsylvanicus
T
43,44
+
Great reed warbler, Acrocephalus arundinaceus
TP
45
+
Redlip blenny, Ophioblennius atlanticus
T
46
+
Blue tit, Parus caeruleus
EPC
40
+
Bullock's oriole, Icterus galbula bullockii
EPC
27
–
Red-winged blackbirds, Agelaius phoeniceus
EPC
47
+
Fallow deer, Dama dama
TE
48
–
Hooded warbler, Wilsonia citrina
EPC
49
+
House sparrow, Passer domesticus
EPC
24
+
Purple martins, Progne subis
EPC
39
–
Sandfly, Lutzomyia longipalpis
LEK
32
+
Yellowhammer, Emberiza citrinella
EPC
25
–
Yellow warbler, Dendroica petechia
EPC
50
better than do those of younger
–
Fruit fly, Drosophila melanogaster
NA
42
males
–
Sandfly, L. longipalpis
NA
32
correlated with resources
Offspring of older males perform
aKey:+
indicates positive support for the evidence; – indicates contradiction.
bAbbreviations:
EPC, choice of extrapair mate; LEK, choice of lekking mate; TE, choice inferred by timing of estrus; TP, choice of territorial
partner (with pair-bonds); T, choice of territorial mate (no pair bonds); NA, no choice mating experiment.
fact that these hypotheses hold up only as long as age and longevity are positively correlated with fitness, a somewhat arbitrary restriction. In evaluating more inclusive good-genes models, it is still worthwhile to ask whether females derive genetic benefits when they mate with older males. The indirect benefit of mate choice (including preferring older males) is the genetic inheritance of fitness by the mutual offspring. Testing of the mechanism, therefore, requires quantitative genetic evidence that the offspring of preferred older males are fitter than are those of other males. Although such tests require experimental designs that are so large as to be prohibitive in many animal systems, two recent laboratory studies of this nature have been attempted. In the first example, five-week-old male Drosophila melanogaster were found to sire offspring that were slightly less likely to survive to maturity than were those sired by two-day-old and two-week-old males42. There were no significant differences among the sire types in the mating ability of sons or the fecundity of daughters. Thus, if anything, younger males sire fitter offspring than extremely old males, but the effects of sire age on offspring fitness appear to be weak – perhaps too weak to provide a fitness benefit to females that discriminate among males based on their age. It is important to note, however, that there is no evidence of a natural correlation between male attractiveness and age in D. melanogaster, making it a potentially poor model for testing the benefits of preferring older mates. http://tree.trends.com
In the second example, Jones et al.32 showed that females of the lekking sandfly Lutzomyia longipalpis preferred to mate with males of intermediate age (four to six days old) over young (zero to two days old) or old (eight to ten days old) males. None of the measures of female reproductive success from these matings, including the number and proportion of eggs hatched, varied significantly in relation to the age class of the mate. However, when virgin females were mated at random to a male from one of the three age groups, hatching success of eggs sired by older males was significantly lower. This might be because of a negative genetic correlation between male longevity and offspring survival to hatching, or it might represent lower sperm number or performance in older males. Unfortunately, post-hatching performance of offspring is not reported and so it is impossible to tell whether sire age influenced further important components of offspring fitness. Thus, although the insights gained from these studies are limited, they do take an important step towards directly quantifying the fitness consequences of mate choice based on age. Conclusion
Females that mate with old rather than with young males might receive indirect (genetic) fitness benefits under many circumstances, but such benefits are not universal. This is reflected empirically in the findings that females often prefer old males, but that they can also prefer younger or intermediate-aged males or even disregard age entirely. The AIM, and viability-indicator
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Acknowledgements The authors would like to thank Michael Jennions, Hanna Kokko and the anonymous referees for helpful discussions and comments on the article. RB was supported by an Australian Postdoctoral Fellowship and an ARC Large grant. DJK was supported by an Australian Postgraduate Research Award.
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models of indirect benefits are falsified by these latter findings. In their place is now a more inclusive understanding of what ‘good genes’ are. The usefulness of the AIM is its historic role in shaping the realization that sexually selected traits should be viewed within a lifehistory context because it is here that the costs of these traits are exacted. Just as behavioural ecologists have rarely considered life-history constraints explicitly7, life historians have traditionally ignored the influences of a social environment on life-history evolution8. Clearly, workers in both fields will benefit from more explicit consideration of the interplay between them7,8. Empirically isolating the effect of age per se on female choice is a difficult assignment, given the
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added complications inherent in separating direct and indirect benefits of choice. It might pay empiricists to switch focus from documenting the relationship between age, attractiveness, display and offspring performance to understanding how these traits trade off. Comparative and interpopulation studies might address how age-dependent mortality influences investment in sexual signalling and other costly reproductive behaviours. Within populations, attempts to partition the relative importance of the acquisition of condition and the allocation of condition to sexual display and survival promise to significantly advance our understanding of the genetic benefits of mate choice.
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