Proc. Natl. Acad. Sc. USA Vol. 74, No. 8, pp. 3476-3479, August 1977
Evolution
Parental investment, mate choice, and mate quality (sexual selection/sociobiology/Columba livia)
NANCY BURLEY* Department of Zoology, University of Texas at Austin, Austin, Texas 78712
Communicated by E. 0. Wilson, March 17, 1977
Current theory in sexual selection is extended ABSTRACT to predict within-sex variability with regard to selectivity towards mates in different mating systems. Generally, the sex that invests more in the care of each offs pring should be more selective of mates than the sex investing less. Within each sex, individuals of low mate quality should be less selective than individuals of high quality, but there should be less variation in selectivity among individuals of the sex investing more. When only one sex contributes parental care, however, individuals of that sex should be uniformly selective, while the other sex is expected to mate indiscriminately. Using feral pigeons (Columba livia), these hypotheses are tested for the case in which both sexes contribute substantial parental care, but in which females contribute more than males. As predicted, females were found to be more selective of mates than males were. On certain criteria, males of lower quality were less selective of mates than males of higher quality.
The recent concept of parental investment has revolutionized biologists' thinking on mating systems and factors that affect them (1, 2). Parental investment (PI) is defined as an investment in an offspring that simultaneously increases the offspring's likelihood of survival and reproduction while decreasing parental ability to invest in other offspring (1). PI patterns are expected to influence the selectivity of individuals of both sexes in choosing mates. Because the sex that invests more (usually female) stands to lose more in a mismating, individuals of that sex should select mates with greater care than members of the sex that invests less (usually male). When one sex contributes little or no PI, its members should be nondiscriminating, except when temporal constraints such as sperm depletion (3, 4) reduce access to simultaneously available mates. Within-sex selectivity Sexual selection theory can be extended to predict differences in selectivity among individuals of the same sex. How selective an individual is in mate choice should be affected by his or her genetic quality and, where applicable, investment capabilities. In most cases, superior individuals should be more selective than inferior ones. By making the assumption that attractiveness of an individual as a potential mate is a good index of the individual's mate quality, it follows that attractive individuals (as judged by members of the opposite sex) should be more selective than unattractive ones when choosing mates. Attractiveness can be ascertained when individuals of one sex or phenotype display consistent preferences for mates of a particular type. The existence of consistent female preferences was postulated by Darwin (5), and has been established for numerous species (1, 6); more recently the possibility of male preferences has also been considered (1, 7, 8), but only a few studies have been performed on it (9, 10). The costs of publication of this article were defrayed in part by the payment of page charges from funds made available to support the research which is the subject of the article. This article must therefore
Within-sex selectivity patterns should vary among breeding systems. In monogamous species that have substantial PI by both sexes, high-quality/attractive females should refuse courtship advances of unattractive males because they can attract superior ones. Unattractive females may be unable to form a pair bond with the most attractive males, and therefore should be more receptive to males of lower quality. However, such low-quality females may attract superior males as short-term copulatory partners, because males have little to lose from such alliances (sperm) and potentially much to gain (offspring in which they invest no PI). In monogamous systems, an inferior male should not restrict pair-bonding attempts to the best females, for he is likely to fail in competition for them with attractive males. In polygamous and promiscuous mating systems, one sex, typically male, invests little or nothing in PI (A in Fig. 1), and members of that sex gain little by being selective; their own attractiveness should not affect their selectivity. Therefore, males may mate indiscriminantly (8), so females are not limited in mate choice by their relative attractiveness. All females should mate with the best males, even if a number of females mate with the same individual. When males incur no PI, female selectivity should be largely independent of female quality (Fig. 2A). This has been demonstrated for Drosophila, among which female reproductive success is not limited by attractiveness, while male reproductive success varies widely and is dependent upon ability to attract females (11, 12). When males have substantial PI, but less than females (Fig. 1, between A and C), males should be more affected than females by their own quality when attempting to secure mates. Females are still more of a limiting resource; therefore males, the limited sex, experience more competition for mates. A female's greater range of mate choice should give her greater independence from her own attractiveness in the selection process. Individuals of the mate-limited sex should vary more overall in their tendency to be selective than should individuals of the limiting sex. In addition, for any given level of attractiveness/quality, individuals of the mate-limited sex (males) should be less selective than those of the limiting sex (females; Fig. 2B). When males and females have identical PI, their own attractiveness as mates should influence their tendency toward selectivity equally (Figs. 1, C, and 2C), although they may not select by the same criteria as long as sex roles are somewhat different. Therefore, as relative parental investment (fraction of total PI) increases from zero to one-half for males, the effect of an individual's attractiveness as a mate on its behavior when looking for a mate should converge for males and females. As male investment increases beyond one-half, as it may in polyandrous birds and some species of fish (2, 13), males should Abbreviation: PI, parental investment. * Present address: Department of Biology, McGill University, Montreal, Quebec H3A iBi, Canada.
be hereby marked "advertisement" in accordance with 18 U. S. C. §1734 solely to indicate this fact.
3476
Evolution: Burley
Proc. Natl. Acad. Sci. USA 74 (1977)
3477
phenotypes that occur in appreciable frequencies in feral pop*tions.,The adaptive significance of plumage polymor-
become more selective than females and less influenced by their own mate quality. Test hypotheses Following the above reasoning, one can test hypotheses that, when females contribute greater PI than males (Fig. 2B): (1) females are less likely than males to select mates on the basis of their own attractiveness, that is, overall their selectivity is higher; (2) within each sex, how selective an individual is will depend on how attractive he or she is to the opposite sex; and (3) overall, females should vary less in selectivity than males. Theoretically, organisms may select mates on the basis of numerous criteria that have both genetic and nongenetic components. Characteristics of potential mates that may be evaluated in species in which both parents contribute PI include fertility and fecundity, survival probability, food-getting and nest defense ability, territory quality, genetic and behavioral complementarity, reproductive experience, and fidelity. Cues to the recognition of these traits probably vary among species, and the sexes may be sensitive to different criteria.
phism is not known, but phenotypes may vary in longevity and/or fertility (15-17). I do not maintain that plumage phenotype is the only basis by which choice of mate is made among pigeons. To the contrary, I have investigated a number of other characteristics, such as nest defense ability, age, size, and reproductive experience, and have found that pigeons are sensitive to numerous traits (unpublished data). It is also possible that because sex roles differ, males and females may select mates by different criteria, or that males may be more selective with regard to some traits, whereas females are more sensitive to others. By studying characteristics of known genetic origin, this possibility is minimized, for if a genetic trait is important to the reproductive success of one sex, it should be of concern to both sexes when choosing mates because the trait will likely be transmitted to offspring. For example, if small size were a disadvantage to males, but had no effect on female reproductive success, both sexes might nevertheless avoid mating with small individuals. Females would avoid small males because of their low reproductive value, while males would avoid small females because of the low reproductive value of resulting sons (unless females only transmit genes for size to daughters). Predominant colors among feral pigeons are blue and ash red; common patterns are checker, velvet, and bar (15, 18, 19). Checker and velvet intergrade phenotypically, and birds from my population respond to them similarly, so I group both under the term "checker." Both color and pattern are simple Mendelian traits (20-22); color is sex-linked (14, 22). Several features of pigeon life history are salient. Courtship may be initiated by individuals of either sex. After forming a pair bond, pairs remain together for life, but individuals will remate within a month after the death or removal of their mate. Both parents share in incubation, brooding, and feeding of young, and nest defense. Females assume somewhat more than half of the total PI invested in each offspring that a pair-raises, on the basis of the relative time spent by females and males at the nest with eggs and offspring. Exact PI contribution of each sex varies among pairs (unpublished data).
MATE PREFERENCES AMONG PIGEONS To test these hypotheses, I have investigated preferences for particular plumage patterns and colors of feral pigeons (Columba livia). These characteristics were chosen for study both because there exists sufficient variability in pigeon plumage to permit testing of the hypotheses, and because the traits are almost entirely genetically determined (14). I have studied only
Experimental design The following experimental design is used to test preferences of pigeons that are captive descendants of wild-caught urban Texas birds. Test enclosures, measuring 4.5 X 2.1 X 2.5 m, contain one nest box at each end. A pigeon is tethered to each nest box on a string that allows it to fly no farther from its box than the center of the pen. Two tethered birds of the same sex
C.,~~~~Ct >Co~~~~~~o
.
0
1
1/2 6 PI/(d + 9) Pi
FIG. 1. Selectivity of males and females as a function of relative parental investment. At A, female choice of mate is independent of other females' choices. As male PI increases, females must consider not only inherent male quality, but also the number of females a given male is mated with. This restriction on female choice (and also on male choice) increases non-linearly with male PI. At C, sexes contribute identical PI and are equally selective. Beyond C, males are more selective than females.
A
c
C.4
C/,
0r Low
x Low High Self's quality as mate FIG. 2. Selectivity as a function of one's own quality as a mate. (A) Females assume total PI. (B) Females assume greater PI than males. For any level of mate quality, a female of that quality is more selective than a male of identical quality. The difference in selectivity for quality X is Y. Overall, females vary less in selectivity (V9) than males (Vd). (C) Males and females contribute equal PI.
High
3478
Evolution:
Burley
Proc. Natl. Acad. Sci. USA 74 (1977)
Table 1. Female choice of mate
of courting the previous female. Such behavior is interpreted to mean that either choice is acceptable to the chooser, and that choice of a particular mate is less important than possession of a box. Because this behavior may have some seasonal variability, all classes within experiments were tested simultaneously. Experiments 1 and 2 below were performed simultaneously between August and December 1975, while 3 and 4 were performed between December 1975 and February 1976. Two categories of experiments were performed, the first (1 and 2) to establish which male phenotypes are preferred by females, the second (3 and 4) to determine which female phenotypes are preferred by males. Individuals in each choice pair were matched for age, breeding experience, time in isolation, and size. I also used subjective measures to match individuals for aggressiveness. To minimize the effects of other types of variability which undoubtedly existed within choice pairs, a minimum of three pairs was used for each preference tested. All choosers had raised at least three clutches prior to experimentation. Because of the small number of ash red birds available, preferences between ash red phenotypes (bar versus checker) were not determined, and the results of experiments for ash red choosers are pooled, disregarding pattern pheno-
Choice A
Chooser phenotype
C
B
Blue Blue checker bar
Ash red
Blue
Ash Blue red bar checker
Bluechecker 8 1 9 1 9 0 Blue bar 13 3 11 1 10 1 Ash red 11 3 8 1 8 1 Total 32 7 28 3 27 2 A: Blue checker versus blue bar males. Eleven females made no choice. B: Blue bar versus ash red bar and blue checker versus ash red checker males. Four females made no choice. C: Blue bar versus ash red checker males. Three females made no choice.
constitute a choice pair from which a bird of the other sex makes a choice. A chooser is released into the pen and allowed to fly back and forth between members of the choice pair until it demonstrates a clear preference. At various intervals, choicepair birds are switched to opposite nest boxes to determine if the chooser actually prefers a bird or a nest box. Criteria of choice of a mate are complex, because individuals vary in behavior. The major criterion used to determine choice is that the chooser directs 90% of its courtship effort and spends most of its time with one individual for at least the hour prior to the end of an experiment. Often such pairs display initial stages of nesting behavior. Two to eight hours are required to fulfill this criterion, depending on season and degree of inequality between members of the choice pair. At the end of this period, the chooser is scored as having made choice of a mate (A or B), choice of a nest box (1 or 2), or no choice. In analysis of preferences, tests resulting in "no choice" are excluded as not being biased toward either mate or nest box. Criteria of choice are discussed in greater detail elsewhere (N. Burley and N. Moran, unpublished data). Nest boxes within pens are identical in size, construction, height above ground, and illumination. Nevertheless, males in particular sometimes establish preference for a certain nest box. When this occurs, a male characteristically spends much time in the preferred box, making "nest box calls" and courtship and nesting postures (14). When a female joins him in his box, he courts her, but when choice-pair birds are switched, he remains in the same box and courts a new bird, even after several hours
type.
Experimental results Experiment 1. Blue bar, blue checker, and ash red females were presented with choices between blue checker and blue bar males. Five choice pairs were used. Females of all phenotypes preferred checker to bar males (binomial two-tailed P < 0.001). There were no significant differences among female phenotype tendencies to prefer checker males (Fisher Exact Test; choice A in Table 1). Experiment 2. Females of the same phenotypes were given a choice between blue bar and ash red bar, between blue checker and ash red checker, and between blue bar and ash red checker. Seven choice pairs were used. All phenotypes preferred blue males to ash red males (binomial two-tailed P < 0.001). There was no significant difference between ash red female and blue female tendency to prefer blue to ash red males (Fisher Exact Test; choice B in Table 1). Blue bar males were preferred to ash red checker males (binomial two-tailed P < 0.001; choice C in Table 1). No female in either experiment 1 and 2 preferred a nest box to a particular male. Results indicate that female preference is transitive. Blue checker males are most preferred, followed by blue bar, and ash red males are least preferred, other factors being equal. If male selectivity depends on male quality, then blue checker males should be more selective in choosing mates than either
Table 2. Male choice of mate Choice
Chooser phenotype
Blue
Blue checker Bluebar Ash red Total
9 8 9 26
A Ash red 1 1
1 3
Nest box
Blue
1 2 4
10 9 8 27
7
B Ash red 0 1 1
2
C Nest box
Female
Nest box
0 2 4 6
16 6 3 25
4 9 22 35
A: Blue bar versus ash red bar and blue checker versus ash red checker. Four males made no choice. B: Blue bar versus ash red checker and blue checker versus ash red bar. Three males made no choice. C: Blue bar versus blue checker. Four males made no choice. [Male preference for bar versus checker females is complex and will be discussed elsewhere (unpublished).]
Evolution:
Proc. Natl. Acad. Sci. USA 74 (1977)
Burley
blue bar or ash red males. In turn, blue bar males sh~tud be more selective than ash reds. Experiment 3. Blue bar, blue checker, and ash red checker males were presented with choices between blue checker and ash red checker females, and between blue bar and ash red bar females. Three choice pairs were used. All male phenotypes preferred blue to ash red females (binomial two-tailed P < 0.002). Contrary to prediction, there was no significant difference between blue and ash red male tendency to prefer blue females, or to prefer a female to a nest box, or between blue checker and blue bar tendency to do so (Fisher Exact Test; choice A in Table 2). When given a choice between blue and ash red females, the three male phenotypes uniformly preferred blue females. The same experiment was repeated presenting the three male phenotypes with choice pairs of blue bar versus ash red checker, and blue checker versus ash red bar. Four choice pairs were used. Again all classes of males preferred blue to ash red females (binomial two-tailed P < 0.001), and no differences in the tendencies of the male phenotypic classes were noted (Fisher Exact Test; choice B in Table 2). Male and female preferences are similar in that color of potential mate (blue versus ash red) is more important than pattern (bar versus checker). Data from the two sets of choices presented in experiment 3 (Table 2, choices A and B) can be pooled to increase sample size, because the results of the experiments are identical. When this is done, it can be seen that ash red males are more likely than blue checker males to select nest boxes over mates (Fisher Exact Test, one-tailed P < 0.01), thus demonstrating some gradient in selectivity. Blue bar male tendency to select nest boxes over mates is intermediate between that of the other phenotypes, but not significantly different from either. Experiment 4. Males of the same three phenotypes were presented with choices between blue checker and blue bar females. Six choice pairs were used. When given this choice, more males picked nest boxes than when given the previous more "important" choice of color (Fisher Exact Test, one-tailed P < 0.001; Table 2, choice C). Blue bar males were more likely to choose nest boxes and accept either female than were blue checker males (Fisher Exact Test one-tailed P < 0.02). In turn, ash red males were more likely to choose nest boxes over particular females than were blue bar males (Fisher Exact Test one-tailed P < 0.05). Finally, comparison of sex-specific tendency to pick nest boxes reveals that males have a greater tendency to select boxes than do females (for data in Tables 1, choices A and B, and 2 choices A and B, Fisher Exact Test one-tailed P < 0.01). Discussion Further studies (unpublished) have shown that experimental females seldom select nest boxes except when males are very evenly matched over a number of criteria. The fact that females demonstrate this behavior, albeit infrequently, shows that nest box selection is not an exclusively male tactic. Its very low frequency indicates that females are overall more discriminating of potential mates than are males. These experiments suggest that in pigeons, females are relatively more selective of mates than males (Hypothesis 1). As expected, on certain criteria males of lower quality are less selective of mates than males of higher quality, that is, males are selective in proportion to their own quality as assayed by female preference (Hypothesis 2). As the relative magnitude of the difference in quality of potential mates increases, differences in male tendency to be selective disappear. High-quality males may be selective over a broader range of criteria, but on some criteria all males are somewhat selective.
3479
Contrary to expectation, females were not selective in proportion to their quality as determined by male choice (Hypothesis 2). However, only two criteria (color and pattern) were examined, and both of these appear to be important to females. A low-quality female should either be selective over a broader range of criteria than a male of similar quality and/or be more selective with regard to some criteria. Also, females should vary less in selectivity than males (Hypothesis 3). Therefore, I expect that the female pattern of selectivity is essentially similar to the male pattern, but that females have a lower threshold of selectivity than males. Results from experiments on other criteria support the finding that females are more selective than males. On some criteria, within-sex variability is apparent for females as well as males, but females do vary less overall than males. A question remains: if preferences are distinct and presumably functional, why are pigeon populations polymorphic? An answer to this question would require detailed demographic data on feral pigeons. A speculative suggestion is that the checker-bar dimorphism may be maintained by heterozygous advantage (23). The ash red-blue dimorphism is more difficult to explain (heterozygotes are ash red, and females are hemizygous for the trait), but a clue may lie in ash red male behavior. In my population, some ash red males are superior competitors for nest boxes, which in a nest-site-limited environment assures them of substantial reproductive success. I thank Nancy Moran, who assisted in developing the experimental design; Jayne Sherer, who collected data on times spent at nests by males and females; and Anthony Joern, Paul Mason, Daniel Otte, Eric R. Pianka, and Richard Symanski for helpful criticisms. This research was supported by National Science Foundation Grant BNS 76-
02972. 1. Trivers, R. L. (1972) in Sexual Selection and the Descent of Man, 1871-1971, ed. Campbell, B. (Aldine Publishing Co., Chicago, 2.
3. 4. 5.
6. 7.
8. 9. 10. 11. 12. 13. 14.
15. 16.
IL), pp. 136-179. Williams, G. C. (1966) Adaptation and Natural Selection (Princeton University Press, Princeton, NJ). Demerec, M. & Kaufmann, B. P. (1941) Am. Nat. 75, 366379. Parker, G. A. (1970) J. Anim. Ecol. 39,205-228. Darwin, C. (1871) The Descent of Man, and Selection in Relation to Sex (John Murray, London). Crook, J. H. (1972) in Sexual Selection and the Descent of Man, 1871-1971, ed. Campbell, B. (Aldine Publishing Co., Chicago, IL), pp. 231-281. Fisher, R. A. (1958) The Genetical Theory of Natural Selection (Dover Press, New York). Orians, G. H. (1969) Am. Nat. 103,589-603. Guiton, P. (1962) Symp. Zool. Soc. London 8,227-249. Hess, E. H. (1973) Imprinting (Van Nostrand-Reinhold, New York). Bateman, A. J. (1948) Heredity 2,349-368. Maynard Smith, J. (1956) J. Genet. 54, 261-279. Dawkins, R. & Carlisle, T. R. (1976) Nature 262, 131-132. Levi, W. (1967) The Pigeon (Levi Publishing Co., Sumter, SC). Dunmore, R. (1960) Am. Midl. Nat. 79, 1-7. Petersen a Botni, N. F. & Williamson, K. (1949) Ibis 91, 17-
23. 17. Murton, R. K. & Clarke, S. P. (1968) Br. Birds 61, 429-448. 18. Goodwin, D. (1952) London Bird Rep. 16,35-36. 19. Murton, R. K., Thearle, R. J. P. & Coombs, C. F. B. (1974) J. Appl.
Ecol. 11,841-854.
20. Cole, L. J. (1914) R.I. Agric. Exp. St. Bull. 158. 21. Hollander, W. (1938) Genetics 23, 12-23. 22. Horlacher, W. R. (1930) Genetics 15,312-346. 23. Ford, E. B. (1965) Genetic Polymorphism (M.I.T. Press, Cam-
bridge, MA).
Evolution
Parental investment, mate choice, and mate quality (sexual selection/sociobiology/Columba livia)
NANCY BURLEY* Department of Zoology, University of Texas at Austin, Austin, Texas 78712
Communicated by E. 0. Wilson, March 17, 1977
Current theory in sexual selection is extended ABSTRACT to predict within-sex variability with regard to selectivity towards mates in different mating systems. Generally, the sex that invests more in the care of each offs pring should be more selective of mates than the sex investing less. Within each sex, individuals of low mate quality should be less selective than individuals of high quality, but there should be less variation in selectivity among individuals of the sex investing more. When only one sex contributes parental care, however, individuals of that sex should be uniformly selective, while the other sex is expected to mate indiscriminately. Using feral pigeons (Columba livia), these hypotheses are tested for the case in which both sexes contribute substantial parental care, but in which females contribute more than males. As predicted, females were found to be more selective of mates than males were. On certain criteria, males of lower quality were less selective of mates than males of higher quality.
The recent concept of parental investment has revolutionized biologists' thinking on mating systems and factors that affect them (1, 2). Parental investment (PI) is defined as an investment in an offspring that simultaneously increases the offspring's likelihood of survival and reproduction while decreasing parental ability to invest in other offspring (1). PI patterns are expected to influence the selectivity of individuals of both sexes in choosing mates. Because the sex that invests more (usually female) stands to lose more in a mismating, individuals of that sex should select mates with greater care than members of the sex that invests less (usually male). When one sex contributes little or no PI, its members should be nondiscriminating, except when temporal constraints such as sperm depletion (3, 4) reduce access to simultaneously available mates. Within-sex selectivity Sexual selection theory can be extended to predict differences in selectivity among individuals of the same sex. How selective an individual is in mate choice should be affected by his or her genetic quality and, where applicable, investment capabilities. In most cases, superior individuals should be more selective than inferior ones. By making the assumption that attractiveness of an individual as a potential mate is a good index of the individual's mate quality, it follows that attractive individuals (as judged by members of the opposite sex) should be more selective than unattractive ones when choosing mates. Attractiveness can be ascertained when individuals of one sex or phenotype display consistent preferences for mates of a particular type. The existence of consistent female preferences was postulated by Darwin (5), and has been established for numerous species (1, 6); more recently the possibility of male preferences has also been considered (1, 7, 8), but only a few studies have been performed on it (9, 10). The costs of publication of this article were defrayed in part by the payment of page charges from funds made available to support the research which is the subject of the article. This article must therefore
Within-sex selectivity patterns should vary among breeding systems. In monogamous species that have substantial PI by both sexes, high-quality/attractive females should refuse courtship advances of unattractive males because they can attract superior ones. Unattractive females may be unable to form a pair bond with the most attractive males, and therefore should be more receptive to males of lower quality. However, such low-quality females may attract superior males as short-term copulatory partners, because males have little to lose from such alliances (sperm) and potentially much to gain (offspring in which they invest no PI). In monogamous systems, an inferior male should not restrict pair-bonding attempts to the best females, for he is likely to fail in competition for them with attractive males. In polygamous and promiscuous mating systems, one sex, typically male, invests little or nothing in PI (A in Fig. 1), and members of that sex gain little by being selective; their own attractiveness should not affect their selectivity. Therefore, males may mate indiscriminantly (8), so females are not limited in mate choice by their relative attractiveness. All females should mate with the best males, even if a number of females mate with the same individual. When males incur no PI, female selectivity should be largely independent of female quality (Fig. 2A). This has been demonstrated for Drosophila, among which female reproductive success is not limited by attractiveness, while male reproductive success varies widely and is dependent upon ability to attract females (11, 12). When males have substantial PI, but less than females (Fig. 1, between A and C), males should be more affected than females by their own quality when attempting to secure mates. Females are still more of a limiting resource; therefore males, the limited sex, experience more competition for mates. A female's greater range of mate choice should give her greater independence from her own attractiveness in the selection process. Individuals of the mate-limited sex should vary more overall in their tendency to be selective than should individuals of the limiting sex. In addition, for any given level of attractiveness/quality, individuals of the mate-limited sex (males) should be less selective than those of the limiting sex (females; Fig. 2B). When males and females have identical PI, their own attractiveness as mates should influence their tendency toward selectivity equally (Figs. 1, C, and 2C), although they may not select by the same criteria as long as sex roles are somewhat different. Therefore, as relative parental investment (fraction of total PI) increases from zero to one-half for males, the effect of an individual's attractiveness as a mate on its behavior when looking for a mate should converge for males and females. As male investment increases beyond one-half, as it may in polyandrous birds and some species of fish (2, 13), males should Abbreviation: PI, parental investment. * Present address: Department of Biology, McGill University, Montreal, Quebec H3A iBi, Canada.
be hereby marked "advertisement" in accordance with 18 U. S. C. §1734 solely to indicate this fact.
3476
Evolution: Burley
Proc. Natl. Acad. Sci. USA 74 (1977)
3477
phenotypes that occur in appreciable frequencies in feral pop*tions.,The adaptive significance of plumage polymor-
become more selective than females and less influenced by their own mate quality. Test hypotheses Following the above reasoning, one can test hypotheses that, when females contribute greater PI than males (Fig. 2B): (1) females are less likely than males to select mates on the basis of their own attractiveness, that is, overall their selectivity is higher; (2) within each sex, how selective an individual is will depend on how attractive he or she is to the opposite sex; and (3) overall, females should vary less in selectivity than males. Theoretically, organisms may select mates on the basis of numerous criteria that have both genetic and nongenetic components. Characteristics of potential mates that may be evaluated in species in which both parents contribute PI include fertility and fecundity, survival probability, food-getting and nest defense ability, territory quality, genetic and behavioral complementarity, reproductive experience, and fidelity. Cues to the recognition of these traits probably vary among species, and the sexes may be sensitive to different criteria.
phism is not known, but phenotypes may vary in longevity and/or fertility (15-17). I do not maintain that plumage phenotype is the only basis by which choice of mate is made among pigeons. To the contrary, I have investigated a number of other characteristics, such as nest defense ability, age, size, and reproductive experience, and have found that pigeons are sensitive to numerous traits (unpublished data). It is also possible that because sex roles differ, males and females may select mates by different criteria, or that males may be more selective with regard to some traits, whereas females are more sensitive to others. By studying characteristics of known genetic origin, this possibility is minimized, for if a genetic trait is important to the reproductive success of one sex, it should be of concern to both sexes when choosing mates because the trait will likely be transmitted to offspring. For example, if small size were a disadvantage to males, but had no effect on female reproductive success, both sexes might nevertheless avoid mating with small individuals. Females would avoid small males because of their low reproductive value, while males would avoid small females because of the low reproductive value of resulting sons (unless females only transmit genes for size to daughters). Predominant colors among feral pigeons are blue and ash red; common patterns are checker, velvet, and bar (15, 18, 19). Checker and velvet intergrade phenotypically, and birds from my population respond to them similarly, so I group both under the term "checker." Both color and pattern are simple Mendelian traits (20-22); color is sex-linked (14, 22). Several features of pigeon life history are salient. Courtship may be initiated by individuals of either sex. After forming a pair bond, pairs remain together for life, but individuals will remate within a month after the death or removal of their mate. Both parents share in incubation, brooding, and feeding of young, and nest defense. Females assume somewhat more than half of the total PI invested in each offspring that a pair-raises, on the basis of the relative time spent by females and males at the nest with eggs and offspring. Exact PI contribution of each sex varies among pairs (unpublished data).
MATE PREFERENCES AMONG PIGEONS To test these hypotheses, I have investigated preferences for particular plumage patterns and colors of feral pigeons (Columba livia). These characteristics were chosen for study both because there exists sufficient variability in pigeon plumage to permit testing of the hypotheses, and because the traits are almost entirely genetically determined (14). I have studied only
Experimental design The following experimental design is used to test preferences of pigeons that are captive descendants of wild-caught urban Texas birds. Test enclosures, measuring 4.5 X 2.1 X 2.5 m, contain one nest box at each end. A pigeon is tethered to each nest box on a string that allows it to fly no farther from its box than the center of the pen. Two tethered birds of the same sex
C.,~~~~Ct >Co~~~~~~o
.
0
1
1/2 6 PI/(d + 9) Pi
FIG. 1. Selectivity of males and females as a function of relative parental investment. At A, female choice of mate is independent of other females' choices. As male PI increases, females must consider not only inherent male quality, but also the number of females a given male is mated with. This restriction on female choice (and also on male choice) increases non-linearly with male PI. At C, sexes contribute identical PI and are equally selective. Beyond C, males are more selective than females.
A
c
C.4
C/,
0r Low
x Low High Self's quality as mate FIG. 2. Selectivity as a function of one's own quality as a mate. (A) Females assume total PI. (B) Females assume greater PI than males. For any level of mate quality, a female of that quality is more selective than a male of identical quality. The difference in selectivity for quality X is Y. Overall, females vary less in selectivity (V9) than males (Vd). (C) Males and females contribute equal PI.
High
3478
Evolution:
Burley
Proc. Natl. Acad. Sci. USA 74 (1977)
Table 1. Female choice of mate
of courting the previous female. Such behavior is interpreted to mean that either choice is acceptable to the chooser, and that choice of a particular mate is less important than possession of a box. Because this behavior may have some seasonal variability, all classes within experiments were tested simultaneously. Experiments 1 and 2 below were performed simultaneously between August and December 1975, while 3 and 4 were performed between December 1975 and February 1976. Two categories of experiments were performed, the first (1 and 2) to establish which male phenotypes are preferred by females, the second (3 and 4) to determine which female phenotypes are preferred by males. Individuals in each choice pair were matched for age, breeding experience, time in isolation, and size. I also used subjective measures to match individuals for aggressiveness. To minimize the effects of other types of variability which undoubtedly existed within choice pairs, a minimum of three pairs was used for each preference tested. All choosers had raised at least three clutches prior to experimentation. Because of the small number of ash red birds available, preferences between ash red phenotypes (bar versus checker) were not determined, and the results of experiments for ash red choosers are pooled, disregarding pattern pheno-
Choice A
Chooser phenotype
C
B
Blue Blue checker bar
Ash red
Blue
Ash Blue red bar checker
Bluechecker 8 1 9 1 9 0 Blue bar 13 3 11 1 10 1 Ash red 11 3 8 1 8 1 Total 32 7 28 3 27 2 A: Blue checker versus blue bar males. Eleven females made no choice. B: Blue bar versus ash red bar and blue checker versus ash red checker males. Four females made no choice. C: Blue bar versus ash red checker males. Three females made no choice.
constitute a choice pair from which a bird of the other sex makes a choice. A chooser is released into the pen and allowed to fly back and forth between members of the choice pair until it demonstrates a clear preference. At various intervals, choicepair birds are switched to opposite nest boxes to determine if the chooser actually prefers a bird or a nest box. Criteria of choice of a mate are complex, because individuals vary in behavior. The major criterion used to determine choice is that the chooser directs 90% of its courtship effort and spends most of its time with one individual for at least the hour prior to the end of an experiment. Often such pairs display initial stages of nesting behavior. Two to eight hours are required to fulfill this criterion, depending on season and degree of inequality between members of the choice pair. At the end of this period, the chooser is scored as having made choice of a mate (A or B), choice of a nest box (1 or 2), or no choice. In analysis of preferences, tests resulting in "no choice" are excluded as not being biased toward either mate or nest box. Criteria of choice are discussed in greater detail elsewhere (N. Burley and N. Moran, unpublished data). Nest boxes within pens are identical in size, construction, height above ground, and illumination. Nevertheless, males in particular sometimes establish preference for a certain nest box. When this occurs, a male characteristically spends much time in the preferred box, making "nest box calls" and courtship and nesting postures (14). When a female joins him in his box, he courts her, but when choice-pair birds are switched, he remains in the same box and courts a new bird, even after several hours
type.
Experimental results Experiment 1. Blue bar, blue checker, and ash red females were presented with choices between blue checker and blue bar males. Five choice pairs were used. Females of all phenotypes preferred checker to bar males (binomial two-tailed P < 0.001). There were no significant differences among female phenotype tendencies to prefer checker males (Fisher Exact Test; choice A in Table 1). Experiment 2. Females of the same phenotypes were given a choice between blue bar and ash red bar, between blue checker and ash red checker, and between blue bar and ash red checker. Seven choice pairs were used. All phenotypes preferred blue males to ash red males (binomial two-tailed P < 0.001). There was no significant difference between ash red female and blue female tendency to prefer blue to ash red males (Fisher Exact Test; choice B in Table 1). Blue bar males were preferred to ash red checker males (binomial two-tailed P < 0.001; choice C in Table 1). No female in either experiment 1 and 2 preferred a nest box to a particular male. Results indicate that female preference is transitive. Blue checker males are most preferred, followed by blue bar, and ash red males are least preferred, other factors being equal. If male selectivity depends on male quality, then blue checker males should be more selective in choosing mates than either
Table 2. Male choice of mate Choice
Chooser phenotype
Blue
Blue checker Bluebar Ash red Total
9 8 9 26
A Ash red 1 1
1 3
Nest box
Blue
1 2 4
10 9 8 27
7
B Ash red 0 1 1
2
C Nest box
Female
Nest box
0 2 4 6
16 6 3 25
4 9 22 35
A: Blue bar versus ash red bar and blue checker versus ash red checker. Four males made no choice. B: Blue bar versus ash red checker and blue checker versus ash red bar. Three males made no choice. C: Blue bar versus blue checker. Four males made no choice. [Male preference for bar versus checker females is complex and will be discussed elsewhere (unpublished).]
Evolution:
Proc. Natl. Acad. Sci. USA 74 (1977)
Burley
blue bar or ash red males. In turn, blue bar males sh~tud be more selective than ash reds. Experiment 3. Blue bar, blue checker, and ash red checker males were presented with choices between blue checker and ash red checker females, and between blue bar and ash red bar females. Three choice pairs were used. All male phenotypes preferred blue to ash red females (binomial two-tailed P < 0.002). Contrary to prediction, there was no significant difference between blue and ash red male tendency to prefer blue females, or to prefer a female to a nest box, or between blue checker and blue bar tendency to do so (Fisher Exact Test; choice A in Table 2). When given a choice between blue and ash red females, the three male phenotypes uniformly preferred blue females. The same experiment was repeated presenting the three male phenotypes with choice pairs of blue bar versus ash red checker, and blue checker versus ash red bar. Four choice pairs were used. Again all classes of males preferred blue to ash red females (binomial two-tailed P < 0.001), and no differences in the tendencies of the male phenotypic classes were noted (Fisher Exact Test; choice B in Table 2). Male and female preferences are similar in that color of potential mate (blue versus ash red) is more important than pattern (bar versus checker). Data from the two sets of choices presented in experiment 3 (Table 2, choices A and B) can be pooled to increase sample size, because the results of the experiments are identical. When this is done, it can be seen that ash red males are more likely than blue checker males to select nest boxes over mates (Fisher Exact Test, one-tailed P < 0.01), thus demonstrating some gradient in selectivity. Blue bar male tendency to select nest boxes over mates is intermediate between that of the other phenotypes, but not significantly different from either. Experiment 4. Males of the same three phenotypes were presented with choices between blue checker and blue bar females. Six choice pairs were used. When given this choice, more males picked nest boxes than when given the previous more "important" choice of color (Fisher Exact Test, one-tailed P < 0.001; Table 2, choice C). Blue bar males were more likely to choose nest boxes and accept either female than were blue checker males (Fisher Exact Test one-tailed P < 0.02). In turn, ash red males were more likely to choose nest boxes over particular females than were blue bar males (Fisher Exact Test one-tailed P < 0.05). Finally, comparison of sex-specific tendency to pick nest boxes reveals that males have a greater tendency to select boxes than do females (for data in Tables 1, choices A and B, and 2 choices A and B, Fisher Exact Test one-tailed P < 0.01). Discussion Further studies (unpublished) have shown that experimental females seldom select nest boxes except when males are very evenly matched over a number of criteria. The fact that females demonstrate this behavior, albeit infrequently, shows that nest box selection is not an exclusively male tactic. Its very low frequency indicates that females are overall more discriminating of potential mates than are males. These experiments suggest that in pigeons, females are relatively more selective of mates than males (Hypothesis 1). As expected, on certain criteria males of lower quality are less selective of mates than males of higher quality, that is, males are selective in proportion to their own quality as assayed by female preference (Hypothesis 2). As the relative magnitude of the difference in quality of potential mates increases, differences in male tendency to be selective disappear. High-quality males may be selective over a broader range of criteria, but on some criteria all males are somewhat selective.
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Contrary to expectation, females were not selective in proportion to their quality as determined by male choice (Hypothesis 2). However, only two criteria (color and pattern) were examined, and both of these appear to be important to females. A low-quality female should either be selective over a broader range of criteria than a male of similar quality and/or be more selective with regard to some criteria. Also, females should vary less in selectivity than males (Hypothesis 3). Therefore, I expect that the female pattern of selectivity is essentially similar to the male pattern, but that females have a lower threshold of selectivity than males. Results from experiments on other criteria support the finding that females are more selective than males. On some criteria, within-sex variability is apparent for females as well as males, but females do vary less overall than males. A question remains: if preferences are distinct and presumably functional, why are pigeon populations polymorphic? An answer to this question would require detailed demographic data on feral pigeons. A speculative suggestion is that the checker-bar dimorphism may be maintained by heterozygous advantage (23). The ash red-blue dimorphism is more difficult to explain (heterozygotes are ash red, and females are hemizygous for the trait), but a clue may lie in ash red male behavior. In my population, some ash red males are superior competitors for nest boxes, which in a nest-site-limited environment assures them of substantial reproductive success. I thank Nancy Moran, who assisted in developing the experimental design; Jayne Sherer, who collected data on times spent at nests by males and females; and Anthony Joern, Paul Mason, Daniel Otte, Eric R. Pianka, and Richard Symanski for helpful criticisms. This research was supported by National Science Foundation Grant BNS 76-
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