Female control of offspring paternity in a western population of red-winged blackbirds (Agelaius phoeniceus)

Extra-pair copulations, which occur when individuals that have formed social relationships to breed copulate outside their pairbond, now are recognized as an important component of reproductive success in many species. In situations where both males and females benefit from extra-pair copulations without incurring much risk, an inevitable conflict arises between pairbonded mates. In this study I investigated the conflict of interest between male and female reproductive strategies in a western population of red-winged blackbirds (Agelaius phoeniceus). Female red wings in this population initiate extra-pair copulations, which resulted in a 35% rate of extra-pair fertilization. Females initiated the majority (78%) of extra-pair copulations away from their nesting territory where pairbonded individuals typically copulate, and females that engaged in extra-pair copulations spent a significantly greater amount of time off the marsh during peak fertilization compared to females that did not. In addition, females that nested in areas with a large number of potential extra-pair partners produced significantly more extra-pair fertilized young compared to females that nested on marshes with few male neighbors. Males’ strategies to protect paternity were limited primarily to patrolling territory boundaries and to opportunistically preventing extra-pair copulations off the marsh when they were visible. In this population females appear to use behavioral means to control nestling paternity, which in turn directly affected their mate’s reproductive success, and males were restricted to using strategies that were largely ineffective at preventing the threat of extra-pair paternity. Received: 23 December 1994/Accepted after revision: 17 December 1995     

Patterns of courtship behavior and ejaculate characteristics in male red-winged blackbirds

Sperm competition in birds is likely to have important effects on the behavior and physiology of reproduction in both sexes. For males, such competition should select for large sperm reserves and behavioral adjustment of copulation when reserves are low. We investigated both these possibilities in free-living red-winged blackbirds (Agelaius phoeniceus), a highly polygynous species with apparently strong sperm competition. We found that the recent copulatory behavior of males did not affect the propensity to copulate with a model female. Ejaculates collected from individual males at 1-h intervals showed no evidence of sperm depletion, yet repeated ejaculates collected less than 10 min apart did. Male ejaculate size was significantly larger if it was the first one of the day (i.e., after an overnight rest). The average ejaculate size was 12.5 (±12.5 SD) million sperm. Males captured during the breeding season had an average of 111.7 (±52.8) million sperm stored in their seminal glomera. Because males average a peak copulation rate of six per female per day, in one day a male might utilize all the sperm in his seminal glomera if more than two females on his territory are fertilizable. We hypothesize that polygyny and sperm competition in this species have combined to select for rapid replenishment of the seminal glomera throughout the day, in contrast to other species that have been studied. Testis size and sperm reserves of male red-winged blackbirds are intermediate between monogamous species and species with intense sperm competition. Several possible explanations for this are discussed. Received: 21 October 1997 / Accepted after revision: 15 February 1998     

Breeding synchrony and extra-pair mating in red-winged blackbirds

Using data from a 6-year paternity study of red-winged blackbirds, I tested the hypotheses that increased nesting synchrony should either promote extra-pair mating by increasing the advantage of extra-pair mating to females, or decrease extra-pair mating by constraining males from seeking extra-pair copulations. Contrary to these hypotheses, the occurrence of extra-pair paternity did not vary with nesting synchrony over the breeding season, or vary with the number of synchronous nests within territories or within marshes, or with nesting order on territories. However, for nearly all nests with extra-pair young, there were fewer females synchronous with that nest on the cuckolder's territory than on the territory of the cuckolded male. This “advantage” of a synchrony difference was less pronounced for older males that cuckolded younger males, particularly when the two males were not neighbors. Collectively, these results suggest that breeding synchrony affects extra-pair mating by affecting mate guarding, but that breeding synchrony alone can not be used to predict which females are more likely to engage in extra-pair mating, nor with which extra-pair males they will mate. Understanding why extra-pair mating by older males is less affected by breeding synchrony may explain much about both the proximate and ultimate causes of extra-pair mating in red-winged blackbirds. Received: 7 June 1996 / Accepted after revision: 25 November 1996     

Bilateral symmetry and social dominance in captive male red-winged blackbirds

There has been much recent interest in subtle departures from perfect symmetry in bilaterally paired morphological characters, and the extent to which such departures reflect aspects of individual quality. We used data from aviary contests involving pairs of wild-caught male red-winged blackbirds (Agelaius phoeniceus) to test the hypothesis that comparatively symmetrical males are disproportionately successful in intra-sexual competition for food. Although paired contestants showed clear and consistent differences in competitive ability, there was no indication that symmetrical males were competitively superior. Winners and losers of aviary contests were indistinguishable based on asymmetry measures made on each of four bilateral characters (tarsus length, wing chord, and two epaulet dimensions), and for a fifth character (length of outer retrix), asymmetry differences, though significant, occurred in the direction opposite to that predicted. Furthermore, there was no detectable association between male competitive ability and a composite measure that combined asymmetry information across all five characters. Our results, in combination with those of several other recent avian studies, suggest that symmetry is generally a poor predictor of social dominance in birds. This finding is inconsistent with the proposal that symmetry provides a readily obtained, reliable measure of phenotypic quality. Received: 15 May 1997 / Accepted after revision: 26 September 1997     

Experimental assessment of ecological and phenotypic factors affecting male mating success and polyandry in northern watersnakes, Nerodia sipedon

To resolve conflicting field observations regarding the action of sexual selection, we used breeding experiments and paternity analysis of the 927 resulting offspring to assess how male size, condition, tail length, genetic similarity to the female, and variation in operational sex ratio (OSR) affected male reproductive success and the incidence of polyandry in northern watersnakes (Nerodia sipedon). Only size affected male mating success. Large males were more successful, but only when male size varied substantially and competition among males was intense (i.e., male-biased OSR). The conditional nature of the size advantage may explain why studies of free-living watersnakes have produced inconsistent results regarding the relationship between male size and mating success. Size differences between males did not affect the proportion of offspring each male sired within multiply sired litters. We found positive size-assortative mating, but only when the OSR was female biased, suggesting that smaller males had improved access to females when competition among males was reduced, but that competition with larger males still restricted mating opportunities of small males to less preferred, smaller females. Most litters (58%) were multiply sired and larger females were more likely to produce multiply sired litters, similar to free-living watersnakes. There was no association between the incidence of multiple paternity and OSR, however, suggesting that polyandry is not simply a function of opportunity, with females passively waiting for males to court them.     

Polygyny in the red-winged blackbird: do females prefer monogamy or polygamy?

Five hypotheses have been proposed to explain polygyny in the red-winged blackbird (Agelaius phoeniceus). We categorized the hypotheses into three groups based on female preference for unmated versus monogamously mated males: (1) the “polygyny threshold” model, “sexy son” hypothesis and the “asynchronous settlement” model, which assume that females prefer unmated males to mated males on breeding situations of homogeneous quality; (2) the “neutral mate choice” hypothesis, which assumes that females have no preference; and (3) the “cooperative female choice” model, which assumes that females prefer monogamously mated males to unmated males. We tested the direction of female preference in two field experiments. In both experiments, newly settling females were given a choice of two adjacent territories, one defended by an unmated male and the other by a monogamously mated male. Male mating status was randomized with respect to the variation in territory quality and male quality. Early in the breeding season, significantly more females settled with the unmated males than with the mated males. Although more females settled with the unmated males than with the mated males late in the breeding season, the difference was no longer significant. Female settlement late in the season appeared to be related to the tenure of the resident females: the new females avoided territories where the resident females were in early stages of their nesting, but settled on territories where the resident females were in late stages. The pattern of female settlement shows that females prefer unmated males to mated males. The preference is consistent with the polygyny threshold model, sexy son hypothesis and the asynchronous settlement model, and inconsistent with the neutral mate choice hypothesis and the cooperative female choice model. For this reason, the latter two hypotheses are unlikely to explain the occurrence of polygyny in our population of red-winged blackbirds. Received: 1 December 1994 / Accepted after revision: 28 October 1995     

Racketed tail of the male and female turquoise-browed motmot: male but not female tail length correlates with pairing success,performance, and reproductive success

Both males and females of many avian species maintain elaborate plumage traits, and elaborate monomorphic plumage may convey adaptive benefits to one or both sexes as inter- or intraspecific signals. Both sexes of the turquoise-browed motmot (Eumomota superciliosa) are elaborately plumed with long racket-tipped tail. I investigated whether the racketed tail functions as a sexually selected signal in one or both sexes by testing the predictions that males and/or females with the largest tails have: (1) greater pairing success, (2) greater reproductive performance (clutch-initiation date, clutch size, and hatching success), and (3) greater reproductive success. Yearling males with longer denuded rachises (wires) on the central tail feathers had greater pairing success. In addition, adult males with longer wires paired with females who laid larger clutches, had greater hatching success independent of clutch size, and fledged more young. There was no relationship between female tail plumage and pairing success, reproductive performance, or fledgling success. These results are consistent with the hypothesis that male tail plumage functions as a mate choice or status signal, but that the tail of the female does not function in a sexually selected context. I discuss alternative hypotheses for the evolutionary maintenance of the elaborate female tail plumage.     

Alternative mating tactics in the Italian treefrog, <Emphasis Type="Italic">Hyla intermedia</Emphasis>

As in many lekking anurans, Italian treefrog males use two mating tactics: they can attract females by calling vigorously or be satellites, that is, they can remain silent in proximity of a calling male and try to intercept females attracted by their neighbour. We investigated the factors that affected the expression of this mating tactic. Consistent with the conditional mating tactic hypothesis, satellites were smaller than average and smaller than their parasitised calling males. They spent a larger-than-average number of nights at the breeding site, where most of them were also observed calling. Moreover, satellites showed lower call rates and lower mating success than those of males they parasitise but not lower than those of males they did not parasitise. Overall, these results, together with those derived from the analyses of the seasonal and spatial distribution of males, provide evidence for a non-random association between satellites and calling males and are consistent with the hypothesis that satellites have spectral and temporal acoustic preferences that parallel those of females. By adopting the less-successful satellite mating tactic, competitively inferior males can nevertheless maximise their potential reproductive fitness by sexually parasitising the most attractive chorusing males.     

Current analyses do not resolve whether extra-pair paternity is male or female driven

Recent studies question the importance of indirect genetic effects in explaining female benefits of extra-pair matings in socially monogamous species. Compiling data on 14 wild bird species, Arnqvist and Kirkpatrick (Am Nat 165:S26–S37, 2005) estimated the average direct cost in terms or reduced parental care to be an order of magnitude larger than the potential effect of genetic benefits. This study has sparked a debate regarding potential confounding factors but no consensus appears to have been reached. Here we focus on the implicit assumption that all individuals face the same selective pressures and argue that this assumption is probably too strong in most cases. Using a theoretical model we show that when the amount of resources that a male provides depends on territory quality, his physical condition or prospects for alternative breeding opportunities, a female may respond to such differences by altering her mating behaviour. Such confounding factors may lead to direct fitness effects that result in negative correlations between paternal care and paternity even if females that produce extra-pair young experience a net benefit. Negative correlations can also result when males forcefully seek copulations and females resist them. We discuss the studies included in the analysis in this light, and conclude that current analyses on the net selective pressures remain uninformative. In addition to considering average effects across individuals and species we suggest giving attention to individual differences and the influence of ecological factors such as territory quality and predation pressures on female mating behaviour.     

Alternative male mating tactics in a cichlid, Pelvicachromis pulcher: a comparison of reproductive effort and success

Pelvicachromis pulcher is a small African cichlid which breeds in holes. Males may either reproduce monogamously (pair males), polygynously (harem males), or be tolerated as helpers in a harem territory (satellite males). These helpers share in defence of the territory against conspecifics, heterospecific competitors and predators. There are two male colour morphs that are fixed for life and are apparently genetically determined. These differ in their potential mating strategy. Red morph males may become harem owners, while yellow morph males may become satellite males, and males of both morphs may alternatively pair up monogamously. We compared the reproductive effort and success of these three male reproductive strategies. Effort was measured as attack rates, time expenditure and the risk of being injured or killed when attacking competitors or predators of three sympatric fish species. Reproductive success was measured by observing how many eggs were fertilized by each male when this was possible, and by using genetic markers. The number of fry surviving to independence of parental care was used as a criterion of success. The reproductive success of harem males was 3.3 times higher than that of pair males and 7 times higher than that of the average satellite male. Dominant satellite males, however, were as successful as monogamous pair males, using the measure of fertilized eggs. To our knowledge, this has not been found previously in any fish species. Both harem and pair males had lower parental defence costs per sired offspring, however, than males using the alternative satellite tactic. Defence effort was significantly related to the risk of injury. Received: 17 January 1996 / Accepted after revision: 9 June 1997     

Differences in acoustic directionality among vocalizations of the male red-winged blackbird (<Emphasis Type="Italic">Agelaius pheoniceus</Emphasis>) are related to function in communication

Studies of animal acoustic communication have found that the frequency and temporal structure of acoustic signals can be shaped by selection for efficient communication. The directionality of acoustic radiation may also be adapted for communication, but we know relatively little about how directionality varies with signal function, sender morphology, and the environment in which the sound is transmitted. We tested the hypothesis that the directionality of a vocalization is adapted to its function in communication. This hypothesis predicts that vocalizations that are directed to multiple conspecifics (e.g., advertisements and alarms) will be relatively omnidirectional because this will maximize the number of neighbors and mates that receive the signal, and that vocalizations directed to particular individuals will be relatively directional because this will maximize detection of the signal by the targeted receiver and minimize eavesdropping. To test these predictions, we measured the directionality and amplitude of red-winged blackbird (Agelaius pheoniceus) vocalizations in the field by recording vocalizations simultaneously on eight calibrated microphones encircling the bird. We found significant variation in directionality among vocalizations. Supporting our predictions, we found that the most omnidirectional vocalizations were those used to alert conspecifics to danger, and the most directional vocalizations are those used during courtship and solicitation of copulation, when the costs of eavesdropping are likely to be high. These results suggest that the directionality of red-winged blackbird vocalizations is shaped by selection for effective communication. This study is the first to provide statistical support for the hypothesis that directionality is related to the function of a signal in communication.     

Mating system and mating success of the desert spider Agelenopsis aperta

Field studies of the desert spider Agelenopsis aperta revealed a primarily monogamous mating system. However polygyny, polyandry and polygynandry were superimposed upon the primary system, with 9% of the marked males and 11% of the marked females in a field population mating more than once. In the laboratory males commonly mated multiply with fertile offspring resulting, while females were less likely than males to mate multiply. Monogamy under field conditions was enforced by two factors: (1) high travel costs to males, and (2) a significant decline in female receptivity after the first mating. Heavy males were more likely to be accepted by females both in the field, and in female choice experiments conducted in the laboratory. Finally, male weight determined the outcome of male-male agonistic interactions over females. One possible explanation for female choice in this system which lacks male parental investment is that females may be using male size as an indicator of future success of their offspring.     

Correlates of extra-pair fertilization success in hooded warblers

We examined correlates of extra-pair fertilization (EPF) success in the hooded warbler (Wilsonia citrina), a species where females pursue extra-pair matings. The good genes hypothesis predicts that females choose extra-pair mates with morphological or behavioral traits that reflect differences in male genetic quality. EPFs were common, as 35.3% (42/119) of broods contained extra-pair young (EPY) and 26.7% (95/356) of nestlings were the result of EPFs. There was a strong skew in male EPF success which increased the variance in annual male mating success 2–3 fold. However, male morphology did not predict EPF success, as extra-pair males were not older or larger than the males they cuckolded. Likewise, there were no significant correlations between the proportion of extra-pair young in a brood and male size or age. The good genes hypothesis predicts that high-quality males will be consistently preferred as genetic mates, but the number of young sired by a male with his social mate was not consistent from one year to the next. There was a significant negative correlation between female age and proportion of EPY produced, which could result if older females obtain higher-quality social mates. We found no strong evidence that females choose extra-pair mates for good genes, but females may use behavioral rather than morphological cues to assess relative male quality. Received: 31 May 1996 / Accepted after revision: 17 October 1996     

Male genital traits and mating interval affect male fertilization success in the water strider Gerris lacustris

Parker's seminal work brought attention to the possibility of postmating sexual selection by non-random fertilization success. Mechanisms for these processes are still only partly understood and there is clearly a need for more studies of intraspecific variation in sperm precedence. Here, we report results from an experimental study of the variation in fertilization success between males of the water strider Gerris lacustris. Genital morphology, male body size, and copulation duration were examined as possible correlates of paternity. The significance of guarding duration was also analysed. Only male genital morphology was correlated to fertilization success. This is one of the first studies showing a relationship between male genital traits and fertilization success, supporting the view that sexual selection may be responsible for the rapid and divergent evolution of genital structures in animals with internal fertilization. The fertilization success of last males varied considerably after double matings with a short mating interval (10 min). Last-male priority ranged from 0 to 100% and usually one of the males involved fertilized almost all the eggs. After double matings with a short mating interval, the proportion of eggs fertilized by the last male averaged 0.68 and was greater than 0.5. In contrast, the average fertilization success was biased towards the first male when the matings were more spread out over time (24 h). These results do not support earlier suggestions of a widespread last-male sperm priority in water striders. Received: 28 July 1998 / Received in revised form: 15 March 1999 / Accepted: 28 March 1999     

Male reproductive success in free-ranging feral horses

In the social organization of feral horses, adult males compete to monopolize groups or bands of females, sometimes called harems. Alternative male strategies are to remain alone or with other bachelors or, less commonly, to accept subordinate status within a harem. The hypothesis that dominant harem stallion status confers a reproductive advantage was tested in free-ranging feral horses. The presence of foals in harems headed by vasectomized (VSX) versus intact stallions was used to assess the ability of these stallions to control reproduction in their harems. Of harems headed by VSX stallions, 17 and 33% contained foals during years 2 and 3 post-treatment, respectively. In contrast, 86 and 80% of harems headed by non-VSX stallions contained foals in those years. Acquisition of pregnant mares appeared more likely than sneak copulations by bachelor stallions to account for foals in harems with a single stallion. However, most foals were born into harems that included a subordinate stallion, an occurrence that was undoubtedly exacerbated by the extended breeding season resulting from the sterility of the harem stallion. Thus, in comparing alternative reproductive tactics, bachelors appeared less successful than subordinate stallions within a harem. However, the highest reproductive success was achieved by the harem stallion, further demonstrating that alternative tactics are not equally profitable. Received: 13 July 1999 / Received in revised form: 24 July 1999 / Accepted: 24 July 1999     

Analysis of the causal components of assortative mating in water striders

Field studies demonstrate that natural populations of a group of water striders (Heteroptera: Gerridae) that share a common mating system are characterized by weak assortative mating by size and by large sizes of mating males and females relative to single individuals. This study presents an experimental assessment of the components of mating that may contribute to these mating patterns. The effects of male and female body size on each of three components of mating were studied in three water strider species in the laboratory. Large females of all three species mated more frequently, copulated for longer and were guarded longer than small females. Large males mated more frequently than small males in all three species, and also guarded females for longer in the two species where the average of mate guarding was long. However, we found an antagonistic effect of male size on copulation duration: small males copulated for longer than large males in all three species. We show that the combined effects of these size biases mimic the mating patterns found in the wild, e.g. weak and variable assortative mating, and stronger and less variable size ratios of mating versus non-mating females relative to males. We suggest that the antagonistic effects of male size on copulation and guarding duration may be a key source of interpopulational variation in assortative mating and sexual selection on male size. Further, neither spatial or temporal covariation in size, nor mechanical constraints, caused the assortative mating observed here in this group of water striders. Some combination of male and female choice (either active or passive forms) of large mates and male-male exploitation competition for mates play potentially important roles in producing population level assortative mating in water striders. Received: 17 March 1995/Accepted after revision: 28 October 1995     

Search costs influence the spatial distribution,but not the level,of extra-pair mating in tree swallows

Costs of searching for a mate are an important component of models of sexual selection, yet they have rarely been examined in wild populations of vertebrates. In this paper, we report an experiment in which we handicapped female tree swallows by clipping some flight feathers. This manipulation increased the costs of flight and searching for extra-pair mates. Despite these costs, handicapped females had the same level of extra-pair mating (percentage of extra-pair young, percentage of broods with extra-pair young, and the number of extra-pair sires per brood) as control females. However, handicapped females were more likely to have young sired by extra-pair males that lived closer to her nest than control females. This change in the distribution of extra-pair mating was most likely due to female choice rather than male coercion, and it suggests that extra-pair mating has significant benefits to females. One important implication of our study is that ecological and social factors that influence search costs could affect the spatial distribution of extra-pair sires and, consequently, the intensity of sexual selection. These effects may have been overlooked in previous studies that did not identify extra-pair sires.     

Within-brood patterns of paternity and paternal behavior in red-winged blackbirds

We video-taped male and female red-winged blackbirds (Agelaius phoeniceus) feeding individual chicks in order to test the hypothesis that food might be differently allocated to within-pair offspring and extra-pair young. We found no evidence that paternity influenced the allocation of food by either males or females. Both males and females fed male offspring significantly more, but there was no tendency for paternity to be skewed by gender. Females fed older offspring significantly more, whereas males did not; extra-pair fertilizations, however, were not associated with lay or hatch order of the chicks. Given that males do not appear to discriminate within-pair from extra-pair offspring directly, these results are consistent with current theory on the effect of paternity on paternal behavior. We discuss briefly some of the possible reasons why discrimination might be lacking in red-winged blackbirds and in other species in which the possibility of discrimination of paternity and allocation of paternal behavior has been studied.     

Reproductive success of monogamous and polygynous pied flycatchers (Ficedula hypoleuca)

One of the most interesting aspects of the mating system of pied flycatchers is the regular occurrence of polygyny. Here we present data on the reproductive success of polygynously paired pied flycatcher males compared to monogamous males based on paternity analyses through DNA fingerprinting. Males paired with two females suffered a higher loss in reproductive output per female compared to monogamous males due to (1) a greater proportion of unhatched eggs in their broods, (2) greater nestling mortality and (3) a greater probability of being cuckolded. Nevertheless, the number of fledglings was significantly greater for polygynous males. Based on the number of nestlings that returned for subsequent breeding seasons, however, the reproductive success of monogamous and polygynous males did not differ significantly. These data raise the question as to why males attempt polygyny. Received: 16 August 1999 / Received in revised form: 15 March 2000 / Accepted: 18 March 2000     

Display rate by male fairy-wrens (Malurus cyaneus) during the fertile period of females has little influence on extra-pair mate choice

Empirical and theoretical studies have only recently begun to examine how females use complex multi-component displays when selecting mates. Superb fairy-wrens are well suited to the study of female choice because females have control over extra-group paternity and cuckold their mates at high rates, while males possess a variety of sexually selected traits. Available evidence suggests that females base their extra-group mate choice on the timing of male moult into breeding plumage or the onset of display. However, males continue to perform elaborate displays throughout the season, and direct most displays to females during their fertile period. We therefore conducted focal observations on fertile females to quantify the frequency of male display and used microsatellite genotyping to compare the role of display rate during the breeding season and the timing of male moult on female mate choice. We show that the addition of data on male display rate does not improve our ability to predict which males obtain extra-group paternity. The timing of male moult into breeding plumage remains the only predictor of male extra-group reproductive success. Nevertheless, we found that males displayed more to females that were unable to select extra-group mates on the basis of the timing of moult or the onset of display. This raises the possibility that there are circumstances when females use display rate to discriminate between potential extra-group sires. Overall this study supports the theoretical prediction that females are more likely to base their mate choice on reliable indicators of male quality such as fixed morphological traits and displays of endurance, in this case an early moult into breeding plumage and the performance of an elaborate display during the winter, than a flexible behavioural trait such as display rate during the breeding season. Received: 26 January 2000 / Revised: 1 August 2000 / Accepted: 26 August 2000