Subordinate superb fairy-wrens (Malurus cyaneus) parasitize the reproductive success of attractive dominant males

Explanations of cooperative breeding have largely focused on the indirect benefits philopatric offspring gain from investing in kin. However, recent molecular studies have revealed that in many species subordinates provision unrelated offspring. This has led to the re-evaluation of the direct and indirect benefits of helping behaviour. In this study, we used microsatellite genotyping to assess the extra-group reproductive success of subordinate superb fairy-wrens (Malurus cyaneus), a species with extremely high rates of extra-group paternity. Extra-group subordinate males sired 10.2% (193 out of 1895) of all offspring sampled between 1993 and 2000 and 21.4% (193 out of 901) of all illegitimate offspring sired by known males. The extra-group success of subordinates was greatly influenced by the attractiveness of their dominant male. Subordinates of attractive dominants sired more extra-group young than did average dominants. Evidence suggests that mate choice in superb fairy-wrens is error-prone and subordinates can gain direct reproductive benefits through parasitizing the reproductive success of attractive dominants.     

Do Female Red-winged Blackbirds Engage in a Mixed Mating Strategy?

Parentage analyses of broods of nestling red-winged blackbirds (Agelaius phoeniceus) revealed that extra-pair fertilizations (EPFs) accounted for 24% of the offspring. 8% of attempted copulations and 13% of male courtship displays during observations of focal females were by extra-pair males. In addition, mates and non-mates often chased and occasionally made physical contact with females; 34% of those chases in which contact was made were extra-pair chases. Females behaved variably during both within-pair and extra-pair events; females crouched less and resisted more frequently during extra-pair courtship than during within-pair courtship. All extra-pair events, whether natural or induced by male removal, were either resisted or accepted by the female. In 318 focal female-hours of observation during the fertilizable period, no female was ever seen in another male's territory soliciting a copulation. In addition, removal of females' mates resulted in frequent extra-pair courtship and copulation; all of these occurred on the removed male's territory. Some females left their mates' territories on occasion — these forays were nearly always off the study area, no female was ever seen copulating with an extra-pair male while on these forays, and neither the frequency nor the duration of female forays correlated with the frequency of extra-pair fertilizations within broods. There were no associations between extra-pair fertilizations and female age, settlement order, nest order, or clutch size. The number of fledglings produced from a nest was significantly positively associated with the number of sires of the brood. Fewer offspring apparently starved in broods that were multiply sired, yet males did not provide courtship feedings during either within-pair or extra-pair copulations, nor was any paternal care provided to young sired through extra-pair matings. The frequency of infertile eggs was low (< 1%); in those instances of infertile eggs the territory owner sired some young in the same nest or another nest on his territory. Fewer broods were a mixture of within-pair and extra-pair paternity than expected by chance. Clear evidence implicating a mixed strategy on the part of females could not be gathered. Because females behaved variably and because not all costs and benefits to females of extra-pair copulations could be measured, it remains possible that female behavior patterns are either (1) part of a mixed strategy, or (2) part of a strategy minimizing the costs of copulation.     

Does male extra‐territory foray effort affect fertilization success in hooded warblers Wilsonia citrina?

Hooded warbler Wilsonia citrina males vary greatly in the frequency and duration of their off-territory forays in search of extra-pair copulations. We used radiotracking and microsatellite parentage analysis in high and low density populations to determine if (1) high foray rate or time off-territory reduces within-pair fertilization success, and (2) if a high foray rate onto the territory of a fertile female increases the likelihood of obtaining EPFs with that female. Males who left their territory often, or for longer periods, did not have lower within-pair fertilization success. Some males repeatedly visited a neighboring fertile female, but in only 3 of 19 cases where radiotagged males visited a fertile female did the male actually sire offspring with that female. Male foray rate onto a fertile female's territory was not a good predictor of whether or not he sired extra-pair offspring with that female. We suggest that mate choice and extra-pair behavior by females may explain why male foray behavior does not correspond closely with actual fertilization success.     

Strategic promiscuity helps avoid inbreeding at multiple levels in a cooperative breeder where both sexes are philopatric

In cooperative breeders, the tension between the opposing forces of kin selection and kin competition is at its most severe. Although philopatry facilitates kin selection, it also increases the risk of inbreeding. When dispersal is limited, extra-pair paternity might be an important mechanism to avoid inbreeding, but evidence for this is equivocal. The red-winged fairy-wren is part of a genus of cooperative breeders with extreme levels of promiscuity and male philopatry, but is unique in that females are also strongly philopatric. Here, we test the hypothesis that promiscuity is an important inbreeding avoidance mechanism when both sexes are philopatric. Levels of extra-pair paternity were substantial (70% of broods), but did not arise through females mating with their helpers, but via extra-group mating. Offspring were more likely to be sired by extra-pair males when the social pair was closely related, and these extra-pair males were genetically less similar to the female than the social male and thus, inbreeding is avoided through extra-pair mating. Females were consistent in their choice of the extra-pair sire over time and preferred early moulting males. Despite neighbouring males often being close kin, they sired 37% of extra-pair offspring. However, females that gained paternity from neighbours were typically less related to them than females that gained paternity further away. Our study is the first to suggest that mating with both closely related social partners and neighbours is avoided. Such sophistication in inbreeding avoidance strategies is remarkable, as the extreme levels of promiscuity imply that social context may provide little cue to relatedness.     

Do male paternity guards ensure female fidelity in a duetting fairy-wren?

Most socially monogamous bird species engage in extra-pair mating,and consequently males may adopt various behavioral strategiesto guard paternity. However, the relationship between mate guardingand extra-pair paternity is unclear: low levels of extra-pairpaternity can be associated either with no mate guarding orwith intense mate guarding. We investigate paternity guardsin the purple-crowned fairy-wren (Malurus coronatus), a duettingspecies where extra-pair paternity is rare. This species isunusual in a genus known for extremely high levels of extra-pairmating. We examine the behavioral interactions between the sexesunderlying these low rates of extra-pair paternity and showthat male purple-crowned fairy-wrens do not use frequent copulationor courtship feeding to assure paternity or guard females acousticallyby duetting. Males maintain close proximity to females bothwhen they are fertile and when they are not breeding and donot invest in courtship displays to extra-pair females. Consistentwith predictions of theoretical models, low extra-pair paternityin this species may be related to female fidelity rather thanmale paternity assurance strategies, but short-term removalof males would be necessary to test this experimentally.     

Extra-pair young in house wren broods are more likely to be male than female

Sex-allocation theory predicts that females should preferentially produce offspring of the sex with greater fitness potential. In socially monogamous animal species, extra-pair mating often increases the variance in fitness of sons relative to daughters. Thus, in situations where offspring sired by a female''s extra-pair mate(s) will typically have greater fitness potential than offspring sired by the within-pair mate, sex-allocation theory predicts that females will bias the sex of offspring sired by extra-pair mates towards male. We examined the relationship between offspring sex and paternity over six breeding seasons in an Illinois population of the house wren (Troglodytes aedon), a cavity-nesting songbird. Out of the 2345 nestlings that had both sex and paternity assigned, 350 (15%) were sired by extra-pair males. The sex ratio of extra-pair offspring, 0.534, was significantly greater than the sex ratio of within-pair offspring, 0.492, representing an increase of 8.5 per cent in the proportion of sons produced. To our knowledge, this is the first confirmed report of female birds increasing their production of sons in association with extra-pair fertilization. Our results are consistent with the oft-mentioned hypothesis that females engage in extra-pair mating to increase offspring quality.     

Male extraterritorial forays, age and paternity in the socially monogamous reed bunting (Emberiza schoeniclus)

Genetic studies have shown that extra-pair paternity is widespread among socially monogamous bird species. Yet, the role of males and females and their behavior leading to this mixed reproductive strategy is poorly understood. Here, we analyze paternity in relation to male age and mating behavior in the socially monogamous reed bunting (Emberiza schoeniclus). We report a positive relation between male extraterritorial forays and success in obtaining extra-pair fertilizations. Extraterritorial forays tended to increase in frequency with male age and older males sired a larger number of extra-pair offspring than young males. Identified extra-pair sires were old in nine out of ten cases. The likelihood of being cuckolded was not affected by male age. Although based on correlative data, our results highlight age-dependent explorative male behavior as a key determinant for the understanding of extra-pair mating in the reed bunting. We do, however, emphasize the need for further studies to reveal the role of females in extra-pair copulations and fertilizations.     

Demography of male reproductive queues in cooperatively breeding superb fairy-wrens Malurus cyaneus

1. Subordinate helpers in cooperative societies may gain both immediate and future benefits, including paternity and territorial inheritance. However, if such opportunities correlate with rank in the queue, it is unclear why such queues should be stable. 2. In cooperatively breeding superb fairy-wrens Malurus cyaneus, only males are generally philopatric, and form stable hierarchical queues for the dominant position. 3. Male opportunities for reproduction are influenced both by their dominance status within the group, and their relatedness to the breeding female. For young queuing subordinates, the breeding female is typically their mother. Because of incest avoidance, reproduction is possible only through extra-group mating, even if the dominant position is achieved while the mother is still on the territory. If the mother dies while the helper is still a subordinate, he can seek matings both outside the group, and with the unrelated replacement female within the group. Finally, males can achieve the dominant position and pair with an unrelated female by inheritance, dispersal to a neighbouring vacancy, or by forming a liaison with an immigrant subordinate female that causes fission of the natal territory. 4. On average males spent more time living with unrelated females than with their mother. Subordinate males gained no survival advantages when living with their mother rather than an unrelated female, contrary to the prediction that parents facilitate the survival of their offspring. 5. Dominants and subordinates also had similar survival. Mortality accelerated over time, probably because older males invest more in extra-group courtship display. 6. Fairy-wren queues are likely to be stable because older birds are superior, and because extra-pair mating provides direct benefits to subordinates.     

Extra-pair paternity as the result of reproductive transactions between paired mates

Transactional ('optimal skew' or concessions') models of social evolution emphasize that dominant members of society can be favoured for donating parcels of reproduction to same-sexed subordinates in return for cooperation by the latter. We developed a mathematically similar model in which extra-pair paternity in broods receiving biparental care is viewed as emerging from a reproductive transaction between the paired mates. The model quantitatively predicted the maximum paternity that a male mate can demand before its female mate is favoured to break the pair bond and caring solitarily for a brood sired entirely by a neighbouring male. The model predicts that extra-pair paternity results when the neighbouring male is of sufficiently higher quality than the male mate. In such cases, the exact amount of extra-pair paternity will vary directly with the difference in quality between the two males and inversely with the value (fitness impact) of the male mate's parental care. Importantly, the transactional model provided a unified explanation for experimental and observational evidence that extra-pair paternity rises with decreasing quality of the male mate, increasing genetic variability among breeding males, increasing breeding density, increasing availability of food and decreasing involvement of the male mate in parental care.     

Are there correlates of male Australian Magpie Gymnorhina tibicen reproductive success in a population with high rates of extra‐group paternity?

The reproductive success of a male bird is often correlated with measurable traits that predict his intrinsic quality. Females are thought to base their selection of mates on the latter's 'quality' in order to gain their 'good genes'. Male Australian Magpies Gymnorhina tibicen of the white-backed race tyrannica were trapped in two breeding seasons. Measurements were taken of morphometric and other characteristics in order to discover whether particular traits of males were associated with: (1) percentage of offspring sired in the territory, (2) number of fledglings produced in the territory per season and (3) whether females select males for their 'good genes'. There were no consistently significant correlations between any of the measured variables and male Magpie reproductive success within territories. In particular, none of the traits measured had any consistent correlation with the percentage of offspring sired in a territorial group. This was an unexpected result given that the species is strongly territorial but also engages regularly in extra-group copulations. These findings appear contrary to the predictions of the 'good genes' hypothesis. The general lack of correlation between the variables and level of genetic paternity may in fact be due to females engaging in extra-group mating primarily to avoid breeding with a close relative rather than to choose a high-quality male. In this case, males would not have to be 'high quality', but merely genetically different from the female's social mate.     

Experimentally Simulating Paternity Uncertainty: Immediate and Long-Term Responses of Male and Female Reed Warblers Acrocephalus scirpaceus

In many socially monogamous species, both sexes seek copulation outside the pair bond in order to increase their reproductive success. In response, males adopt counter-strategies to combat the risk of losing paternity. However, no study so far has tried to experimentally prove the function of behaviour for paternity assurance. Introducing a potential extra-pair partner during the female fertile period provides a standardised method to examine how pair members respond immediately (e.g. increase mate guarding or copulation frequency) or long term (e.g. later parental investment and paternity uncertainty). In this study on a socially monogamous passerine species, we experimentally confronted pairs of reed warblers with a conspecific male (caged male simulating an intruder) during egg-laying. Our results revealed that occurrence of an intruder during that period triggered aggression against the intruder, depending on the presence of the female. The male territory owner also attacked the female partner to drive her away from the intruder. Thus territory defence in reed warblers also serves to protect paternity. The increase in paternity uncertainty did not affect later paternal investment. Paternal investment was also independent of the actual paternity losses. In females, the experiment elicited both, immediate and long-term responses. E.g. female copulation solicitations during the intruder experiment were only observed for females which later turned out to have extra-pair chicks in their nest. In relation to long term response females faced with an intruder invested later less in offspring feeding, and had less extra-pair chicks in their nests. Extra-pair paternity also seems to be affected by female quality (body size). In conclusion female reed warblers seem to seek extra-pair fertilizations but we could demonstrate that males adopt paternity assurance tactics which seems to efficiently help them to reduce paternity uncertainty.     

EXTRAPAIR MATE CHOICE AND HONEST SIGNALING IN COOPERATIVELY BREEDING SUPERB FAIRY-WRENS

In many species of monogamous birds females copulate with males other than their social mates, resulting in extrapair fertilizations. Little is known about how females choose extrapair mates and whether the traits used to choose them are reliable indicators of male quality. Here we identify a novel male trait associated with extra-group mating success in the superb fairy-wren (Malurus cyaneus), a cooperatively breeding bird with one of the highest known frequencies of extra-group mating. Female fairy-wrens chose extra-group mates that molted earlier into breeding plumage. Males molted up to five months before the breeding season began, and only males that molted at least one month prior to its onset gained any extra-group fertilizations. This conclusion held after controlling statistically for the effect of age and social status on molt date. Once males acquired breeding plumage, they began courtship display to females on other territories. Thus, some males were displaying to females for several months before the breeding season began. This extraordinarily long period of advertisement by males may be facilitated by the long-term ownership of territories. We suggest that early acquisition of breeding plumage or the subsequent display behavior can be reliable cues for mate choice because they are costly to acquire or maintain.     

Yearling male great tits, Parus major, suffer more strongly from cuckoldry than older males

In the majority of socially monogamous bird species, females have offspring sired by males other than their social mate as the result of extra-pair copulations. While it is widely recognised that there is considerable variation in the frequency of extra-pair paternity between species, between populations of a species and between individuals of a population, determinants of this variation are surprisingly difficult to establish. With respect to individual variation within a population, it is an important step to test for male and female correlates of cuckoldry to better understand the patterns as well as the adaptive significance of extra-pair mating behaviour. Here, we analysed patterns of extra-pair paternity in relation to male age, female age and their interaction in the great tit Parus major, a socially monogamous passerine with a moderate frequency of extra-pair paternity. Based on a large sample of 316 genotyped first broods from five successive years, we failed to demonstrate interaction effects of male and female age on both the proportion of extra-pair offspring and the likelihood that at least one extra-pair offspring is present within a brood. However, both the proportion of extra-pair offspring and the likelihood of paternity loss were higher for yearling as compared to older males, while this was not the case for yearling vs. older females. Furthermore, the proportion of extra-pair offspring within a brood decreased with increasing age of the attending male in within-individual analyses. We found a comparable effect also for attending females in within-individual analyses, but only when excluding two individuals with 100% extra-pair paternity. A female (extra-pair) mating preference for older males and/or a limited ability of yearling males to prevent cuckoldry in their broods could explain these age-related patterns of paternity loss. Effect sizes, however, were not particularly large and substantial residual variation within age categories suggests the importance of further yet unidentified determinants of variation in paternity loss in the study population.     

Extra-pair paternity and song characteristics in the willow warbler Phylloscopus trochilus

Complexity in bird song is often argued to be advantageous in processes of sexual selection, and numerous studies show that characteristics of song are associated with increased success in territory defence or mate attraction. Less evidence exists on the relationship between bird song characteristics and patterns of extra-pair paternity. We tested whether males that suffered from extra-pair paternity differed in song characteristics from males with no extra pair paternity in the willow warbler Phylloscopus trochilus . In the Scottish population that we studied, we found that 23.5% of young were not related to the social father, and that 47% of nests contained at least one extra pair young. Older males were less likely to suffer paternity loss. While song repertoire size was not related to loss of paternity, males with short songs suffered higher paternity loss than males with long songs. Although arrival date is a good correlate of social mate choice in this population, it was not related to extra-pair paternity. These results suggest that females use song length, or a trait correlated with this song characteristic, as a cue for choosing extra-pair partners in this species, or alternatively that variance in the success of mate guarding or female coercion is related to this song variable.     

Multiple Paternity in Polyandrous Barn Owls (Tyto alba)

In polyandrous species females produce successive clutches with several males. Female barn owls (Tyto alba) often desert their offspring and mate to produce a 2^nd annual brood with a second male. We tested whether copulating during chick rearing at the 1^st annual brood increases the male''s likelihood to obtain paternity at the 2^nd annual breeding attempt of his female mate in case she deserts their brood to produce a second brood with a different male. Using molecular paternity analyses we found that 2 out of 26 (8%) second annual broods of deserting females contained in total 6 extra-pair young out of 15 nestlings. These young were all sired by the male with whom the female had produced the 1^st annual brood. In contrast, none of the 49 1^st annual breeding attempts (219 offspring) and of the 20 2^nd annual breeding attempts (93 offspring) of non-deserting females contained extra-pair young. We suggest that female desertion can select male counter-strategies to increase paternity and hence individual fitness. Alternatively, females may copulate with the 1^st male to derive genetic benefits, since he is usually of higher quality than the 2^nd male which is commonly a yearling individual.     

Factors influencing mate guarding and territory defence in the stitchbird (hihi)

Socially monogamous male birds are predicted to maximise their reproductive success by pursuing extra-pair copulations (EPCs) while engaging in anti-cuckoldry behaviour such as mate guarding. In the stitchbird, Notiomystis cincta, high levels of forced EPCs and a high proportion of nestlings resulting from extra- pair fertilisations lead to the prediction that males of this species should exhibit intense paternity guarding behaviours. While studying an isolated stitchbird population on Tiritiri Matangi Island New Zealand (3636'S, 17453'E), I collected daily behavioural data throughout the breeding season from 15 males in 2000/01 and 27 males in 2001/02. In this study, male stitchbirds demonstrated clear paternity guarding by exhibiting: (1) an increased likelihood of being close to their mate during her fertile period, (2) an increased initiation of mate contact during her fertile period, (3) switching from site-specific territorial defence during the pre-fertile period to defending an area centring on the their female partners location during her fertile period, and (4) an increased following of the female to communal feeding sites outside the territory during her fertile period. For polygynous males, mate guarding and territorial defence were conditional on which of their females was fertile. Additional evidence supporting the hypothesis that mate guarding in this species is a form of paternity assurance, rather than protection from harassment, is that males protected their partner from harassment by other stitchbird males but did not intervene when females were harassed by male bellbirds, Anthornis melanura. While mate-guarding intensity in many species is conditional on the stage of female fertility, male stitchbirds also modified their behaviour depending on the location of the female and the rate of intrusions by extra-pair males. Resident males adopted a best-of-a-bad-job tactic when they were unable to locate their female by defending an area around her last known location. Furthermore, when the rate of intrusions by extra-pair males increased they traded-off the area they could defend within their territory against their ability to guard the female. Territory takeovers were uncommon, but when they did occur older males displaced younger males and healthy birds displaced sick ones. Contrary to the prevailing view that mate guarding is a male response to female infidelity, male stitchbirds appear to use mate guarding primarily to prevent paternity losses from forced EPCs. Future assessments of mate guarding function should consider the possibility that mate guarding involves a combination of conflict and co-operation between the sexes.     

Breaking the rules: sex roles and genetic mating system of the pheasant coucal

Generally in birds, the classic sex roles of male competition and female choice result in females providing most offspring care while males face uncertain parentage. In less than 5% of species, however, reversed courtship sex roles lead to predominantly male care and low extra-pair paternity. These role-reversed species usually have reversed sexual size dimorphism and polyandry, confirming that sexual selection acts most strongly on the sex with the smaller parental investment and accordingly higher potential reproductive rate. We used parentage analyses and observations from three field seasons to establish the social and genetic mating system of pheasant coucals, Centropus phasianinus, a tropical nesting cuckoo, where males are much smaller than females and provide most parental care. Pheasant coucals are socially monogamous and in this study males produced about 80% of calls in the dawn chorus, implying greater male sexual competition. Despite the substantial male investments, extra-pair paternity was unusually high for a socially monogamous, duetting species. Using two or more mismatches to determine extra-pair parentage, we found that 11 of 59 young (18.6%) in 10 of 21 broods (47.6%) were not sired by their putative father. Male incubation, starting early in the laying sequence, may give the female opportunity and reason to seek these extra-pair copulations. Monogamy, rather than the polyandry and sex-role reversal typical of its congener, C. grillii, may be the result of the large territory size, which could prevent females from monopolising multiple males. The pheasant coucal’s exceptional combination of classic sex-roles and male-biased care for extra-pair young is hard to reconcile with current sexual selection theory, but may represent an intermediate stage in the evolution of polyandry or an evolutionary remnant of polyandry.     

Female mate choice in relation to heterozygosity in Tribolium castaneum

Abstract Female mate choice, both before and after copulation, is pervasive among insect species. It is often hypothesized that females would preferentially mate with males that are genetically dissimilar to promote the genetic variability of the offspring. We used various strains of red flour beetle, Tribolium castaneum, and tested the effect of male and female genetic backgrounds on precopulatory and post‐copulatory female mate choice. Simultaneous mate choice experiments using previously well established pheromone assays did not detect female preference for males of different strains. Post‐copulatory female mate choice was examined through paternity analysis. Two parameters were used to measure post‐copulatory female mate choice, including male defence capacity (P₁, proportion of offspring sired by the first male when a female mated with two males consecutively) and offence capacity (P₂, proportion of offspring sired by the second of two males to mate with a female). When female and male beetle strains were same, defence capacity was significantly higher than when female and male strains were different. However, such a pattern was not observed for offence capacity. The results suggest that female precopulatory mate choice is not affected by genetic background, but the outcome of post‐copulatory processes depends on the genetic background of male and female beetles.     

Swingin' in the rain: condition dependence and sexual selection in a capricious world

Signals used in mate attraction are predicted to be highly condition dependent, and thus should be sensitive to environmental contributions to condition. However, the effects of temporal fluctuations in the environment on sexual selection in long-lived animals have been largely ignored. Female superb fairy-wrens, Malurus cyaneus, use the time that males moult into nuptial plumage prior to the onset of the breeding season to distinguish between the extra-group sires that dominate paternity. Although moult varies predictably with age, and shows marked differences between males, the phenotypic distribution also changes radically with climate; so after dry summers few males can attempt early moult. We use the recently introduced de-lifing technique to examine sexual selection gradients over 15 years of selection. Overall, there was strong evidence of directional sexual selection for early moult. However, sexual selection was much stronger when the conditions were favourable (rainfall was high), and selection was undetectable in some years. The contribution of early moulting males to population growth increased when many males moulted early, decreased when early moulting males suffered disproportionate mortality and decreased when females lacked subordinate helpers, forcing them to cede paternity to their social partner. These data suggest that short-term and laboratory studies of mate choice and sexual selection may misrepresent or underestimate the complexity of the sexual selection landscape.     

Relatedness,body size and paternity in the alpine newt,Triturus alpestris

Sexual selection has traditionally been investigated assuming that male quality is as skewed as patterns of male reproductive success can sometimes be. Recently, female choice has been investigated under the model of genetic compatibility, which assumes that each individual female has her own 'best' mate and there is no overall optimal choice for all females. We investigated female mate choice in the newt species Triturus alpestris, a member of a genus where female choice has been investigated only within the context of the optimal male (female choice for condition-dependent traits). We provided females with two males that differed in one condition-dependent trait (body size) and overall genetic composition. Both male body size and female body size did not influence paternity, but the degree of genetic relatedness between females and potential mates did. Two components of fitness (fecundity and hatching success) did not differ between singly and multiply sired clutches, indicating that females do not employ polyandry as a means of increasing offspring fitness through genetic bet-hedging. Instead, we hypothesize that females may mate initially for fertility assurance, but prefer less-related males as the most genetically compatible mates.