Mate choice by female white-crowned sparrows in a mixed-dialect population

Summary It has been argued that the song dialects of white-crowned sparrows, Zonotrichia leucophrys, may function to restrict gene flow between dialect populations, thus promoting adaptation to local environmental conditions. One proposed mechanism whereby this may occur is if a female mates preferentially with males singing her natal dialect, typically the song type of her father. Previous field and laboratory studies of the role played by song differences in mate choice by female white-crowned sparrows have produced equivocal results. These investigations were conducted in populations in which a single song dialect was predominant. We examined mate choice in a population in which two song dialects are equally common. We found that songs of mates of individual females in successive years were no more likely to be of the same dialect than expected by chance. In addition, individual females did not mate preferentially with males whose songs matched those of their fathers. We conclude that, in this population, females choose mates on the basis of characteristics other than song type.     

The behavioral response of female Nuttall's White-crowned Sparrows to male song of natal and alien dialects

Summary Female Nuttall's White-crowned Sparrows (Zonotrichia leucophrys nuttalli) were tested in a laboratory experiment to determine their response to stimulation by songs from their natal dialect (Clear) and by songs from three different alien dialects (Fig. 1). The greatest number of copulation solicitation displays and amount of locomotor activity were caused by songs of the subject's natal dialect (Clear); the next most potent stimulus was the contiguously adjacent dialect (Buzzy); the least effective stimuli were songs from a dialect 25 km distant (McClure), representing the same non-migratory subspecies, and a dialect 1,900 km distant (Sand Creek), representing a migratory montane subspecies of White-crowned Sparrow (Figs. 2–4).These results constitute a test of a deduction made from the assortative mating theory and suggest that female White-crowned Sparrows find male song of their natal dialect sexually more stimulating. Thus, speculating about the natural circumstances, females given an unrestricted choice would be expected to mate with males from their natal dialect region.     

Effects of early auditory experience on the development of local song preference in female swamp sparrows

A growing number of studies show that learning about male mating signals can shape the way females discriminate among males and may influence the evolution of both female preferences and the male traits under selection. Female songbirds commonly prefer local songs over foreign songs from a different population. In some species, however, the extent of variation among songs sung by different males within a population is as great as the variation observed between populations, raising the question of how females are able to discriminate local from foreign songs. Here, we report that laboratory-reared female swamp sparrows (Melospiza georgiana) not only show a preference for the particular song types with which they were tutored as compared with both foreign songs and unfamiliar local songs but also show preference for unfamiliar local songs over unfamiliar foreign songs. An acoustic analysis comparing tutor songs and those presented as unfamiliar local and foreign songs suggests that female swamp sparrows might be attuned to the specifics of local note phonology when assessing the attractiveness of unfamiliar songs. Our results demonstrate that early auditory experience influences response to geographic song variation in female swamp sparrows, and suggest the possibility that female songbirds may generalize what they learn from songs early in life to novel songs heard in adulthood. Additional work is needed to evaluate the contribution of unlearned predispositions for local song.     

Female brown-headed cowbirds' (<Emphasis Type="Italic">Molothrus ater</Emphasis>) social assortment changes in response to male song: a potential source of public information

In many species, females' behavior appears to be influenced by that of other females, particularly regarding mate choice. Females theoretically can reduce the costs associated with independent male assessment by observing conspecifics. Studies of brown-headed cowbirds suggest that females pay attention to other females' behavior. Group-housed females modify their song preferences, whereas females housed in pairs do not. What information is available to females in a group environment? To address this question, we studied two groups of juvenile (i.e. hatch-year birds) and adult female cowbirds in a naturalistic group setting. We used a longitudinal ABA design, consecutively introducing and removing males that differed in age, amount of song production and stage of song development, to isolate the male characteristics that related to changes in female behavior. Juvenile and adult females assorted by age class when singing adult males were in the aviary, but not when singing juveniles or silent males of any age class were in the aviary. Results from playback tests confirmed that adult male song alone influenced female age class assortment. Videotape analysis from playback tests revealed that females also wing stroked in response to male song. Other females sometimes approached females who wing stroked and observed them. We hypothesize that group-level changes in social organization and individual females' responses can serve as visual signals for other individuals.     

Female mate choice in the zebra finch — the effect of male beak colour and male song

Studies of female mate preference in zebra finches (Taenopygia guttata) have shown that male beak colour and song rate are important. However, the two characters are correlated. Here the effect of beak colour and song rate on female choice are examined independently. In mate choice tests involving two males, beak colour was manipulated artificially using nail varnish. The results showed that females showed a significant preference for males with a high song rate, but not with a red beak. Females did not prefer males with a red beak if song rate was low and females preferred males with orange beaks who expressed a high song rate. Female preference for males with red beaks was not found when beak and song characters were no longer correlated.     

Phenotypic differentiation in female preference related to geographic variation in male predation risk in the Trinidad guppy (Poecilia reticulata)

Summary Populations of the Trinidad guppy range from areas with high levels of predation by other species of fish to areas with little or no piscine predation. Previous studies have shown that variation among populations in male coloration can be explained by a balance between female preference for brighter males and natural selection against bright males. High levels of male courtship activity may also increase both predation risk and mating success. Therefore, in high-predation areas, females that mate with males that court frequently as well as those that choose bright males would presumably produce male offspring with low survivorship. Consistent with this variation in natural selection, we observed that females from high-predation populations were less likely to choose bright and frequently courting males than females from low-predation populations. This result supports the hypothesis that female preference is evolving as a character genetically correlated with the preferred male character, in which case higher levels of natural selection acting against the male character should be related to lower levels of female preference.     

The efficacy of female choice in chimpanzees of the Taï Forest, Côte d’Ivoire

Male–male competition has historically been considered the major force driving sexual selection. However, female choice and inter-sexual conflict are increasingly recognized as important influences affecting differential mating and reproductive success. Many females exhibit preferences for particular males; however, male strategies may conflict with females’ ability to obtain their mate preferences. To influence paternity, females must affect both (1) whether or not sexual interactions occur, particularly during the periovulatory period (POP) and (2) the outcome of sexual interactions. This study focuses on the effectiveness of female choice in wild chimpanzees (Pan troglodytes verus). Over 2,600 h of data were collected on two habituated chimpanzee communities in the Taï National Park, Côte d’Ivoire. Female mate preferences were measured by quantifying proceptive and resistance behavior toward males in both the periovulatory period and non-POP phases of estrus. The efficacy of female preference was measured both (1) by measuring success rates of female proceptivity and resistance behaviors and (2) by determining how well measures of female mate preference (proceptivity and resistance rates) predict male mating success. Though male chimpanzees are clearly dominant to females, the results indicate that females could effectively resist male solicitations and, in most cases, unwanted copulations were averted. Both female proceptivity and resistance rates correlate (positively and inversely, respectively) with male mating success in POP. Outside POP, female proceptivity rates corresponded with male mating success, but resistance rates did not. Males (irrespective of rank) that were preferred by females obtained higher mating success compared to other males during the POP, suggesting that females were effective in their mate choice and that, despite clear male dominance, female choice influences paternity in wild chimpanzees.     

Asexuals looking for sex: conflict between species and mate-quality recognition in sailfin mollies (Poecilia latipinna)

When two closely related species are sympatric the process of species recognition (identifying conspecifics) and mate-quality recognition (increased fitness benefits) can yield a conflict when heterospecifics resemble high-quality conspecifics. Conflict in species versus mate-quality recognition may serve as a possible mechanism for the persistence of unisexual, gynogenetic Amazon mollies (Poecilia formosa). Amazon mollies require sperm from closely related species (e.g., sailfin mollies, P. latipinna) to start embryogenesis but inheritance is strictly maternal. When choosing mates, male sailfin mollies from populations sympatric with Amazon mollies may rely on traits indicating species identity rather than those indicating mate quality. Conversely, males from allopatric populations may rely more on traits indicating mate quality. Previous work has found that male sailfin mollies in sympatry exhibit a significantly greater mating preference for female sailfin mollies over Amazon mollies compared to males in allopatry. In addition, male sailfin mollies prefer to associate with and produce more sperm in the presence of larger conspecific females, which are more fecund. We hypothesized that male sailfin mollies experience a conflict in species recognition and mate-quality recognition in the presence of Amazon mollies that are relatively larger than female sailfin mollies. To test this hypothesis, we paired males from sympatric and allopatric populations with a larger Amazon molly and a smaller female sailfin molly. We scored the number of mating attempts that males directed to conspecific and heterospecific females. Males in most sympatric and allopatric populations demonstrate no clear preference for conspecifics. In addition, we found some evidence for a difference in mating preference between allopatric and sympatric populations with males from allopatry showing a greater heterospecific mate preference. These results indicate a conflict between species and mate-quality recognition. In sympatry this conflict may contribute to the persistence of gynogenetic Amazon mollies.     

Song sharing correlates with lifetime social pairing success but not territory tenure in the Puget Sound white-crowned sparrow

Imitative song learning in birds often results in the formation of vocal dialects or local song neighborhoods in which males in close proximity share very similar songs. If song sharing confers a selective advantage due to intra-sexual competition or inter-sexual mate choice, song sharing should enhance the singer’s territory tenure or lifetime pairing success. We tested this in a migratory population of the Puget Sound white-crowned sparrow, Zonotrichia leucophrys pugetensis, in which some territory neighbors share whole songs. Song sharing with territory neighbors in the first year on territory did not correlate with territory tenure but correlated positively with social pairing success throughout a male’s lifetime when length of territory tenure was controlled. Thus, song sharing in this migratory population does not appear to confer a benefit in male–male interactions, at least as measured by the length of territory tenure. However, males that share songs do benefit from higher lifetime pairing success. Combined with the data available for other species, it appears that intra- and inter-sexual selection may have stronger effects on song sharing in sedentary and migratory populations, respectively.     

Mate preferences in <Emphasis Type="Italic">Drosophila</Emphasis> infected with <Emphasis Type="Italic">Wolbachia</Emphasis>?

The maternally inherited bacterium Wolbachia pipientis generates strong reproductive incompatibilities between uninfected females and infected males (cytoplasmic incompatibility), significantly reducing both female and male reproductive success. Such fitness costs are thought to place selective pressure on hosts to evolve pre-copulatory preferences for mating with compatible mates, thereby enabling them to avoid the reproductive incompatibilities associated with Wolbachia. Therefore, uninfected females are predicted to prefer mating with uninfected males, whereas infected males are predicted to prefer mating with infected females. Despite these predictions, previous investigations of pre-copulatory mate preferences in Wolbachia-manipulated Drosophila have not found evidence of female preference for uninfected or compatible males. However, none of these studies utilised a design where focal individuals are provided with a simple choice in a relatively non-competitive situation. We examined both female and male pre-copulatory mate preference based on mate infection status in Drosophila simulans and D. melanogaster using simple choice assays involving between 30–50 replicates per treatment. Although we found no evidence of female pre-copulatory mate preferences in either species, male D. simulans exhibited some preference for mating with females of the same infection status. However, this preference was not evident when we repeated the experiment to confirm this finding. Consequently, we conclude that neither male nor female D. melanogaster and D. simulans exhibit significant Wolbachia-associated pre-copulatory mate preferences.     

Body size preferences in the pot-bellied seahorse <Emphasis Type="Italic">Hippocampus abdominalis:</Emphasis> choosy males and indiscriminate females

Male seahorses (genus Hippocampus) provide all post-fertilization parental care, yet despite high levels of paternal investment, these species have long been thought to have conventional sex roles, with female mate choice and male–male competition. Recent studies of the pot-bellied seahorse (Hippocampus abdominalis) have shown that sex-role reversal occurs in high-density female-biased populations, indicating that male mating preferences may lead to sexual selection on females in this species. Egg size, egg number, and offspring size all correlate positively with female body size in Hippocampus, and by choosing large mating partners, male seahorses may increase their reproductive success. While male brood size is also positively correlated with body size, small H. abdominalis males can carry exceptionally large broods, suggesting that the fecundity benefits of female preference for large partners may be limited. We investigated the importance of body size in reproductive decisions of H. abdominalis, presenting focal individuals of both sexes with potential mating partners of different sizes. Mating preferences were quantified in terms of time spent courting each potential partner. Male seahorses were highly active throughout the mate-choice trials and showed a clear behavioral preference for large partners, while females showed significantly lower levels of activity and equivocal mating preferences. The strong male preferences for large females demonstrated here suggest that sexual selection may act strongly on female body size in wild populations of H. abdominalis, consistent with predictions on the importance of female body size for reproductive output in this species. An erratum to this article can be found at     

An experimental investigation of the bioacoustics of cowbird song

Summary Female cowbirds (Molothrus ater ater), maintained in isolation from males during the breeding season, respond to the playback of male song with copulatory postures. They respond to some songs more than to others. Cowbird song potency can thus be operationally defined by the proportion of copulatory postures a song elicits across multiple playbacks. The purpose of the present study was to explore whether song potency changes with distance in the field. No field recordings elicited high levels of responding by the females. When songs of known high potency are systematically degraded, the results indicate that female cowbirds are sensitive to small changes in signal to noise ratio and to atmospheric attenuation. The data suggest that cowbird song potency degrades very rapidly with transmission distance in the field.     

Sex-specific reproductive behaviours and paternity in free-ranging Barbary macaques (Macaca sylvanus)

In a wide variety of species, male reproductive success is determined by contest for access to females. Among multi-male primate groups, however, factors in addition to male competitive ability may also influence paternity outcome, although their exact nature and force is still largely unclear. Here, we have investigated in a group of free-ranging Barbary macaques whether paternity is determined on the pre- or postcopulatory level and how male competitive ability and female direct mate choice during the female fertile phase are related to male reproductive success. Behavioural observations were combined with faecal hormone analysis for timing of the fertile phase (13 cycles, 8 females) and genetic paternity analysis (n = 12). During the fertile phase, complete monopolisation of females did not occur. Females were consorted for only 49% of observation time, and all females had ejaculatory copulations with several males. Thus, in all cases, paternity was determined on the postcopulatory level. More than 80% of infants were sired by high-ranking males, and this reproductive skew was related to both, male competitive ability and female direct mate choice as high-ranking males spent more time in consort with females than low-ranking males, and females solicited copulations mainly from dominant males. As most ejaculatory copulations were female-initiated, female direct mate choice appeared to have the highest impact on male reproductive success. However, female preference was not directly translated into paternity, as fathers were not preferred over non-fathers in terms of solicitation, consortship and mating behaviour. Collectively, our data show that in the Barbary macaque, both sexes significantly influence male mating success, but that sperm of several males generally compete within the female reproductive tract and that therefore paternity is determined by mechanisms operating at the postcopulatory level.     

The effects of male–male contests and female eavesdropping on female mate choice and male mating success in the jumping spider, <Emphasis Type="Italic">Thiania bhamoensis</Emphasis> (Araneae: Salticidae)

In experiments that comprised of three phases (fight, choice, and mating) under “seen” and “unseen” conditions, we examined the effects of the outcomes of male–male contests and female eavesdropping on female mate choice and male mating success in the fighting spider, Thiania bhamoensis (Salticidae). The results revealed female eavesdropping on agonistic interactions. Females that had watched an aggressive interaction showed no distinctive preference for the winner over the loser, but they preferred the loser when they had not observed a fight. Winners, however, achieved a greater mating success than did losers during the mating phase. Gaining access to females was based on the insistence of the winners in courtship in terms of the number of quivers, rather than on the fighting behavior of the males. Hence, the outcome of male–male contests may not be an important determinant of a male’s mating success in T. bhamoensis. Instead, courtship display plays an important role in determining the success of male mating in this species. This study also suggests that female mate preference may not be a good indicator of eventual female mate choice and male mating success. Thus, a causal relationship between female mate preference and male mating success cannot be inferred. Joanna P. Y. Chan, Pei Rong Lau, and Ai Jie Tham contributed equally.     

Operant conditioning and copulation solicitation display assays reveal a stable preference for local song by female swamp sparrows <Emphasis Type="Italic">Melospiza georgiana</Emphasis>

Operant conditioning assays are increasingly being used to test mating signal preferences in female birds. Operant behavior may be seen as farther removed from mate choice behavior as compared to other methods for measuring mating signal preferences, which could limit the evolutionary interpretation of operant results. I compared the song preferences of female swamp sparrows (Melospiza georgiana) as measured both by a copulation solicitation display assay and by an operant preference test. Both methods revealed a strong preference for songs from the females' Conneaut Marsh breeding population over songs from a Millbrook population over 500 km distant, which remained stable after extensive exposure to Millbrook songs. Further, there was a striking congruence in results on an individual level from the two assays. These findings support the conclusion that operant methods reveal evolutionarily significant mate choice preferences, providing the opportunity to study such preferences under circumstances when the copulation solicitation assay is less practical.     

An experimental examination of female preference patterns for components of the male advertisement call in the quacking frog,<Emphasis Type="Italic"> Crinia georgiana</Emphasis>

Even though females prefer particular components of a male display, their preferences may not be expressed during mate choice. Here, we quantified female preference patterns in the frog Crinia georgiana for call rate, pulse number and dominant frequency using two-speaker trials. Females typically chose signals emitted at a higher rate, with more pulses (when variation was extreme) and with an average dominant frequency. The results for pulse number and call rate agree with a previous field study which found that these two call components explained significant variation in male mating success. In contrast, the strong preferences for average dominant frequencies detected here disagree with the previous field study which failed to find any relationship between dominant frequency and male mating success. To explain the discrepancy we investigated whether the patterns of female preference for dominant frequency changed when another property, call rate, was varied simultaneously. Most females chose the call with an average dominant frequency when offered a choice between a call with an average dominant frequency and call rate or a non-average dominant frequency (±2 SD) and high call rate. When the differences in dominant frequency were reduced (±1 SD), females showed no clear preference for either signal. Accordingly, female preference patterns for one call component can vary with the expression of another. These results do not explain why dominant frequency did not account for any variation in male mating success under field conditions.Communicated by T. Beschlitz     

Repeatable female preferences, mating order and mating success in the poeciliid fish, Heterandria formosa

Sexual selection via female choice can afford preferred males comparably higher mating success than those males that lack preferred traits. In addition, many models of sexual selection assume that both male traits and female preferences are heritable. In this study we test whether females of the poeciliid fish, Heterandria formosa, have repeatable pre-copulatory preferences for larger males. We also test whether female pre-copulatory preferences are always reliable indicators of male mating success. When given a choice between a large and a small male, females prefer larger males, and the repeatability of this preference is high. Although there are no overall differences in male mating success between large and small males, large males have a higher mating success when they are the first to mate than when they are the second to mate. Likewise, preferred males also have higher mating success when they are the first to mate than when they mate second. Therefore, the repeatable female preferences observed in this study only predict male mating success when the preferred male mates first. These results illustrate that even significantly repeatable female preferences do not translate into male mating success, which is an assumption of many examinations of the importance of female choice in sexual selection.     

Developmental stress affects the attractiveness of male song and female choice in the zebra finch (Taeniopygia guttata)

Developmental stress has recently been shown to have adverse effects upon adult male song structure in birds, which may well act as an honest signal of male quality to discriminating females. However, it still remains to be shown if females can discriminate between the songs of stressed and non-stressed males. Here we use a novel experimental design using an active choice paradigm to investigate preferences in captive female zebra finches (Taeniopygia guttata). Nine females were exposed to ten pairs of songs by previously stressed and non-stressed birds that had learned their song from the same tutor. Song pairs differed significantly in terms of song complexity, with songs of stressed males exhibiting lower numbers of syllables and fewer different syllables in a phrase. Song rate and peak frequency did not differ between stressed and non-stressed males. Females showed a significant preference for non-stressed songs in terms of directed perching activity and time spent on perches. Our results therefore indicate that developmental stress affects not only the structure of male song, but that such structural differences are biologically relevant to female mate choice decisions.     

Dissecting the mechanisms underlying old male mating advantage in a butterfly

Selection is expected to maximize an individual’s own genetic reward regardless of the potential fitness consequences for its sexual partners, which may cause sexual conflict. Although performance in holometabolous insects typically diminishes with age, old male mating advantage has been documented in a few species. Whether this pattern arises from female preference for older males based on, e.g., pheromone blends (intersexual selection), or from increased eagerness to mate in older compared to younger males is currently debated. We explore the mechanistic basis of old male mating advantage, using a series of experiments including behavioral as well as manipulative approaches, in the tropical butterfly Bicyclus anynana. Consistent with the residual reproductive value hypothesis, old male mating advantage was associated with a greater eagerness to mate, evidenced by a two times higher flying and courting activity in older than in younger males. In contrast, we found only limited support for a contribution of female preference for older males based on pheromone composition, although male sex pheromones clearly do play a role in mating success. Our results suggest that male behavior may play a primary role in old male mating advantage, and that pheromones are likely of secondary importance only. Male mating success was related to higher overall pheromone titers rather than variation in a single component. A dominant importance of male behavior in determining mating success may result in sexual conflict.     

Indirect fitness benefits are not related to male dominance in a killifish

Recent theoretical and empirical studies have shown that male dominance is often at odds with female mate preference and that indirect (genetic) benefits of mate choice may not be related to male dominance. We tested whether female preference corresponded to male dominance and whether mating with dominant males conveyed benefits to offspring fitness in a small freshwater fish, the African annual killifish Nothobranchius korthausae (Cyprinodontiformes), a species without parental care. The experimental design used controlled for the effect of male age, possibility of sperm and egg depletion, and accounted for a potential that females express their preference through maternal effects by manipulation of egg mass during ovulation. By sequentially mating females with males of known dominance, we found that female N. korthausae showed no mate preference in terms of egg numbers deposited with respect to male dominance or body size and no congruent mate preference to specific males was detected. However, males sired offspring with consistently higher hatching success and the effect was repeatable across individual females. Thus, some males provided females with indirect benefits related to additive genetic quality (“good genes”) and expressed via increased hatching rate, but this benefit was not related to male dominance status or body size.