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.     

Paternity analysis reveals opposing selection pressures on crown coloration in the blue tit (Parus caeruleus)

In socially monogamous species, extra-pair paternity can increase the variance in reproductive success and thereby the potential for sexual selection on male ornaments. We studied whether male secondary sexual ornaments are selected through within- and/or extra-pair reproductive success in the blue tit (Parus caeruleus). Male blue tits display a bright blue crown plumage, which reflects substantially in the ultraviolet (UV) and previously has been indicated to be an important sexual signal. We show that males with a more UV-shifted crown hue were less cuckolded, which probably resulted from female preference for more ornamented mates. By contrast, however, older males and males with a less UV-shifted hue sired more extra-pair young. This probably did not reflect direct female preference, since cuckolders were not less UV-ornamented than the males they cuckolded. Alternatively, a trade-off between UV ornamentation and other traits that enhance extra-pair success could explain this pattern. Our results might reflect two alternative male mating tactics, where more UV-ornamented males maximize within-pair success and less UV-ornamented males maximize extra-pair success. Since crown colour was selected in opposite directions by within-pair and extra-pair paternity, directional selection through extra-pair matings seemed weak, at least in this population and breeding season. Reduced intensity of sexual selection due to alternative mating tactics constitutes a potential mechanism maintaining additive genetic variance of male ornaments.     

Extra-pair paternity in the socially monogamous mountain bluebird Sialia currucoides and its effect on the potential for sexual selection

Sexual selection theory posits that ornamental traits can evolve if they provide individuals with an advantage in securing multiple mates. That male ornamentation occurs in many bird species in which males pair with a single female is therefore puzzling. It has been proposed that extra-pair mating can substantially increase the variance in reproductive success among males in monogamous species, thus increasing the potential for sexual selection. We documented the frequency of extra-pair paternity and examined its effect on variation in male reproductive success in the mountain bluebird Sialia currucoides , a socially monogamous songbird in which males possess brilliant plumage ornamentation. Extra-pair paternity was common in our Wyoming study population, with 72% of broods containing at least one extra-pair offspring. The standardized variance in actual male reproductive success (i.e., the total number of within-pair and extra-pair offspring sired) was more than seven times higher than the variation in apparent success (i.e., success assuming that no extra-pair mating occurred). Success at siring within-pair and extra-pair offspring both contributed to the variation in overall male reproductive success. Within-pair success, however, did not predict a male's level of extra-pair success, suggesting that males do not sacrifice within-pair paternity to gain extra-pair paternity. Calculation of the sexual selection (Bateman) gradient showed that males sire approximately two additional offspring for each extra-pair mate that we identified. Thus, in this sexually dichromatic species, extra-pair mating increases the variance in male reproductive success and provides the potential for sexual selection to act.     

Individual Quality and Extra-Pair Paternity in the Blue Tit: Sexy Males Bear the Costs

Adaptive explanations for the evolution of extra-pair paternity (EPP) suggest that females seek extra-pair copulations with high quality males. Still, the link between ornamentation, individual quality, and paternity remains unclear. Moreover, honest signaling is essential when explaining EPP because it is needed for sexual selection to occur; yet, it is understudied in multiple ornaments. Because blue tits (Cyanistes caeruleus) show variable color expression in several plumage patches, we tested: (i) over two seasons, whether males in better condition, more ornamented and less infected by blood parasites gain EPP and have higher reproductive success, and (ii) over three seasons, whether mating patterns affect color change. Males with more saturated yellow feathers, brighter tails, and in better condition had higher reproductive success in one of the seasons. Contrary to expectation, in another season, males that gained EPP were parasitized by blood parasites, suggesting increased vector exposure during extra-pair copulations. Our results for two seasons show that males siring more extra-pair young were older and grew brighter cheek or tail feathers for the following season. Despite the increased mating costs, in socially monogamous avian systems, high quality males incur in EPP without compromising traits that may be under sexual selection.     

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.     

Manipulation of male quality in wild tits: effects on paternity loss

Extrapair paternity (EPP) has proved to be widespread and highlyvariable among birds and other taxa, including socially monogamousspecies. A multitude of hypotheses have been put forward toexplain this variation, but its occurrence is not fully understood.Male age, social dominance rank, song and breeding density orsynchrony have been among the suggested correlates of EPP, butresults so far are inconclusive. We interspecifically cross-fosteredblue tits (Parus caeruleus) and great tits (Parus major) inthe wild, thus manipulating males to exhibit reduced socialdominance rank, sing aberrant songs, and consequently be perceivedas low-quality males as compared to controls. This allowed usto test if male quality had an influence on loss of paternity.We found no statistically significant differences between cross-fosteredand control males of either species, neither with respect tolevels of cuckoldry nor proportions of extrapair young (EPY)in the broods. Paternity levels were comparable to other studieson the same species. No effect of density could be detectedon levels of EPP either, while an age effect seemed to be presentat least in the blue tit, EPY being almost absent in broodsof older blue tit males. We conclude that the effects of malequality on paternity loss are minor, if any, in these populations.     

Fertilization success and UV ornamentation in blue tits Cyanistes caeruleus: correlational and experimental evidence

Cases where less ornamented males are favored through sexualselection are rare among birds. Here we show, based on datafrom 3 consecutive breeding seasons, that male blue tits withless ultraviolet (UV)-ornamented crown feathers sire more offspring.This pattern was mainly driven by the higher success of older,less UV-ornamented males at siring extrapair offspring. Thereason behind this relationship is unclear although we hypothesizethat being less UV-ornamented may enable adult males to intrudeinto nearby territories by mimicking juveniles. To test causality,we experimentally manipulated male crown coloration creating2 groups, one with higher (UV(+) treatment) and one with lowerUV reflectance (UV(–) treatment). Contrary to our expectations,UV(–) males were less likely to sire extrapair offspringthan UV(+) males. The treatment had no effect on the likelihoodof losing paternity in a male's own nest. Because the experimentalevidence does not support the observational data, a direct effectof male crown color on extrapair success cannot be confirmed.However, potential pitfalls of this and other such color manipulationexperiments, like fading of treatment with time and mismatchesbetween behavior and coloration, call for new improved manipulationtechniques and detailed behavioral observations to conclusivelytest for the effect of blue tit crown coloration on male extrapairsuccess.     

A spatial genetic structure and effects of relatedness on mate choice in a wild bird population

Inbreeding depression, as commonly found in natural populations, should favour the evolution of inbreeding avoidance mechanisms. If natal dispersal, the first and probably most effective mechanism, does not lead to a complete separation of males and females from a common origin, a small-scale genetic population structure may result and other mechanisms to avoid inbreeding may exist. We studied the genetic population structure and individual mating patterns in blue tits (Parus caeruleus). The population showed a local genetic structure in two out of four years: genetic relatedness between individuals (estimated from microsatellite markers) decreased with distance. This pattern was mainly caused by immigrants to the study area; these, if paired with fellow immigrants, were more related than expected by chance. Since blue tits did not avoid inbreeding with their social partner, we examined if individuals preferred less related partners at later stages of the mate choice process. We found no evidence that females or males avoided inbreeding through extra-pair copulations or through mate desertion and postbreeding dispersal. Although the small-scale genetic population structure suggests that blue tits could use a simple rule of thumb to select less related mates, females did not generally prefer more distantly breeding extra-pair partners. However, the proportion of young fathered by an extra-pair male in mixed paternity broods depended on the genetic relatedness with the female. This suggests that there is a fertilization bias towards less related copulation partners and that blue tits are able to reduce the costs of inbreeding through a postcopulatory process.     

Extra-pair paternity in relation to male age in Bullock's orioles

Single-locus minisatellite DNA profiling was used to assign paternity in a population of Bullock's orioles, Icterus galbula bullockii, and to determine the contribution of age to a male's success in obtaining extra-pair paternity. There was a very low rate of intraspecific brood parasitism (2/202 = 1.0% of chicks). Older adult males lost less within-pair paternity and gained more extra-pair fertilizations than did yearling subadult males. This resulted in adult males benefiting from an annual reproductive success more than double that of subadult males. Behavioural observations, used to determine the role of female choice in extra-pair copulations (EPCs), indicated that females actively participate in EPCs and that they prefer to obtain them from older males. While it was possible that females obtained EPCs as an insurance against the possible infertility of their social mate, the results of this study fit best with the hypothesis that females were attempting to obtain better-quality genes for their offspring by obtaining EPCs with older, better-quality males.     

Are extra-pair young better than within-pair young? A comparison of survival and dominance in alpine marmot

1. In socially monogamous species, females may seek extra-pair copulation to gain genetic benefits. In order to test this 'genetic quality' hypothesis, one must compare the performance of extra-pair young (EPY) and within-pair young (WPY). Such tests, however, are scarce and results published so far are inconclusive. 2. Here, we test the 'genetic quality' hypothesis using multistate capture-recapture models to compare age-specific survival and access to dominance between EPY and WPY in the alpine marmot Marmota marmota, a socially monogamous mammal showing extra-pair paternities. 3. When compared with WPY, survival of EPY was higher by 15%, 10% and 30%, for juveniles, yearlings and 2-year-old individuals, respectively. Survival at older ages did not differ. 4. Survival corresponded to true survival for yearlings and juveniles as dispersal does not occur before 2 years of age in marmots. For older individuals, survival estimates included a mixture of survival and dispersal. The 30% increase of the 2-year-old EPY survival might reflect delayed dispersal rather than high survival of EPY as compared with WPY. 5. WPY and EPY had the same probability (0.28) to access dominance at 2 years of age, but EPY were more successful at older ages than WPY (0.46 vs. 0.10). 6. Both survival and reproductive performance were higher in EPY than in WPY. The fitness advantages of adopting such a mixed mating tactic are thus likely to be high for marmot females. We suggest that obtaining genetic benefits is the main evolutionary force driving extra-pair paternity in alpine marmots.     

Sources of (co)variation in alternative siring routes available to male great tits (Parus major)

Males of socially monogamous species can increase their siring success via within‐pair and extra‐pair fertilizations. In this study, we focused on the different sources of (co)variation between these siring routes, and asked how each contributes to total siring success. We quantified the fertilization routes to siring success, as well as behaviors that have been hypothesized to affect siring success, over a five‐year period for a wild population of great tits Parus major. We considered siring success and its fertilization routes as “interactive phenotypes” arising from phenotypic contributions of both members of the social pair. We show that siring success is strongly affected by the fecundity of the social (female) partner. We also demonstrate that a strong positive correlation between extra‐pair fertilization success and paternity loss likely constrains the evolution of these two routes. Moreover, we show that more explorative and aggressive males had less extra‐pair fertilizations, whereas more explorative females laid larger clutches. This study thus demonstrates that (co)variation in siring routes is caused by multiple factors not necessarily related to characteristics of males. We thereby highlight the importance of acknowledging the multilevel structure of male fertilization routes when studying the evolution of male mating strategies.     

MEASURING THE EFFECTS OF PAIRING SUCCESS,EXTRA-PAIR COPULATIONS AND MATE QUALITY ON THE OPPORTUNITY FOR SEXUAL SELECTION

Sexual selection can act through variation in the number of social mates obtained, variation in mate quality, or variation in success at obtaining extra-pair fertilizations. Because within-pair fertilizations (WPF) and extra-pair fertilizations (EPF) are alternate routes of reproduction, they are additive, rather than multiplicative, components of fitness. We present a method for partitioning total variance in reproductive success (a measure of the opportunity for selection) when fitness components are both additive and multiplicative and use it to partition the variance into components that correspond to each mechanism of sexual selection. Computer simulations show that extra-pair fertilizations can either increase or decrease total variance, depending on the covariance between within-pair and extra-pair success. Simulations also suggest that for socially monogamous species, extra-pair fertilizations have a greater effect than variation in mate quality or pairing status on the opportunity for selection. Application of our model to data gathered for a population of red-winged blackbirds (Agelaius phoeniceus) indicates that most of the variance in male reproductive success was attributable to within-pair sources of variance. Nevertheless, extra-pair copulations increased the opportunity for selection because males varied both in the proportion of their social young that they sired and in the number of extra-pair mates that they obtained. Furthermore, large and positive covariances existed between the number of extra-pair mates a male obtained and both social pairing success and within-pair paternity, indicating that, in this population, males preferred as social mates also were preferred as extra-pair mates.     

Extrapair paternity in the great tit (Parus major): a test of the "good genes" hypothesis

In 1993 and 1994 we determined the frequency of extrapair paternityin broods of great tits, Parus major using multilocus DNA fingerprinting.We found no instances of intraspecific brood parasitism, but40% of broods (31/78) contained extrapair-fathered young and83% of offspring (58/681) were xtrapair We identified the geneticfathers of 60% of the extrapair nestlings (35/ 58). Males withfull and lost paternity did not differ significantly in traitsthat have been suggested to indicate male quality, nor did thegenetic and social fathers of extrapair offspring. In 1993,cuckolded males sired more offspring that recruited to the subsequentbreeding season than males with full paternity. Moreover, eventhough genetic fathers of extrapair young (EPY) sired more fledglingsthan the males they cuckolded, genetic and social fathers ofEPY did not differ in the number of recruits sired. Also, theEPY of a brood did not survive better than their half sibs.Thus, our results do not supportthe hypothesis that femaleschoose better quality males for extrapair matings ("good genes"hypothesis). Further, the level of extrapair paternity differedmarkedly between the two years. Our data show that females areconstrained in their extrapair activities by the availabilityof extrapair mates. This is at least partly due to yearly differencesin breeding synchrony.     

How female reed buntings benefit from extra-pair mating behaviour: testing hypotheses through patterns of paternity in sequential broods

Extra-pair paternity is an important aspect of reproductive strategies in many species of birds. Given that in most species females control whether fertilization occurs, they are expected to benefit in some way from the extra-pair matings. In this study we use patterns of extra-pair paternity (EPP) in broods of individual reed buntings (Emberiza schoeniclus), both within and between seasons, to test four hypothesized female benefits: (1) assessing potential future partners and seeking (2) genetic diversity (3) good genes, or (4) compatible genes. Reed buntings are socially monogamous, multibrooded passerines with extremely high levels of extra-pair paternity. We studied a population of reed buntings in the Netherlands in 2002 and 2003; 51% of offspring in 74% of nests were extra-pair. We showed that patterns of EPP did not support the first and second hypotheses, since females did not form a pair with previous extra-pair partners, EPP was not evenly distributed among broods and more broods than expected were sired by a single male. Furthermore, there was no relation between a male's within- and extra-pair fertilization success, no consistency in EPP between breeding attempts, no effect of parental relatedness on EPP and several cases of reciprocal paternity. These patterns do not support the good genes hypothesis and are most consistent with the genetic compatibility hypothesis. However, our previous finding that older males are more successful in gaining EPP, suggests some effect of good genes. These hypotheses need not be mutually exclusive, as females may select compatible males above a certain quality threshold (e.g. old males).     

Do extra‐pair paternities provide genetic benefits for female blue tits Parus caeruleus?

A large body of theories on extra-pair paternity (EPP) in birds has proposed four main "genetic" hypotheses to explain this behaviour: the "good genes" hypothesis, the genetic diversity hypothesis, the genetic compatibility hypothesis and the fertility insurance hypothesis. Empirical tests have been scarce, mainly because high sample sizes are difficult to collect. We have tested these hypotheses in three Mediterranean populations of blue tits Parus caeruleus in which 50–68% of the broods contained extra-pair young. Results showed that the distribution of extra-pair young among broods was not random, and that survival to fledging of extra-pair young was higher than that of their within-pair sibs. These results support the idea of genetic effects benefiting extra-pair young. However, comparison of cuckolded and cuckolding males showed no significant difference in their body size, age, survival or relatedness with their paired females, and offspring morphometrics did not differ between extra-pair and within-pair young. We conclude that none of the genetic hypotheses can explain fully the high level of extra-pair paternity, at least in our populations of Mediterranean blue tits. We suggest that direct ecological benefits of EPP for females should be tested more often in correlative as well as experimental approaches.     

Age-specific patterns of infection with haemosporidians and trypanosomes in a warbler: implications for sexual selection

Although the selective loss of individuals susceptible to disease can favor the evolution of female preference for older males, the interrelationship between age, infection, longevity, and mating success remains poorly characterized in natural populations. In a longitudinal study of 61 male common yellowthroats (Geothlypis trichas), we found that the probability of infection with hematozoa increased as males aged from 1 to 5 years. Despite a significant, negative association between infection and longevity that partially masked age-effects, the odds that a male was infected with Trypanosoma, Plasmodium, or Leucocytozoon increased 71–212% per year. Nearly 75% of males in their first breeding season were either uninfected or infected with only a single parasite, while 50% of older males were infected with at least two parasites and 16% were infected with all three. No males escaped infection after their second breeding season. Older males were also more likely to sire extra-pair young (EPY) and, as a consequence, infection with multiple parasites was associated with a fourfold increase in the odds of producing EPY. Unlike younger males, 80% of the oldest males had a history of either surviving chronic infection or recovering. Combined with previous work showing higher diversity at the major histocompatibility complex among older males, our results suggest that the song and plumage traits that signal male age in common yellowthroats also, perforce, signal resistance to parasites. By preferring older males, females may obtain good genes for disease resistance even in the absence of any effect of infection on male ornamentation.     

Correlates of complete brood failure in blue tits: could extra‐pair mating provide unexplored benefits to females?

Behavioural ecologists have for decades investigated the adaptive value of extra‐pair copulation (EPC) for females of socially monogamous species. Despite extensive effort testing for genetic benefits, there now seems to be a consensus that the so‐called ‘good genes’ effects are at most weak. In parallel the search for direct benefits has mostly focused on the period surrounding egg laying, thus neglecting potential correlates of EPC that might be expressed at later stages in the breeding cycle. Here we used Bayesian methods to analyse data collected over four years in a population of blue tits Cyanistes caeruleus, where no support was previously found for ‘good genes’ effects. We found that broods with mixed paternity experienced less brood failure at the nestling stage than broods with single paternity, and that females having experienced complete brood failure in their previous breeding attempt had higher rates of mixed paternity than either yearling or previously successful females. To better understand these observations we also explored relationships between extra‐pair mating, male and female phenotype, and local breeding density. We found that in almost all cases the sires of extra‐pair offspring were close neighbours, and that within those close neighbourhoods extra‐pair sires were older than other males not siring extra‐pair offspring. Also, females did not display consistent EPC status across years. Taken together our results suggest that multiple mating might be a flexible female behaviour influenced by previous breeding experience, and motivate further experimental tests of causal links between extra‐pair copulation and predation.     

Reed bunting females increase fitness through extra-pair mating with genetically dissimilar males

Females of many socially monogamous species accept or even actively seek copulations outside the social pair bond. As females cannot increase the number of offspring with promiscuous behaviour, the question arises why they engage in extra-pair mating. We used microsatellite data to determine paternity, heterozygosity and genetic relatedness in the reed bunting (Emberiza schoeniclus), a species with high levels of extra-pair paternity (EPP). We found that extra-pair young (EPY) were more heterozygous than within-pair young (WPY). The high heterozygosity of the EPY resulted from a low genetic similarity between females and their extra-pair mates. EPY were heavier and larger when compared with their maternal half-siblings shortly before they left the nest. Recapture data indicated a higher fledgling survival of EPY compared with WPY. Our data suggest that reed bunting females increase the viability of their offspring and thus fitness through extra-pair mating with genetically dissimilar males.     

Love the one you're with: proximity determines paternity success in the barnacle Tetraclita rubescens

A species' mating system sets limits on the strength of sexual selection. Sexual selection is widespread in dioecious species, but is less well documented in hermaphrodites, and may be less important. We used four highly polymorphic microsatellite markers to assign paternity to broods of the hermaphroditic eastern Pacific volcano barnacle Tetraclita rubescens. These data were used to describe the species' mating system and to examine factors affecting male reproductive success. Tetraclita can sire broods over distances of 11.2 cm, but proximity to the sperm recipient had a highly significant effect on the probability of siring success. There was no effect of body size or the mass of male reproductive tissues on siring success. Broods showed relatively low frequencies of multiple paternity; even at high densities, 75% of broods had only one father. High frequencies of single‐paternity broods imply either that this species does not compete via sperm displacement, or that sperm displacement is extremely effective, potentially explaining the lack of a positive relationship between male investment and paternity. In addition, there was low variance in siring success among individuals, suggesting a lack of strong sexual selection on male traits. Low variance among sires and the strong effect of proximity are probably driven by the unusual biology of a sessile copulating species.     

Lifespan, lifetime reproductive performance and paternity loss of within-pair and extra-pair offspring in the coal tit Periparus ater

The hypothesis that females of socially monogamous species obtain indirect benefits (good or compatible genes) from extra-pair mating behaviour has received enormous attention but much less generally accepted support. Here we ask whether selection for adult survival and fecundity or sexual selection contribute to indirect selection of the extra-pair mating behaviour in socially monogamous coal tits (Periparus ater). We tracked locally recruited individuals with known paternity status through their lives predicting that the extra-pair offspring (EPO) would outperform the within-pair offspring (WPO). No differences between the WPO and EPO recruits were detected in lifespan or age of first reproduction. However, the male WPO had a higher lifetime number of broods and higher lifetime number of social offspring compared with male EPO recruits, while no such differences were evident for female recruits. Male EPO recruits did not compensate for their lower social reproductive success by higher fertilization success within their social pair bonds. Thus, our results do not support the idea that enhanced adult survival, fecundity or within-pair fertilization success are manifestations of the genetic benefits of extra-pair matings. But we emphasize that a crucial fitness component, the extra-pair fertilization success of male recruits, has yet