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Female mate choice in pied flycatchers: An answer and a problem
TREE vol.
1, no. 4, October
1986
When a migratory female passerine returns to her breeding grounds she must choose a mate. Her choice could be based on the quality of resources a male controls’, or on the quality of the male himself (his genes 24 and/or his parental ability5). Determining how such females make their decision has not been easy, but Rauno Alatalo, Arne Lundberg and Carolyn Glynn at the University of Uppsala have recently managed to determine experimentally whether pied flycatcher (Ficedula hypoleuca) females select their mates on the basis of male characteristics or of the quality of the males’ territorie8. Pied flycatcher males arrive on the breeding grounds before females, and the order of male arrival correlates with the subsequent mating order: the first females to arrive choose those males which arrived first. This could be either because those males arriving first get the best nest sites, and females prefer males with good nest sites, or because the 3est males arrive first, and females prefer high quality males (older males, for example, arrive earlier and may make better mates because of their greater experience). The beauty of pied flycatchers as study animals is that it is possible to separate these alternatives by forcing males to occupy territories at random. Pied flycatchers are hole nesters, but in the areas of this study there are few natural holes and these are of low quality, so the birds prefer to nest in boxes. Boxes were put up in random locations, and sequentially, so that the first male to arrive took the first nest box, another was put up and the second male to arrive took that box, and so on. Thus all the males were randomly distributed with respect to territory quality. Once the territories were occupied, the order in which males subsequently paired was recorded. Alatalo, Lundberg and Glynn found that under the conditions of their experiment there was no correlation between arrival order and mating order, and that this was significantly different from the situation recorded previously in the natural copulation. In two of the study areas, -nated females were removed and a second group of females allowed to .?ttle. Their mating order was simirar to that of the first group. Thus ‘emales were not choosing early Prriving males per se, and nor was i:,eir choice of mate random. But Andrew Read, Zoology Department, Oxford $versity, South ParksRoad,Oxford OX1 3PS,
news
Female MateChoice inPiedFlycatchers: anAnswer anda Problem Andrew F. females were not basing their choice on any of the measured male characteristics (age, size, colour or song repertoire). Instead, mating order was correlated with measures of nest site quality (security of the boxes from predators and the proportion of the surrounding area covered by favourable feeding habitat). Thus it seems that territory quality is the most important criterion for female mate choice in the pied flycatcher. Similar conclusions have come from studies of other bird species’-‘, although this is the first time that female choice of males and territory quality have been so rigorously separated. However, further questions are raised. During breeding, pied sexually flycatchers are dull brown dichromatic, with females and vivid black and white males (although the males may also have variable amounts of grey and brown plumage). After breeding, males assume similar colours to those of the females. Most current explanations for such sex differences follow from Darwin’s” hypothesis of sexual selection acting through female choice. Females, he suggested, are attracted to more brightly coloured males. The increased risk of predation that is assumed to be associated with bright colouration puts an upper limit on the brightness of male plumage and leads to strong selection for males to be bright only when females are choosing males; hence the seasonal changes in plumage patterns. Clearly, it is central to all hypotheses which attempt to explain the origin of plumage colouration in terms of female choice’&‘* that, to some extent at least, females choose males on the basis of their plumage colouration. But the pied flycatcher experiment appears to contradict this: not only was territory quality rather than male quality shown to be the most important criterion for female mate choice, but males with higher proportions of brown or grey in their plumage were selected by females as often as blacker males. So how can we explain the seasonal sexual dimorphism of pied flycatchers? There are several post hoc explanations which could be offered by those favouring female
choice models. Perhaps females choose males for extra-pair copulations on the basis of their plumage, or perhaps plumage is a deciding factor if two males are available with territories of very similar quality or in areas where good territories are not scarce. Another possibility is that female choice on the basis of plumage was an important selective force in ancestral flycatchers only, and that extant species have remained dichromatic in the absence of such choice, although this seems unlikely given the hypothesized risk of predation and the possible physiological cost to males. Perhaps mechanisms other than female choice’3r’4 may be involved. As has been so elegantly demonstrated by Alatalo, Lundberg and Glynn, the pied flycatcher is a good species for about mate studying questions choice. It remains to be seen whether ideas about the evolution of sexual colour dimorphism can be tested so effectively.
References 1 Davies, N.B. (1978) in Behavioural Ecology: An EvolutionaryApproach (Krebs, JR. and Davies, N.B., eds), pp. 317-350, Blackwell 2 Lande, R. (1981) Proc. NatlAcad. Sci USA 78‘3721-3725 3 Andersson, M. (1982) Biol. J. Linn. Sot. 17.375-393 4 Kirkpatrick, M. (1982) Evolution 36, l-12 5 Hallidav. T.R. (1983) in Mate Choice (Bateson; P., ed.), pp. 3-32, Cambridge University Press 6 Alatalo, R.V., Lundberg,A. and Glynn, C. (1986) Nature 323,152-l 53 7 Davies, N.B. and Lundberg, A. (1984) J. Anim. Ecol. 53,896-912 8 Pleszczynska, W.K. (1978) Science 201, 935-937 9 Searcy, W.A. (1979) Am. Nat. 114, 77-l 00 10 Darwin, CR. (1871) The Descent of Man, and Selection in Relation to Sex, John Murray 11 Hamilton, W.D. and Zuk, M. (1982) Science 218,384-387 12 O’Donald, P. (1983) The Arctic Skua, Cambridge University Press 13 Baker, RR. and Parker, G.A. (1979) Philos. Trans. R. Sot. London Ser. B 287.63-130 14 Hingston. R.W.G. (1933) The Meaning ofAnimal Colouration andAdornment, Edward Arnold
1, no. 4, October
1986
When a migratory female passerine returns to her breeding grounds she must choose a mate. Her choice could be based on the quality of resources a male controls’, or on the quality of the male himself (his genes 24 and/or his parental ability5). Determining how such females make their decision has not been easy, but Rauno Alatalo, Arne Lundberg and Carolyn Glynn at the University of Uppsala have recently managed to determine experimentally whether pied flycatcher (Ficedula hypoleuca) females select their mates on the basis of male characteristics or of the quality of the males’ territorie8. Pied flycatcher males arrive on the breeding grounds before females, and the order of male arrival correlates with the subsequent mating order: the first females to arrive choose those males which arrived first. This could be either because those males arriving first get the best nest sites, and females prefer males with good nest sites, or because the 3est males arrive first, and females prefer high quality males (older males, for example, arrive earlier and may make better mates because of their greater experience). The beauty of pied flycatchers as study animals is that it is possible to separate these alternatives by forcing males to occupy territories at random. Pied flycatchers are hole nesters, but in the areas of this study there are few natural holes and these are of low quality, so the birds prefer to nest in boxes. Boxes were put up in random locations, and sequentially, so that the first male to arrive took the first nest box, another was put up and the second male to arrive took that box, and so on. Thus all the males were randomly distributed with respect to territory quality. Once the territories were occupied, the order in which males subsequently paired was recorded. Alatalo, Lundberg and Glynn found that under the conditions of their experiment there was no correlation between arrival order and mating order, and that this was significantly different from the situation recorded previously in the natural copulation. In two of the study areas, -nated females were removed and a second group of females allowed to .?ttle. Their mating order was simirar to that of the first group. Thus ‘emales were not choosing early Prriving males per se, and nor was i:,eir choice of mate random. But Andrew Read, Zoology Department, Oxford $versity, South ParksRoad,Oxford OX1 3PS,
news
Female MateChoice inPiedFlycatchers: anAnswer anda Problem Andrew F. females were not basing their choice on any of the measured male characteristics (age, size, colour or song repertoire). Instead, mating order was correlated with measures of nest site quality (security of the boxes from predators and the proportion of the surrounding area covered by favourable feeding habitat). Thus it seems that territory quality is the most important criterion for female mate choice in the pied flycatcher. Similar conclusions have come from studies of other bird species’-‘, although this is the first time that female choice of males and territory quality have been so rigorously separated. However, further questions are raised. During breeding, pied sexually flycatchers are dull brown dichromatic, with females and vivid black and white males (although the males may also have variable amounts of grey and brown plumage). After breeding, males assume similar colours to those of the females. Most current explanations for such sex differences follow from Darwin’s” hypothesis of sexual selection acting through female choice. Females, he suggested, are attracted to more brightly coloured males. The increased risk of predation that is assumed to be associated with bright colouration puts an upper limit on the brightness of male plumage and leads to strong selection for males to be bright only when females are choosing males; hence the seasonal changes in plumage patterns. Clearly, it is central to all hypotheses which attempt to explain the origin of plumage colouration in terms of female choice’&‘* that, to some extent at least, females choose males on the basis of their plumage colouration. But the pied flycatcher experiment appears to contradict this: not only was territory quality rather than male quality shown to be the most important criterion for female mate choice, but males with higher proportions of brown or grey in their plumage were selected by females as often as blacker males. So how can we explain the seasonal sexual dimorphism of pied flycatchers? There are several post hoc explanations which could be offered by those favouring female
choice models. Perhaps females choose males for extra-pair copulations on the basis of their plumage, or perhaps plumage is a deciding factor if two males are available with territories of very similar quality or in areas where good territories are not scarce. Another possibility is that female choice on the basis of plumage was an important selective force in ancestral flycatchers only, and that extant species have remained dichromatic in the absence of such choice, although this seems unlikely given the hypothesized risk of predation and the possible physiological cost to males. Perhaps mechanisms other than female choice’3r’4 may be involved. As has been so elegantly demonstrated by Alatalo, Lundberg and Glynn, the pied flycatcher is a good species for about mate studying questions choice. It remains to be seen whether ideas about the evolution of sexual colour dimorphism can be tested so effectively.
References 1 Davies, N.B. (1978) in Behavioural Ecology: An EvolutionaryApproach (Krebs, JR. and Davies, N.B., eds), pp. 317-350, Blackwell 2 Lande, R. (1981) Proc. NatlAcad. Sci USA 78‘3721-3725 3 Andersson, M. (1982) Biol. J. Linn. Sot. 17.375-393 4 Kirkpatrick, M. (1982) Evolution 36, l-12 5 Hallidav. T.R. (1983) in Mate Choice (Bateson; P., ed.), pp. 3-32, Cambridge University Press 6 Alatalo, R.V., Lundberg,A. and Glynn, C. (1986) Nature 323,152-l 53 7 Davies, N.B. and Lundberg, A. (1984) J. Anim. Ecol. 53,896-912 8 Pleszczynska, W.K. (1978) Science 201, 935-937 9 Searcy, W.A. (1979) Am. Nat. 114, 77-l 00 10 Darwin, CR. (1871) The Descent of Man, and Selection in Relation to Sex, John Murray 11 Hamilton, W.D. and Zuk, M. (1982) Science 218,384-387 12 O’Donald, P. (1983) The Arctic Skua, Cambridge University Press 13 Baker, RR. and Parker, G.A. (1979) Philos. Trans. R. Sot. London Ser. B 287.63-130 14 Hingston. R.W.G. (1933) The Meaning ofAnimal Colouration andAdornment, Edward Arnold