Song Repertoire and Mate Choice in Birds'

Transcription

1 AMER. ZOOL., 32:71-80 (1992) Song Repertoire and Mate Choice in Birds' WILLIAM A. SEARCY Department of Biological Sciences and Pymatuning Laboratory of Ecology, University of Pittsburgh, Pittsburgh, Pennsylvania SYNOPSIS. In many species of birds, individual males possess "repertoires" of multiple versions of the species song. Females of several of these species have been shown to respond preferentially in courtship to larger song repertoires. The female preference for large repertoires usually has little effect on female settlement, but is likely to affect mate choice in extra-pair copulations. A number of hypotheses have been proposed to explain the evolution of the female preference. Some of these posit a natural selective advantage for the preference, in securing for the female a better territory, better paternal care for the offspring, or a mate with good genes. Another hypothesis suggests the male trait and female preference have coevolved in a process of runaway sexual selection. Here I show that female common grackles (Quiscalus quiscula) court preferentially for repertoires of four song types compared to equal numbers of repetitions of single song types. The female preference exists in common grackles despite the fact that males in this species sing only one song type each. None of the usual hypotheses, based on natural or sexual selection, can explain the occurrence of the female preference in a species in which males lack the preferred trait. Instead, the female preference may be a simple consequence of two properties of most response systems: habituation and stimulus specificity. If so, female preferences for repertoires may in general pre-date the evolution of male song repertoires, which evolve to exploit the pre-existing female response bias. INTRODUCTION Bird songs are complex vocalizations that often constitute a prominent part of male display during the breeding season. In some species of birds, each male sings only one version of the species' song, though versions may still differ between males. In other species, each male sings multiple versions, and the collection of versions sung by one male is termed his "repertoire." Repertoires are of two kinds. In one, a male has a variable number of song components ("notes" or "syllables"), which he assembles in many different combinations; we can call this a "syllable repertoire." In the second, a male sings only certain, stereotyped combinations of notes and syllables, each combination being termed a "song type," and the collection of song types a "song type repertoire." Both syllable and song type repertoires can be considered elaborate male display traits, elaborate compared to the alternative of singing only one song type. Darwin (1871) proposed the theory of sexual selection to explain the evolution of 1 From the Symposium on Mechanisms of Mate Choice presented at the Annual Meeting of the American Society of Zoologists, December 1990, at San Antonio, Texas. 71 elaborate traits that differ between the sexes, so it is natural to hypothesize that sexual selection has played a part in the evolution of song repertoires (Kroodsma, 1977; Krebs andkroodsma, 1980; Catchpole, 1982). There is considerable evidence that repertoires have effects on intrasexual competition in male birds (Krebs et ai, 1978; Yasukawa, 1981a; Dufty, 1986), but here I shall concentrate solely on intersexual effects of repertoires. I willfirst review the evidence that female birds prefer more elaborate repertoires, and then I will consider the thornier question of how such preferences have evolved. FEMALE PREFERENCES Female preferences for elaborate repertoires have been examined through both laboratory experiments and field observations. In the laboratory experiments, bouts of song are played to captive females, and the response measure is some female behavior assumed to reflect female mating preferences. Table 1 reviews the results of such experiments for species in which males have either syllable or song type repertoires. The first such study (Kroodsma, 1976) measured female response in terms of nestbuilding behavior and egg laying, while all sub-

2 72 WILLIAM A. SEARCY TABLE 1. Laboratory tests of preferences for song repertoires in female birds. Species Response measure Results Reference Canary {Serinus canarius) Song sparrow (Melospiza melodid) Swamp sparrow (Melospiza georgiana) Sedge warbler (Acrocephalus schoenobaenus) Great reed warbler (Acrocephalus arundinaceus) Great tit (Pants major) Yellowhammer (Emberiza citrinella) Red-winged blackbird (Agelaius phoeniceus) nest-building, egglaying greater response to 35 syllables than to 5 syllables greater response to four types than to 1, to 8 types than to 4, and to 16 types than to 8 weak preference for four song types over one greater response to 24 and 41 syllables than to 14 greater response to syllable repertoires of 23 than 13 greater response to 3-5 song types than to 1-2 greater response to 2 or 3 song types than to 1 greater response to 4 song types than to 1 Kroodsma, 1976 Searcy and Marler, 1981 Searcy, 1984 Searcy et ai, 1982 Catchpole et al., 1984 Catchpole et ai, 1986 Baker et al., 1986 Bakers al., 1987 Searcy, 1988 sequent studies have measured copulation solicitation, a display given by female birds of many species before and during copulation. Details of methods differ between studies, but the results are uniform: females respond preferentially to large over small repertoires. The field studies have been entirely observational, examining correlations between male repertoire size and some measure of success in attracting females, such as earliness of pairing or number of females attracted. Results of the field studies are less uniform (Table 2). Some studies have found no correlation between repertoire size and measures of male success. Other studies have initially found significant correlations, but have then demonstrated that the correlation diminishes or disappears when some other factor is controlled, such as territory quality or male age. Only one study (Catchpole, 1980) has found a strong correlation between repertoire size and female choice with no evidence that the correlation is indirect. How can we reconcile the laboratory and field results? The laboratory results would seem to provide a reliable guide to female preferences for variants in male song, but these song-based preferences apparently are often not offirst importance in female choice of mates, at least not as mate choice is usually measured. The standard measures of male success in mating, as reflected in Table 2, actually measure female settlement on territories. The act of settling on a territory, besides influencing which male will father the female's offspring, also determines which male will provide parental care and what environment the young will be raised in. Territory quality is particularly important to female reproductive success in many birds, so it is not surprising that it also has a particular importance to female settlement choices (Searcy, 1982), an importance which tends to overshadow any effect of male song attributes. However, female birds in many species also exercise mate choice in another context, that of extra-pair copulations (Westneat et al., 1990), where neither territory quality nor male parental quality would be expected to play any role. In this context it is much more likely that song attributes such as repertoire size will play an important part in choice. Moreover, a male with a large repertoire may be more successful in stimulating his own mate to choose intra-pair over extra-pair copulations. Experiments measuring solicitation

3 SONG REPERTOIRE AND MATE CHOICE IN BIRDS 73 TABLE 2. Field tests of preferences based on song repertoire size in female birds. Species Results Reference males with large repertoires pair earlier, correlation largely disappears when territory Howard, 1974 quality controlled males with large repertoires do not have earlier laying dates or larger clutches harem size positively correlated with repertoire size but correlation disappears when male experience controlled males with large repertoires pair earlier Catchpole, 1980 Northern mockingbird (Mimus polyglottos) Great tits {Parns major) Red-winged blackbird (Agelaius phoeniceus) Sedge warblers (Acrocephalus schoenobaenus) Song sparrows (Melospiza melodia) Great reed warbler (Acrocephalus arundinaceus) males with large repertoires do not pair earlier, do not obtain replacement females faster males with large repertoires have larger harems, correlation reduced but still positive when territory quality controlled Krebs et at, 1978 McGregor et al., 1981 Yasukawa et al., 1980 Searcy, 1984 Catchpole, 1986 display seem to mimic extra-pair copulation events rather well. In the brood-parasitic brown-headed cowbird (Molothrus ater), males provide neither a territory nor parental care, and results on which song variants evoke solicitation display are excellent predictors of actual mating patterns (West etai, 1981). In conclusion, laboratory experiments show consistent preferences in female birds for large repertoires, while field observations argue that, in general, repertoire size has at most weak effects on female settlement patterns. However, it seems likely that female preferences for large repertoires have a more decided influence on female choice in the context of copulation. This prediction ought to be tested by relating repertoire sizes of males to their success in achieving fertilizations as determined by DNA methods. EVOLUTION OF FEMALE PREFERENCES Why do females prefer large repertoires? A large number of hypotheses have been proposed to answer this question (Searcy and Andersson, 1986). Here I will use the red-winged blackbird (Agelaius phoeniceus) to illustrate the various possibilities. Male red-winged blackbirds have repertoires of two to eight song types (Yasukawa, 1981a). The evidence for a female preference comes from laboratory experiments showing that female red-winged blackbirds implanted with estradiol display more for 32 songs of 4 song types than for 32 songs of single song types (Searcy, 1988). Again, it is not clear that this preference affects settlement patterns: Yasukawa et al. (1980) found that harem size was positively correlated with repertoire size, but the correlation disappeared when male breeding experience was controlled. Even if repertoire sizes do not influence female choice during settlement, they may still affect choice during extra-pair copulations, which are known to be common in this species (Gibbs et al, 1990). Male red-winged blackbirds, when confronted with a courting female, display their repertoires by switching song types more frequently, while they decrease switching frequencies when confronted with another male (Searcy and Yasukawa, 1990). These results argue that intersexual selection has been more important than intrasexual selection in the evolution of song repertoires in this species. A number of hypotheses propose that female preferences for repertoires have evolved in response to natural selective advantages. Thus, the preference may be advantageous in: (1) Securing a better territory. This possibility is plausible for redwinged blackbirds because repertoire size is correlated with male experience (Yasukawa et al, 1980), and more experienced males tend to have larger and better territories (Yasukawa, 1981ft). There is also direct evi-

4 74 WILLIAM A. SEARCY dence of correlations between repertoire size and territory quality (Yasukawa et al, 1980). Females settling on superior territories should experience improved breeding success. (2) Obtaining better male parental care. Again, males with large repertoires tend to be more experienced. Experienced males bring food to the nestlings more often than do younger males, and male feeding of young has a positive effect on the reproductive success of aided females (Patterson, 1979; Yasukawa et al, 1990). (3) Obtaining "good genes" for the offspring. This hypothesis assumes that large repertoire size is an "honest advertisement" (Kodric-Brown and Brown, 1984) of the possession of genes conferring high viability. Again, the correlation between male experience and repertoire size lends credence to this hypothesis, as experienced males have demonstrated their capacity for survival. The honest advertisement hypothesis has been advocated for the evolution of repertoire preferences in general by Baker et al (1986, 1987). Another possibility is that female preferences for large repertoires have been favored by sexual selection rather than natural selection. Under this hypothesis, the female preference and male trait coevolve in a Fisherian runaway process (Fisher, 1930). Here, the preference is favored because females with the preference have sons that possess the favored trait and that therefore experience high mating success. Genetic models indicate that this coevolutionary process may work (Lande, 1981, 1982). This hypothesis has been advocated as a general explanation of repertoires and repertoire preferences by Catchpole (1980; Catchpole et al., 1986). The revolutionary models must assume that both the male trait and the female preference are heritable, which has not been tested in red-winged blackbirds. Yet another general explanation for female preferences based on male display is that the preferences have evolved to further species recognition. This hypothesis seems unlikely to apply to repertoire preferences. Searcy and Andersson (1986) argue that female preferences that evolve to further species recognition ought usually to favor display values in the middle of the species' character distribution. Repertoire preferences, on the other hand, seem to favor extreme values, i.e., the largest repertoires (Searcy, 1984; Catchpole et al, 1984), though this has not been examined in redwinged blackbirds. Moreover, the structure of individual songs allow species recognition in red-winged blackbirds (Brenowitz, 1983; Searcy, 1990) without requiring females to listen to long bouts of song. We are left, then with three hypotheses that assume a natural selective benefit of repertoires and one that assumes a sexual selective benefit. Repertoire preferences cannot be said to be adaptive under all of these hypotheses, as runaway selection does not produce adaptation as it is usually understood. However, under each hypothesis the female preference is shaped by selection, so I will categorize all four hypotheses as "selection hypotheses." The selection hypotheses assume that the female preference has either evolved in response to an existing male trait and its value as a signal of good territory, good parental care, or good genes, or that the preference and male trait have coevolved. A contrasting possibility is that the female preference pre-dates the male trait. One way for this to occur is for the female preference to reflect a general sensory bias, which the male display trait subsequently exploits (Ryan et al, 1990). For example, female preferences for calls containing low frequency chucks in the frog Physalaemus pustulosus reflect the tuning of the female's basilar papilla. As evidence that the tuning of the auditory system pre-dates the male display feature, Ryan et al. (1990) showed that in a closely related species, Physalaemus coloradorum, basillar papilla tuning was similar, even though calls of males do not contain a chuck. Thus the chuck in pustulosus may represent "sensory exploitation." Clearly, one type of evidence for preexisting female preferences is the existence of preferences in species lacking the male trait. Focussing again on avian song repertoires, female preferences for repertoires have been investigated in two species in which males lack repertoires, field sparrows (Spizella pusilla) and white-throated spar-

5 SONG REPERTOIRE AND MATE CHOICE IN BIRDS 75 rows {Zonotrichia albicollis). In neither species was there a significant female preference for four song types over single song types (Searcy and Marler, 1984). These results argue against pre-existing female preferences. However, more recent experiments on common grackles (Quiscalns quiscula) indicate pre-existing preferences for repertoires can occur. RESPONSE TO REPERTOIRES IN COMMON GRACKLES Here I report previously unpublished results on the response of female common grackles to 32 songs of either four song types or a single song type. Male common grackles sing only one song type each (Wiley, 1976), so the "repertoires" were compiled from different individuals. This is the same procedure used with field sparrows and whitethroated sparrows (Searcy and Marler, 1984). Methods replicated closely those used in tests of red-winged blackbirds (Searcy, 1988). Subjects were adult female common grackles captured during the spring of 1987 and 1988 in the vicinity of the Pymatuning Laboratory of Ecology in Linesville, Pennsylvania. Each subject was given a single implant of 17-beta-estradiol in silastic tubing. Implants were of 1.96 mm outside diameter and 24 mm long, and contained mm of hormone. An implant was slipped under the skin of a subject's back through a small incision made after application of a topical anesthetic. Subjects were housed singly in sound attenuation chambers and maintained on cycles of 16 hours light, 8 hours dark. Testing began 7 days after treatment. Songs were played from a Tandberg TB15 tape recorder over a Realistic speaker (effective range 90-20,000 Hz) inside the chamber. An observer viewed the subject from behind a blind in a darkened room and through a window in the chamber door. Responses were scored on a 0 to 3 scale: 0 for no display, 1 for an incomplete display, 2 for a complete display of short duration (<1 sec), and 3 for a complete, prolonged display. Test songs were recorded from males in the Linesville area. The repertoire vs. single song type experiment was performed twice, with different repertoires. In each case, the repertoire playback consisted of 32 songs of 4 types, ordered in eventual variety (8 As, 8 Bs, 8Cs, and 8Ds). For both experiments, four single-type bouts were recorded, each consisting of 32 repetitions of one of the same song types used in the corresponding four-type bout. Subjects were tested on four days in each experiment. On day 1, one of the single-type bouts was chosen randomly for each subject, on day 2 one of the remaining three single-type bouts was chosen, etc. This design ensures that all subjects hear each song type equally often in single-type and repertoire playbacks, thus controlling for the possibility that females prefer certain song types over others. The four-type bout was recorded so that the 32 songs could be started with any of the four types, and the starting type was chosen randomly each day for each subject. Order of presentation of single-type and four-type playbacks was randomized for each subject on the first and third days of testing and was reversed on the second and fourth. Playbacks to a given subject within a day were performed at least 3 hours apart. Before the repertoire tests, female common grackles were tested for discrimination between a single grackle song type and a single heterospecific song, as a test of whether conspecific song stimulates female courtship in this species. The heterospecific song was from a male red-winged blackbird. Playback tapes in this preliminary test consisted of 12 songs recorded at one song every 15 sec. Subjects were tested twice each, with the order randomized the first time and reversed the second. Eight of nine female grackles displayed for the grackle song, vs. two for heterospecific song. Display scores averaged 30.2 (±9.4 SE) for the 24 repetitions of conspecific song compared to 2.2 (±1.8) for the heterospecific songs (Wilcoxon T = 0, z = 2.53, P < 0.05 two-tailed). Number of displays was also significantly greater for the conspecific song (13.0 ± 3.4) than for the heterospecific (1.2 ± 1.0; T = 0, z = 2.53, P < 0.05). The first repertoire vs. single type experiment was performed with 18 subjects, 17 of which responded with displays. The mean

6 76 WILLIAM A. SEARCY display score per 32 songs was significantly higher for four song types (38.8 ± 6.4) than for the single songs (33.5 ± 6.2; T = 14, N = 17, z = 2.96, P < 0.01 two-tailed). Mean number of displays was also significantly higher for the repertoire (17.1 ± 2.6) than for the single songs (15.3 ± 2.6; T = 25, z = 2.44, P < 0.05). The second repertoire vs. single type experiment was performed with 10 subjects, of which 8 responded with displays. Mean display score per 32 songs was again significantly higher for four-types (42.3 ± 8.9) than for the single types (32.6±7.5;T = 0, z = 2.52, P < 0.05 two-tailed). Mean number of displays was also significantly higher for the repertoire (18.8 ± 3.7) than for the single song types (15.9 ± 3.3; T = 3.5, z = 2.03, P < 0.05). Female grackles, then, show a preferential response to repertoires even though male grackles do not have repertoires. None of the selection-based hypotheses proposed to explain the repertoire preference in redwinged blackbirds can explain the preference in grackles. In grackles, the preference cannot have evolved to aid females in securing better territories, as repertoire size can provide no information on territory quality in a species in which all males have but a single song type. Following similar reasoning, the preference for repertoires in grackles cannot have evolved to aid females in obtaining mates that will provide better parental care or better genes. Finally, runaway selection cannot have caused the coevolution of the female preference and the male trait, as the male trait has not evolved. While the existence of a preference for repertoires in female grackles is not compatible with any of the selection hypotheses, it is compatible with the hypothesis that male display traits evolve to exploit preexisting female biases. HABITUATION AND RESPONSE SPECIFICITY Why might female birds have a pre-existing bias to respond preferentially to multiple song types? An answer is suggested by looking at the details of female response to the repertoire presentations. Figure 1 shows for both sets of repertoire and single-type playbacks the mean response of female grackles to each song in the 32 song bouts, averaged across all subjects and all trials. In each of the two experiments, mean response was high for the first song in both the repertoire and single-type bouts, and then decreased for subsequent songs. The response decrement continues through all 32 songs for the single song type bouts, while for the repertoire bouts the decrease is interrupted by a recovery in response whenever song types are switched. It is the effect of these recoveries that causes overall response to be greater for repertoires than for single song types. The increase in response is significant for each of the three song type switches in both experiments (P < 0.05 by two-tailed Wilcoxon Matched Pairs tests). By contrast, there are no significant increases in response between any two successive songs for the single-type bouts. Female red-winged blackbirds showed a similar time course of response, though here, in the one experiment done, only two of three recoveries were statistically significant (Searcy, 1988). In swamp sparrows (where males have repertoires of two to five song types), females tested in the same manner also snowed this pattern of response, with two of three recoveries being significant (Searcy and Marler, 1984). Female field sparrows and white-throated sparrows, though showing no overall preference for repertoires, did show an increase in mean response at each switch, and in field sparrows one of the recoveries was significant (Searcy and Marler, 1984). It can be argued that the response pattern shown by grackles is the product of two builtin features of animal nervous systems: habituation and stimulus specificity. Habituation is "the relatively permanent waning of a response as a result of repeated stimulation which is not followed by any kind of reinforcement" (Thorpe, 1963). "Relatively permanent" is specified to exclude very short term waning of response due to neuronal refractory periods, effector fatigue, or sensory adaptation (Hinde, 1970). Habituation is nearly universal in animal behavior (Hinde, 1970). Stimulus specificity means that the response decrement is specific to a particular stimulus, so that response

7 SONG REPERTOIRE AND MATE CHOICE IN BIRDS 77 recovers when the stimulus is changed. Again, stimulus specificity is very widespread (Hinde, 1970), and in fact it is hard to imagine a complete lack of specificity. Habituation and stimulus specificity combine to make the pattern of response shown by female birds to song very widespread. For example, this pattern of habituation and recovery is shown in the orientation response of the water bug Notonecta glauca towards disturbance in the surface film (Wolda, 1961), the withdrawal response of the snail Limnaea stagnalis to mechanical and visual stimuli (Crook, 1970), the aggressive response of the fish Gasterosteus aculeatus towards male conspecifics (Peeke and Veno, 1973), and the gobbling response of turkeys (Meleagris gallapavo) to sounds of different frequencies and intensities (Schleidt, 1954). Similar patterns of habituation and recovery can also be seen at the cellular level, as in the response of cells in the superior colliculus of the rabbit to tones of different frequencies (Horn and Hill, 1966). This pattern can also be seen in other responses to song by birds, for example in the aggressive response of male red-winged blackbirds to song (Yasukawa, 1981a). The argument, then, is that habituation and stimulus specificity are very widespread features of response systems, likely to be built into nervous systems in the absence of selection against them. A response pattern in which female response habituates to repetitions of one song type and recovers when the song type is switched would therefore be the null state, the pattern expected unless there is explicit selection against it. Thus we might expect a pre-existing female bias in favor of larger repertoires. To summarize, the evidence in favor of pre-existing female preferences for multiple song types is: (1) the existence of a preference for multiple song types in female common grackles, a species in which males lack repertoires so that none of the selection hypotheses can explain the preference; (2) the pattern of habituation and recovery shown to playbacks of multiple song types by females in common grackles and other species; and (3) the widespread nature of this type of response pattern in animals in general. Q. in a Song Number Song Number FIG. 1. Response of female common grackles to (a) the first set of 32 songs of either four song types (repertoire) or a single song type and (b) the second set of 32 songs of either four types or a single type. * indicates a change in response significant at the 0.05 level (by a two-tailed Wilcoxon matched pairs test). COEVOLUTION OF FEMALE PREFERENCES AND MALE TRAIT Even when there is a pre-existing female bias towards a particular male display trait, both the female preference and the male trait can still be exaggerated over time through coevolution. Such coevolution is predicted by some genetic models of the evolution of female choice (Fisher, 1930; Lande, 1981). These models make a number of assumptions that have not been tested in regards to avian song repertoires, notably that both the strength of the female preference and the elaboration of the male trait are heritable. Nevertheless, we can test a prediction of the coevolutionary models, namely that across species the strength of the female preference should be correlated with the elaboration of the male trait. In practice, testing this prediction is not straightforward in regards to song reper-

8 78 WILLIAM A. SEARCY c o O at E 0.8 Median Repertoire Size FIG. 2. Strength of female preference for four song types over single song types plotted against median repertoire sizes of males for six species of passerine birds. The six species are white-throated sparrows, field sparrows, and common grackles with median repertoires of one, swamp sparrows with median repertoires of three, red-winged blackbirds with median repertoires of four, and song sparrows with median repertoires of nine. toires. One problem is that comparisons of repertoire sizes across species can be misleading (Kroodsma, 1982), especially when one mixes song type repertoires and syllable repertoires. This problem is minimized in our work because the three species we have studied that possess repertoires all have song type repertoires. Another difficulty is that details of playback organization and response measures often differ between studies, making comparisons of female preference strengths across studies problematic. Again, this problem is minimized in our work, because we have presented to six different species the same playback organization, namely 32 songs of either four types or single types, and have used the same response measure throughout. The results on strengths of female preference vs. male repertoire size are illustrated in Figure 2 for the six species studied: song sparrows, swamp sparrows, white-throated sparrows, field sparrows, red-winged blackbirds, and common grackles. Strength of preference is measured as the ratio of mean female response score for four types relative to the mean for single types. No statistical test of relationship is made, primarily because of the problem of not knowing which sample points are independent (Ridley, 1983). Nevertheless, visual inspection of the results gives some preliminary support for the coevolutionary hypothesis. The correlation shown in Figure 2 is a test of the coevolutionary hypothesis, in that absence of such a correlation would constitute evidence against coevolution. However, this is not a strong test because alternative hypotheses also predict the same correlation. As one example, females in each species might have pre-existing preferences, and the strength of these preferences might differ between species. Males might then evolve larger or smaller repertoires in response to the strength of the female preference in their species, producing the observed correlation. CONCLUSIONS I have argued that female birds may have pre-existing preferences for large repertoires, pre-existing in the sense that they pre-date the evolution of repertoires in males. The preferences come about because the courtship responses of female birds to male song show both habituation and stimulus specificity, as do almost all response systems. Habituation and stimulus specificity are presumably properties of the central nervous system rather than the sense organs, so the evolution of repertoires in males might better be termed "neural exploitation" rather than "sensory exploitation." Neural exploitation would explain the origin of repertoires, which might or might not have been further elaborated due to Fisherian sexual selection. ACKNOWLEDGMENTS This research was supported by NSF grants BNS and BNS I thank John Mull and Donald Gillespie for help with the experiments, and Steve Gaulin, Walt Wilczynski, and an anonymous reviewer for comments on the manuscript. REFERENCES Baker, M. C, T. K. Bjerke, H. Lampe, and Y. Espmark Sexual response of female great tits to variation in size of males' song repertoires. Am. Natur. 128: Baker, M. C, T. K. Bjerke, H. Lampe, and Y. Espmark Sexual response of female yellowhammers to differences in regional song dialects and repertoire sizes. Anim. Behav. 35: Brenowitz, E. A The contribution of temporal song cues to species recognition in the red-winged blackbird. Anim. Behav. 31:

9 SONG REPERTOIRE AND MATE CHOICE IN BIRDS 79 Catchpole, C. K Sexual selection and the evolution of complex songs among European warblers of the genus Acrocephalus. Behaviour 74: Catchpole, C. K The evolution of bird sounds in relation to mating and spacing behavior. In D. E. Kroodsma, E. H. Miller, and H. Oullet (eds.), Acoustic communication in birds, Vol. 1, pp Academic Press, New York. Catchpole, C. K Song repertoires and reproductive success in the great reed warbler Acrocephalus arundinaceus. Behav. Ecol. Sociobiol. 19: Catchpole, C. K., J. Dittami, and B. Leisler Differential responses to male song repertoires in female songbirds implanted with oestradiol. Nature 312: Catchpole, C. K., B. Leisler, and J. Dittami Sexual differences in the responses of captive great reed warblers Acrocephalus arundinaceus to variation in song structure and repertoire size. Ethology 73: Cook, A Habituation in a freshwater snail (Limnaea stagnalis). Anim. Behav. 178: Darwin, C The descent of man, and selection in relation in sex. John Murray, London. Dufty, A. M., Jr Singing and the establishment and maintenance of dominance hierarchies in captive brown-headed cowbirds. Behav. Ecol. Sociobiol. 19: Fisher, R. A The genetical theory of natural selection. Clarendon, Oxford. Gibbs, H. L., P. J. Weatherhead, P. T. Boag, B. N. White, L. M. Tabak, and D. J. Hoysak Realized reproductive success of polygynous redwinged blackbirds revealed by DNA markers. Science 250: Hinde, R. A Behavioural habituation. In G. Horn and R. A. Hinde (eds.), Short-term changes in neural activity and behaviour, pp Cambridge Univ. Press, Cambridge. Horn, G. and R. M. Hill Responsiveness to sensory stimulation of units in the superior colliculus and subjacent tectotegmental regions of the rabbit. Exp. Neurol. 14: Howard, R. D The influence of sexual selection and interspecific competition on mockingbird song (Mimus polyglottos). Evolution 28: Kodric-Brown, A. and J. H. Brown Truth in advertising: The kinds of traits favored by sexual selection. Amer. Natur. 124: Krebs, J. R., R. Ashcroft, and M. I. Webber Song repertoires and territory defence. Nature 271: Krebs, J. R. and D. E. Kroodsma Repertoires and geographical variation in bird song. Adv. Study Behav. 11: Kroodsma, D. E Reproductive development in a female songbird: Differential stimulation by quality of male song. Science 192: Kroodsma, D. E Correlates of song organization among North American wrens. Am. Natur. 111: Kroodsma, D. E Song repertoires: Problems in their definition and use. In D. E. Kroodsma, E. H. Miller, and H. Oullet (eds.), Acoustic communication in birds, Vol. 2, pp Academic Press, New York. Lande, R Models of speciation by sexual selection of polygenic traits. Proc. Natl. Acad. Sci. U.S.A. 78: Lande, R Rapid origin of sexual isolation and character divergence in a cline. Evolution 36: McGregor, P. K., J. R. Krebs, and C. M. Perrins Song repertoires and lifetime reproductive success in the great tit (Parus major). Am. Natur. 118: Patterson, C. B Relative parental investment in the red-winged blackbird. Ph.D. Diss., Indiana University. Bloomington, Indiana. Peeke, H. V. S. and A. Veno Stimulus specificity of habituated aggression in three-spined sticklebacks (Gasterosteus aculeatus). Behav. Biol. 8:427^32. Ridley,M The explanation of organic diversity: The comparative method and adaptations for mating. Clarendon Press, Oxford. Ryan, M. J., J. H. Fox, W. Wilczynski, and A. S. Rand Sexual selection for sensory exploitation in the frog Physalaemus pustulosus. Nature 343: Schleidt, M Untersuchungen uber die Auslosung des Kollerns beim Truthahn (Melagris gallopavo). Z. Tierpsychol. 11: Searcy, W. A The evolutionary effects of mate selection. Ann. Rev. Ecol. Syst. 13: Searcy, W. A Song repertoire size and female preferences in song sparrows. Behav. Ecol. Sociobiol. 14: Searcy, W. A Dual intersexual and intrasexual functions of song in red-winged blackbirds. Proc. XIX Int. Congr. Ornithol. 1: Searcy, W. A Species recognition of song by female red-winged blackbirds. Anim. Behav. 40: Searcy, W. A. and M. Andersson Sexual selection and the evolution of song. Ann. Rev. Ecol. Syst. 17: Searcy, W. A. and P. Marler A test for responsiveness to song structure and programming in female sparrows. Science 213: Searcy, W. A. and P. Marler Interspecific differences in the response of female birds to song repertoires. Z. Tierpsychol. 66: Searcy, W. A., M. H. Searcy, and P. Marler The response of swamp sparrows to acoustically distinct song types. Behaviour 80: Searcy, W. A. and K. Yasukawa Use of the song repertoire in intersexual and intrasexual contexts by male red-winged blackbirds. Behav. Ecol. Sociobiol. 27: Thorpe, W. H Learning and instinct in animals. Harvard Univ. Press, Cambridge. West, M. J., A. P. King, and D. H. Eastzer Validating the female bioassay of cowbird song: Relating differences in song potency to mating success. Anim. Behav. 29: Westneat, D. F., P. W. Sherman, and M. L. Morton The ecology and evolution of extra-pair copulations in birds. Current Ornithol. 7:

10 80 WILLIAM A. SEARCY Wiley, R. H Communication and spatial relationships in a colony of common grackles. Anim. Behav. 24: Wolda, H Response decrement in the preycatching activity of Notonecta glauca L. (Hemiptera). Arch. Neerl. Zool. 14: Yasukawa, K. 1981a. Song repertoires in the redwinged blackbird (Agelaius phoeniceus): A test of the Beau Geste hypothesis. Anim. Behav. 29: Yasukawa, K Male quality and female choice of mate in the red-winged blackbird (Agelaius phoeniceus). Ecology 62: Yasukawa, K., J. L. Blank, and C. B. Patterson Song repertoires and sexual selection in the redwinged blackbird. Behav. Ecol. Sociobiol. 7: Yasukawa, K., J. L. McClure, R. A. Boley, and J. Zanocco Provisioning of nestlings by male and female red-winged blackbirds, Agelaius phoeniceus. Anim. Behav. 40: