Correlated changes in male plumage coloration and female mate choice in cardueline finches

The coevolution of extravagant male traits and female mate preferences is a central tenet of sexual selection theory. In lineages in which males have developed more elaborate sexual characters, females favour the most extreme expression of the trait. In some taxa, however, ornamental displays have evolved from more to less exaggerated states. Under these circumstances, it is unclear whether females show preferences for an ancestral male condition or for the current, less elaborate display. Here, we tested female mate preferences relative to male ornamental coloration in two species of cardueline finch (the American goldfinch, Carduelis tristis, and pine siskin, Carduelis pinus) that have evolved less elaborate carotenoid-based colour displays from more elaborately coloured ancestral states. We presented females of each species with a choice of males having either large patches of red colour (the elaborate, ancestral condition) or with species-typical patches of yellow colour (the less elaborate, derived state). Female goldfinches and siskins showed consistent preferences for the natural colour displays of males, and not for the more elaborate, ancestral colour pattern. Previous research on another cardueline finch taxon (a subspecies of the house finch, Carpodacus mexicanus griscomi), however, showed that females prefer more elaborate, ancestral coloration to the current form of reduced colour expression. The lack of congruence between male trait expression and female trait preference in the lineage with the most recently derived reduction in trait expression suggests that there may be evolutionary lags in the correspondence between male traits and female preferences. A shift in the expression of male coloration appears to be the first step towards the evolution of reduced colour displays in these finches.     

Female mate choice as a condition-dependent life-history trait

The acquisition of resources is an important determinant of patterns of variation in and covariation among traits that are costly to produce and are dependent on condition for their expression. However, the extent to which variation in female mate choice behavior is condition dependent, and how this is related to other life-history traits, remains largely unknown. We manipulated the acquisition of dietary protein in the black field cricket, Teleogryllus commodus, and measured the effects of this on several important life-history traits and on female mate choice behavior. Females reared on a high-protein diet developed faster, were heavier at eclosion, and lived longer than females reared on a low-protein diet. Two lines of evidence suggest that female mate choice behavior in T. commodus is condition dependent. First, females reared on the high-protein diet were more sexually responsive and expressed stronger linear and quadratic preference functions for call rate and dominant frequency, respectively. Second, within treatments, females that developed faster were lighter, generally less sexually responsive, and, in the high-protein-diet treatment, expressed weaker preferences than slower-developing females. Collectively, our findings suggest an important role for resource acquisition in generating variation in mate choice behavior.     

An experimental test of condition-dependent mating behavior and habitat choice by water striders in the wild

Individual condition is expected to be an important determinantof many behaviors, including mating dynamics and habitat choice.In this study we experimentally investigated the linkages betweenindividual condition, habitat use, and mating dynamics in thewild. We manipulated recent feeding history of the water strider,Aquarius remigis, and then quantified the habitat use and matingactivity of males and females. Females could choose from threehabitats (refuge, near shore, and open). On the water surface(open and near-shore habitats), in contrast to refuge, femalescan forage, but they are exposed to predation and sexual harassmentby males. We tested three main hypotheses. First, we predictedthat single females that were fed, relative to those that werenot, would reduce their exposure to predators and male harassmentby increasing their use of refuge. Similarly, we predicted thatfed females that were mating would spend more time in refugethan those that were not fed. Our results support these twopredictions. Fed single and mating females significantly increasedtheir use of refuge. Third, we predicted that mating activity(proportion of time spent mating) of fed females would be reducedrelative to starved females, because of reduced exposure tomales while in refuge, and perhaps because of decreased receptivityto male mating attempts while on the water surface. Mating activityof fed females was about one third that of starved females.The decrease in mating activity could not be accounted for byany change in female receptivity, but could be accounted forby change in habitat use. The decrease in mating activity mayhave resulted from decreases in both mating frequency and matingduration. Our estimates of minimum mating frequency indicatea large and significant decrease, but we were unable to assessmating duration. We found no significant effect of our manipulationon habitat use or mating activity of males.[Behav Ecol 7: 474–479(1996)]     

Early exposure leads to repeatable preferences for male song in female zebra finches

This study addressed the question of how early learning processes in females influence later preferences for a male trait. I tested whether exposure to song alone (of a male other than the father) was sufficient for inducing a stable (repeatable) preference in female zebra finches (Taeniopygia guttata) by limiting early exposure to tape tutoring. A group of controls heard no songs before also being tested in adulthood. Repeated tests for preferences for tutor or unfamiliar song were made, interspersed with additional tests involving new songs. Preferences were tested in an operant task where pecking of response keys led to song playback. Most females significantly preferred one of the two songs in a given test. In the first test, the relative preference for the tutor song was significantly higher for the tutored than for the control females. Subsequently, tutored females' preferences for the tutor song remained higher on average, but the two groups did not differ significantly. However, tutored, but not untutored females' preferences were highly repeatable between tests, suggesting that early exposure to song might lead to a consolidation ol choice behaviour, a previously unknown effect of early exposure to song in female songbirds.     

Bill redness is positively associated with reproduction and survival in male and female zebra finches

Sexual traits can serve as honest indicators of phenotypic quality when they are costly. Brightly coloured yellow to red traits, which are pigmented by carotenoids, are relatively common in birds, and feature in sexual selection. Carotenoids have been linked to immune and antioxidant function, and the trade-off between ornamentation and these physiological functions provides a potential mechanism rendering carotenoid based signals costly. Mutual ornamentation is also common in birds and can be maintained by mutual mate choice for this ornament or by a correlated response in one sex to selection on the other sex. When selection pressures differ between the sexes this can cause intralocus sexual conflict. Sexually antagonistic selection pressures have been demonstrated for few sexual traits, and for carotenoid-dependent traits there is a single example: bill redness was found to be positively associated with survival and reproductive output in male zebra finches, but negatively so in females. We retested these associations in our captive zebra finch population without two possible limitations of this earlier study. Contrary to the earlier findings, we found no evidence for sexually antagonistic selection. In both sexes, individuals with redder bills showed higher survival. This association disappeared among the females with the reddest bills. Furthermore, females with redder bills achieved higher reproductive output. We conclude that bill redness of male and female zebra finches honestly signals phenotypic quality, and discuss the possible causes of the differences between our results and earlier findings.     

Cultural influences on female mate choice: an experimental test in cowbirds, Molothrus ater

Previous studies of brown-headed cowbirds Molothrus ater, have shown that social learning and cultural transmission can influence courtship and mating patterns. These earlier studies did not test whether cultural background influenced mate choice in females and therefore whether culture could potentially play a role in sexual selection in this species, as has been suggested by recent theory. Here, we tested whether culture influences female mate choice in brown-headed cowbirds. Female cowbirds from a South Dakota population were housed with adult cowbirds from the same South Dakota population or with adult cowbirds from a behaviourally distinct population from Indiana. We tested the mating preferences of females of the South Dakota culture and females of the Indiana culture in sequential mate-choice trials with males, controlling for intrasexual interactions. The males were South Dakota cowbirds that had also been housed either in the South Dakota culture or in the Indiana culture. Females showed mating preferences for males from their own culture. These results suggest that mate choice in female cowbirds can be influenced by cultural background. We briefly discuss the effect that culture may have on sexual selection and on the evolution of female mating preferences. Copyright 1999 The Association for the Study of Animal Behaviour.     

Coevolution of costly mate choice and condition-dependent display of good genes.

Females often choose their mates, instead of mating at random, even when a father contributes nothing but genes to his offspring. Costly female preferences for males with exaggerated traits that reduce viability, such as the peacock's tail, are particularly puzzling. Such preferences can evolve if directly favoured by natural selection or when the exaggerated trait, although maladaptive per se, indicates high overall quality of the male's genotype. Two recent analyses suggested that the advantage to mate choice based on genetic quality is too weak to explain extreme cases of exaggeration of display traits and the corresponding preferences. We studied coevolution of a female mate-preference function and a genotype-dependent male display function where mutation supplies variation in genotype quality and mate preference is costly. Preference readily evolves, often causing extreme exaggeration of the display. Mate choice and trait expression can approach an equilibrium, or a limit cycle, or exaggeration can proceed forever, eventually causing extinction.     

Effects of central vasotocin and mesotocin manipulations on social behavior in male and female zebra finches

Male and female zebra finches (Taeniopygia guttata; total n = 40) were fitted with chronic guide cannulae directed at the lateral ventricle and were tested for aggression, affiliation, and partner preference following infusions of mesotocin (MT), vasotocin (VT), their antagonists, and vehicle control. Aggressive behavior was tested in a mate competition paradigm and tests of intersexual affiliation and partner preference were conducted following 1 day of cohabitation with an opposite-sex individual. These tests also provided data on male courtship singing. The results demonstrate a modest dose-dependent facilitation of aggression by VT, but not MT, in both male and female finches. However, only males were sensitive to infusions of a vasopressin antagonist, suggesting that endogenous VT is more important for behavioral modulation in males. Peptide effects were specific to aggression, as no treatments influenced intersexual affiliation, partner preference, or male courtship singing. Thus, in contrast to rodents, partner preference is not readily induced by VT or MT in this species. However, the potential necessity of endogenous VT and MT for natural pair-bond formation remains to be tested.     

Neighbours' breeding success and the sex ratio of their offspring affect the mate preferences of female zebra finches

Several hypotheses on divorce predict that monogamous pairs should split up more frequently after a breeding failure. Yet, deviations from the expected pattern "success-stay, failure-leave" have been reported in several species. One possible explanation for these deviations would be that individuals do not use only their own breeding performance (i.e., private information) but also that of others (i.e., public information) to decide whether or not to divorce. To test this hypothesis, we investigated the relative importance of private and public information for mate choice decisions in female zebra finches (Taeniopygia guttata).We manipulated the reproductive performance of breeding pairs and measured females' preferences for their mate and the neighbouring male first following pair formation and then seven weeks later when all females had laid eggs and the young were independent. Although all females reduced their preference for their mate after a breeding failure, the decrease was significant only when the neighbouring pair had reproduced successfully. Furthermore, there was no evidence that females biased the sex ratio of their offspring according to their mate's attractiveness. On the other hand, after reproduction, both successful and unsuccessful females increased their preferences for males who had produced a larger proportion of sons. Despite the fact that other mechanisms may have also contributed to our findings, we suggest that females changed their mate preferences based on the proportion of sons produced by successful males, because offspring sex ratio reflects the male's testosterone level at the moment of fertilization and hence is an indicator of his immune condition.     

First experimental evidence for female mate choice in a nocturnal primate

Female mate choice can be hypothesised in most nocturnal primates, since females show a higher investment in their offspring than males. The aim of this experimental study was to investigate if female grey mouse lemurs perform mate choice and whether age, relatedness (to the male), or male advertisement call activity systematically influence their decisions. A two-way mate choice design was developed in which females could choose between two males. Mate choice was deduced from the time spent in proximity to the males and from mating behaviour. During oestrus 12 of 17 females participated actively in the experiment and all of them showed either a significant spatial (n=11) or behavioural (n=1) preference for one male. In four cases copulations were observed. The influence of age on female mate choice was not statistically significant. In the cases with copulations, however, females mostly preferred the older male. This might indicate a preference for older age as an indicator of experience, fitness, and/or status. The influence of relatedness on female mate choice could not be definitely clarified. However, results imply a mechanism of kin recognition on the basis of familiarity. In the majority of choices, females preferred the male with higher trill call activity. Since trill call activity correlates with the relative dominance status of males, these results suggest an importance of the male dominance status for female mate choice in grey mouse lemurs. Altogether our findings indicate that females use a complex of different cues to choose their mates.     

Sexual conflict and the evolution of female mate choice and male social dominance

Conflicts between the sexes over control of reproduction are thought to lead to a cost of sexual selection through the evolution of male traits that manipulate female reproductive physiology and behaviour, and female traits that resist this manipulation. Although studies have begun to document negative fitness effects of sexual conflict, studies showing the expected association between sexual conflict and the specific behavioural mechanisms of sexual selection are lacking. Here we experimentally manipulated the opportunity for sexual conflict in the cockroach. Nauphoeta cinerea and showed that, for this species, odour cues in the social environment influence the behavioural strategies and fitness of males and females during sexual selection. Females provided with the opportunity for discriminating between males but not necessarily mating with preferred males produced fewer male offspring than females mated at random. The number of female offspring produced was not affected, nor was the viability of the offspring. Experimental modification of the composition of the males' pheromone showed that the fecundity effects were caused by exposure to the pheromone component that makes males attractive to females but also makes males less likely to be dominant. Female mate choice therefore carries a demographic cost but functions to avoid male manipulation and aggression. Male-male competition appears to function to circumvent mate choice rather than directly manipulating females, as the mate choice can be cryptic. The dynamic struggle between the sexes for control of mating opportunities and outcomes in N. cinerea therefore reveals a unique role for sexual conflict in the evolution of the behavioural components of sexual selection.     

Distribution of the nuclear receptor for vitamin D in female and male zebra finches,Taeniopygia guttata

In this study, we describe the distribution of high affinity binding sites for 1,25(OH)₂-vitamin D₃ (1,25-D₃) in the zebra finch (Taeniopygia guttata). Four hours following the injection of tritiated 1,25-D₃, binding of the steroid hormone was found primarily in the cell nuclei of a variety of differnt organs. Neurons in numerous discrete regions of the forebrain were labeled. These forebrain regions included the nucleus accumbens, nucleus dorsomedialis posterior thalami, lobus parolfactorius, nucleus septalis lateralis and medialis, nucleus septalis, lamina medullaris dorsalis, nucleus striae terminalis, palaeostriatum augmentatum, and stratum griseum. The choroid plexuses, however, remained clear. Labeled cells were seen in several organs of the alimentary canal, in both the exocrine and the endocrine pancreas, in the proximal tubules of the kidney, in the spleen, in the bursa of Fabricius, and in the heart. The basal cells of the uropygial gland were also labeled. No specific retention was evident in the gonads of either sex. Vitamin D is thus bound by cells in systems with widely different functions. Since several of the labeled tissues are not primarily involved in calcium homeostasis, the data support the concept that vitamin D-soltriol is a steroid hormone that acts as a seasonal neuroendocrine-endocrine regulator and somatotrophic modulator.     

Evolution of the genetic covariance between male and female components of mate recognition: an experimental test

The evolution of a positive genetic correlation between male and female components of mate recognition systems will result as a consequence of assortative mating and, in particular, is central to a number of theories of sexual selection. Although the existence of such genetic correlations has been investigated in a number of taxa, it has yet to be shown that such correlations evolve and whether they may evolve as rapidly as suggested by sexual selection models. In this study, I used a hybridization experiment to disrupt natural mate recognition systems and then observed the subsequent evolutionary dynamics of the genetic correlation between male and female components for 56 generations in hybrids between Drosophila serrata and Drosophila birchii. The genetic correlation between male and female components evolved from 0.388 at generation 5 to 1.017 at generation 37 and then declined to -0.040 after a further 19 generations. These results indicated that the genetic basis of the mate recognition system in the hybrid populations evolved rapidly. The initial rapid increase in the genetic correlation was consistent with the classic assumption that male and female components will coevolve under sexual selection. The subsequent decline in genetic correlation may be attributable to the fixation of major genes, or, alternatively, may be a result of a cyclic evolutionary change in mate recognition.     

Behavioral and hormonal responses of male zebra finches to antiandrogens

After it was shown that the sexual behavioral patterns of male zebra finches are dependent on testosterone, the effects of treatment with two antiandrogens were investigated. The antiandrogens cyproterone (Cy) and cyproterone acetate (CyA) were used in this study. The results show that injections of CyA depress the sexual activity of the birds as measured by the amount of courtship song. The undirected song, too, is negatively influenced by a higher dosage of CyA. With the same dosage of Cy neither of these effects is observed. Radioimmunoassay for plasma testosterone showed that birds treated with CyA had lower, and birds treated with Cy had higher, testosterone levels in comparison with control animals. CyA is described as an antiandrogen with gestagenic side effects while Cy acts as a pure antiandrogen without side effects. Presumably the gestagenic side effects of CyA stop the production of testosterone by negative feedback mechanisms. This negative feedback combined with the antiandrogenic activity seems to account for the effects of CyA on behavior. Cy has no gestagenic side effect but is antiandrogenic with respect to blocking of androgen receptors. The organism tries to compensate for this deficit by increasing the testosterone production. The antiandrogenic activity of Cy probably is neutralized by this stimulated testosterone production.     

Hormonal specificity and activation of sexual behavior in male zebra finches

Castrated zebra finches receiving one of six hormone treatments were given three weekly tests with different females and their sexual behavior was contrasted with that of two control groups consisting of intact or castrated males given implants of cholesterol. The six hormone treatments were: two aromatizable androgens, testosterone (T) and androstenedione (AE); two nonaromatizable androgens, androsterone (AN) and dihydrotestosterone (DHT); an estrogen, estradiol (E); or a combination of E + DHT. Half the males receiving DHT received the 5α-isomer, half received the 5β-isomer. Castration significantly reduced the proportion of males which courted females, total courtship displays, high-intensity courtship displays, beak wiping activity, and significantly increased the latencies to show these behaviors compared to intact males. Castrated males never attempted to mount a female. All of these measures of courtship and copulatory behavior were restored to normal levels only by treatments providing both estrogenic and α-androgenic metabolites (i.e., T, AE, E + αDHT). AE was clearly the most effective of these, raising behavior significantly above normal on several measures. AN treatment was more effective than αDHT on all measures and not significantly different from intact birds on some. Treatment with E, αDHT, βDHT, or E + βDHT was totally ineffective. Surprisingly, females only solicited males whose hormone treatments provided estrogenic metabolites. Not only did they solicit males given aromatizable androgens, which showed high rates of courtship activity, they also solicited males given E or E + βDHT, some of which never even courted. Castration and hormone treatment also affected body and syringeal weight, but in opposite directions. Castration increased body weight while decreasing syringeal weight. Hormone treatments providing α-androgenic metabolites decreased body weight and increased syrinx weight. Treatments supplying estrogen as well were slightly more effective.     

Castration and antisteroid treatment impari vocal learning in male zebra finches

Both song behavior and its neural substrate are hormone sensitive: Castrated adult male zebra finches need replacement of gonadal steroids in order to restore normal levels of song production, and sexsteroids are necessary to establish male-typical neural song-controlcircuits during early development. This pattern of results suggests that hormones may be required for normal development of learned songbehavior, but evidence that steroids are necessary for normal neuraland behavioral development during song learning has been lacking. Weaddressed this question by attempting to eliminate the effects of gonadal steroids in juvenile male zebra finches between the time of initial song production and adulthood. Males were castrated at 20 daysof age and received systemic implants of either an antiandrogen (flutamide). an antiestrogen (tamoxifen), or both drugs. The songs of both flutamide-and tamoxifen-treated birds were extremely disrupted relative to normal controls in terms of the stereotypy and acoustic quality of individual note production, as well as stereotypy of the temporal structure of the song phrase. We did not discern any differences in the pattern of behavioral disruption between birds that were treated with either flutamide, tamoxifen, or a combination of both drugs. Flutamide treatment resulted in a reduced size of two forebrain nuclei that are known to play some role unique to early phases of song learning [lateral magnocellular nucleus of the anterior neostriatum (IMAN) and area X (X)], but did not affect the size of two song-control nuclei that are necessary for normal song productionin adult birds [caudal nucleus of the ventral hyperstriatum (HVc) and robust nucleus of the archistriatum (RA)]. In contrast, treatment with tamoxifen did not result in any changes in the size of song-control nuclei relative to normal controls, and it blocked the effects of flutamide on the neural song-control system in birds that were treated with both drugs. Castration and antisteroid treatment exerted no deleterious effects on the quality of song behavior in adult birds, indicating that gonadal hormones are necessary for the development of normal song behavior during a sensitive period. © 1992 John Wiley & Sons, Inc.