Extra-pair Behaviour Research Articles

Mate choice copying in monogamous species: should females use public information to choose extrapair mates?

Empirical evidence that females can copy each other's mating preferences comes predominantly from research on lekking species, but recent laboratory studies revealed that public information can also play a role in the evolution of mate preferences in monogamous species with biparental care. Although the question of why monogamous females copy each other's mating preferences is still debated, it has been suggested that public information could be used by females to assess and choose extrapair mates. Since there is only indirect empirical support for this hypothesis, I developed a game-theoretic model to explore the possible roles that mate choice copying may play in mediating extrapair behaviours in monogamous species. Like previous game-theoretic models on mate choice copying, the model predicts that only females that have a high probability of obtaining a better partner should copy the mating decisions of others. On the other hand, unlike previous games that applied to lekking species, the present model predicts that mate choice copying can be advantageous even when there is no variation among females in their discrimination ability and they all can assess the quality of potential partners without error. Moreover, as mate choice copying essentially benefits high-quality males, males of lower quality would be interested in developing defensive tactics to discourage females from seeking extrapair copulations, thereby contributing to intraspecific and interspecific variations in the rate of extrapair paternity.

High levels of environmental noise erode pair preferences in zebra finches: implications for noise pollution

Male–female pair bonds are common to most bird species, and these bonds affect fundamental aspects of mating systems and the strength of selection, for example, by limiting extrapair paternity. Therefore, understanding factors that strengthen and erode pair bonds are important in elucidating the selection pressures that avian populations will experience. Here, we studied the effects of environmental noise on pair bonds and the strength of pair preferences (i.e. preferences for a pair-bonded partner versus an unfamiliar individual) in the monogamous zebra finch, Taeniopygia guttata, a model species in studies of sexual selection. Based on a previous study, we hypothesized that high-amplitude environmental noise would decrease the strength of pair preferences. Explicitly, we tested whether females' relative preference for their pair-bonded males, compared with extrapair males, decreased as the amplitude of environmental white noise increased. Our results generally supported our hypothesis, as females' preference for their pair-bonded males significantly decreased under conditions of high environmental noise. This erosion of preference may result from the masking or distortion of the paired males' pair-bond maintaining call, although the decrease in preference could also occur because a female cannot recognize her pair-bonded male. Our findings suggest that songbird populations in areas with high environmental noise may have (temporarily or permanently) weakened pair bonds, suggesting that extrapair behaviours could increase in areas of greater environmental noise.

Ecological, social, and genetic contingency of extrapair behavior in a socially monogamous bird

Extrapair mating strategies are common among socially monogamous birds, but vary widely across ecological and social contexts in which breeding occurs. This variation is thought to reflect a compromise between the direct costs of mates’ extrapair behavior and indirect benefits of extrapair fertilizations (EPF) to offspring fitness. However, in most free‐living populations, the complete spatial and temporal distribution of mating attempts, genetic characteristics of available mates, and their relative contribution to EPF strategies are difficult to assess. Here we examined prevalence of EPF in relation to breeding density, synchrony, and genetic variability of available mates in a wild population of house finches Carpodacus mexicanus where all breeding attempts are known and all offspring are genotyped. We found that 15% of 59 nests contained extra‐pair offspring and 9% of 212 offspring were sired by extra‐pair males. We show experimentally that paired males and females avoided EPF displays in the presence of their social partners, revealing direct selection against EPF behavior. However, at the population level, the occurrence of EPF did not vary with nests dispersion, initiation date, synchrony, or with distance between the nests of extrapair partners. Instead, the occurrence of EPF closely covaried with genetic relatedness of a pool of available mates and offspring of genetically dissimilar mating tended to be resistant to a novel pathogen. These results corroborate findings that, in this population, strong fitness benefits of EPF are specific to each individual, thus highlighting the ecological, social, and genetic contingency of costs and benefits of an individual's extrapair behaviors.

Ecological, social, and genetic contingency of extrapair behavior in a socially monogamous bird

Ecological, social, and genetic contingency of extrapair behavior in a socially monogamous bird

Reed bunting (Emberiza schoeniclus) males sing an 'all-clear' signal to their incubating females

AbstractWhile sexual functions of birdsong have been intensively investigated, non-sexual functions have received less attention. After pair formation males may sing to communicate with their established mates. Song aimed at incubating and feeding females could serve as an 'all-clear' signal, showing that there is no risk of predation and that it is safe for the female to exit the nest or to feed the young. Females should therefore preferentially leave nests when mates are singing nearby. Additionally, a vigilant male near the nest site could protect the brood from potential risks like predation and females could stay away longer for foraging. In this study, we investigated aspects of male singing activity of reed buntings (Emberiza schoeniclus) during incubation and feeding of nestlings after pair formation. Exits of incubating females from the nest occurred significantly more often than expected during male song output. When their mates were singing at high rates, females stayed away longer for incubation breaks. During the nestling period we found a high variation in male song output. Males that sang more fed their young significantly less. This suggests that time devoted to singing limits other activities such as feeding of offspring. Male reed buntings could choose different strategies for paternal investment: They either feed at high rates or they sing more to signal their vigilance. Another reason for this trade-off might be a conflict between paternal investment and territory defence or extrapair behaviour. However, even if male song after pairing has additional sexual functions, we suggest that non-sexually selected functions may be more common than expected.

Mother guarding: how offspring may influence the extra-pair behaviour of their parents

In this paper we propose a novel form of social control of mate choice. Through mother guarding, offspring can help in protecting the paternity of their father by preventing their mother from engaging in extra-pair matings. We present a model that predicts the circumstances under which mothers should be selected to seek or avoid extra-pair matings, and existing offspring should be selected to prevent or promote such matings. In its simplest form, our model shows that offspring are selected to mother guard as long as the viability of extra-pair young is less than twice that of within-pair young; when the relative viability is greater, offspring are selected to promote extra-pair mating by their mother. If the existing offspring are not necessarily sired by their mother's social mate, then the potential for conflict is further reduced. We also consider whether offspring have an interest in the extra-pair reproduction of their fathers. We show that when the costs of the father's infidelity to the mother's brood are high, existing offspring are selected to prevent extra-pair mating by their father; when such costs are low, offspring are selected to promote extra-pair mating by their father. In principle, our model applies to all species where offspring show delayed dispersal and where breeding pairs raise multiple broods or litters. This situation exists in, but is not limited to, the majority of cooperatively breeding species. The significance of this model with regard to our current understanding of the evolution of extra-pair behaviour in such species is discussed.

Mate Opportunity Hypothesis and Extrapair Paternity in Waved Albatrosses (Phoebastria Irrorata)

Abstract Early arrival at breeding sites can influence reproductive success through enhanced access to critical resources such as nest sites or mates. One hypothesis explaining protandry, or male-first arrival at breeding sites, proposes that males arrive earlier to increase their extrapair copulation (EPC) opportunities, which may, in turn, enhance males' reproductive success through extrapair fertilizations (EPFs) (“mate opportunity hypothesis”). Extrapair behavior is unexpected in long-lived birds, in which the male is expected to abandon a brood of uncertain paternity, because his probability of future reproduction is high. A previous study of the Waved Albatross (Phoebastria irrorata), a long-lived, socially monogamous seabird, showed evidence of EPFs in 4 of 16 (25%) families. Here, we combined behavioral observations of copulations with additional molecular genetic evidence of EPFs in Waved Albatross families to investigate the fitness consequences of protandry under the mate opportunity hypothesis. During three breeding seasons, we documented 3,661 attempted copulations between birds of known identity; >60% of copulations that involved at least one breeding bird were classified as EPCs. Protandry was pronounced in all three study years: 76.3–96.6% of males arrived before (typically, 6–10 days before) their social mates. Early arrival was associated with increased opportunities for copulations: individual EPC frequencies were higher for breeding males than for breeding females, and males that arrived earlier than their social mates engaged in the most EPCs. Extrapair fertilizations were also regular in our study population; social fathers were excluded as the genetic sire in 14–21% of families. Egg laying dates of EPFs tended to be earlier in the season than those of within-pair fertilizations (WPFs). However, earlier arrival by a male did not translate into a higher probability of siring either within-pair or extrapair offspring, nor did cuckolding males have enhanced reproductive success. Although the fitness consequences of early arrival remain unclear, these findings suggest alternative advantages of early arrival for male Waved Albatrosses. La Hipótesis de Oportunidad de Apareamiento y Paternidad Extra-pareja en Phoebastria irrorata

MATE OPPORTUNITY HYPOTHESIS AND EXTRAPAIR PATERNITY IN WAVED ALBATROSSES (PHOEBASTRIA IRRORATA)

Abstract Early arrival at breeding sites can influence reproductive success through enhanced access to critical resources such as nest sites or mates. One hypothesis explaining protandry, or male-first arrival at breeding sites, proposes that males arrive earlier to increase their extrapair copulation (EPC) opportunities, which may, in turn, enhance males' reproductive success through extrapair fertilizations (EPFs) (“mate opportunity hypothesis”). Extrapair behavior is unexpected in long-lived birds, in which the male is expected to abandon a brood of uncertain paternity, because his probability of future reproduction is high. A previous study of the Waved Albatross (Phoebastria irrorata), a long-lived, socially monogamous seabird, showed evidence of EPFs in 4 of 16 (25%) families. Here, we combined behavioral observations of copulations with additional molecular genetic evidence of EPFs in Waved Albatross families to investigate the fitness consequences of protandry under the mate opportunity hypothesis...

Mate guarding, male attractiveness, and paternity under social monogamy

Socially monogamous species vary widely in the frequency of extrapair offspring, but this is usually discussed assuming that females are free to express mate choice. Using game-theory modeling, we investigate the evolution of male mate guarding, and the relationship between paternity and mate-guarding intensity. We show that the relationship between evolutionarily stable mate-guarding behavior and the risk of cuckoldry can be complicated and nonlinear. Because male fitness accumulates both through paternity at his own nest and through his paternity elsewhere, males evolve to guard little either if females are very faithful or if they are very unfaithful. Attractive males are usually expected to guard less than unattractive males, but within-pair paternity may correlate either positively or negatively with the number of extrapair offspring fertilized by a male. Negative correlations, whereby attractive males are cuckolded more, become more likely if the reason behind female extrapair behavior applies to most females (e.g., fertility insurance) rather than the subset mated to unattractive males (e.g., when females seek “good genes”) and if mate guarding is efficient in controlling female behavior. We discuss the current state of empirical knowledge with respect to these findings.

Extrapair Fertilizations in Red Bishops (Euplectes Orix): Do Females Follow Conditional Extrapair Strategies?

AbstractAlthough many studies have revealed differences in patterns of extrapair paternity between species and between populations of the same species, possible differences in female extrapair behavior within populations have received far less attention. Here, we propose and test the hypothesis that females of the highly polygynous Red Bishop (Euplectes orix) follow two different extrapair strategies, with benefits of extrapair copulations depending on the quality of their social mate (”conditional-extrapair-strategy hypothesis”). In particular, we propose that females mated to low-quality males enhance the genetic quality of their offspring by performing extrapair copulations with males of higher quality than their social mate (in accordance with the good-genes hypothesis), whereas females mated to high-quality males perform extrapair copulations as insurance against temporary infertility of their social mate caused by sperm depletion due to frequent copulations (in accordance with the fertility-insurance hypothesis). Several predictions derived from our hypothesis, regarding differences in frequency and distribution of both unhatched eggs and extrapair young between high-quality and low-quality males, are tested and shown to be supported. Most importantly, hatching failures occurred more often in territories of high-quality males than in those of low-quality males, and the proportion of unhatched eggs within the territory was positively correlated to breeding synchrony for high-quality males only. Those results suggest that sperm depletion is a risk for females mated to high-quality males with many mating opportunities. The fact that broods of high-quality males without unhatched eggs had a significantly higher proportion of extrapair young than broods of high-quality males with unhatched eggs is consistent with the hypothesis that females mated to high-quality males were successful in performing EPCs as insurance against temporary infertility of their social mates. Furthermore, genetic fathers of extrapair young hatched in territories of low-quality males were found to be of higher quality than the corresponding social fathers, whereas no difference in quality was found between genetic and social fathers of extrapair young hatched in territories of high-quality males. Although we cannot exclude the possibility that the observed pattern was a result of females mating randomly from within the available pool of extrapair males, it is in accordance with our prediction that females mated to low-quality males perform extrapair copulations with males of higher quality than their social mate to enhance offspring fitness. Overall, the data presented here suggest that females within our study colony adjusted their extrapair behavior to the quality of their social mate, even if we cannot entirely rule out alternative explanations for some of the results obtained. Thus, the study provides support for the conditional-extrapair-strategy hypothesis, which states that within populations, females may follow different extrapair strategies to gain different benefits.Fertilizaciones Extra-pareja en Euplectes orix: ¿Siguen las Hembras Estrategias Extra-pareja Condicionales?

EXTRAPAIR FERTILIZATIONS IN RED BISHOPS (EUPLECTES ORIX): DO FEMALES FOLLOW CONDITIONAL EXTRAPAIR STRATEGIES?

Abstract Although many studies have revealed differences in patterns of extrapair paternity between species and between populations of the same species, possible differences in female extrapair behavior within populations have received far less attention. Here, we propose and test the hypothesis that females of the highly polygynous Red Bishop (Euplectes orix) follow two different extrapair strategies, with benefits of extrapair copulations depending on the quality of their social mate (”conditional-extrapair-strategy hypothesis”). In particular, we propose that females mated to low-quality males enhance the genetic quality of their offspring by performing extrapair copulations with males of higher quality than their social mate (in accordance with the good-genes hypothesis), whereas females mated to high-quality males perform extrapair copulations as insurance against temporary infertility of their social mate caused by sperm depletion due to frequent copulations (in accordance with the fertility-insuran...

High frequency of extra-pair fertilisations in the moustached warbler, a songbird with a variable breeding system

Summary We examined the genetic mating system of the moustached warbler Acrocephalus melanopogon, a multi-brooded songbird that sometimes breeds in trios (one female and two males). The second male, which appears relatively late in the breeding cycle, participates in all forms of parental care but provides less care than the pair male. DNA fingerprinting revealed a high frequency of extra-pair paternity: 39% (7/18) of the broods contained extra-pair young, comprising 27% (12/44) of the chicks. An additional 7 broods contained at least 9 chicks (out of 20) that were not sired by the resident male. We were able to assign paternity for 11 (52%) of the extra-pair young. Of these, 7 (64%) were sired by secondary males and 4 (36%) by close neighbours (nesting within 50 m). Consistently, pairs with extra-pair young had more close neighbours, and they also tended to have a secondary male at the nest. Caring for nestlings that they might have sired through extra-pair copulations may be a way for secondary males to salvage their reproductive effort. They may also provide parental care because of the possibility of pairing with the female in future breeding attempts. Our results suggest that female moustached warblers obtain direct benefits (i.e., help with brood care) from extra-pair copulations. However, a skewed fertilisation pattern implies that genetic compatibility between mates and copulation partners may also influence female extra-pair behaviour in this species.

Intense extrapair behaviour in a semicolonial passerine does not result in extrapair fertilizations

Sperm competition is a strong force on the evolution of mating behaviour of animals, particularly birds. In monogamous birds extrapair behaviour is one main source of variation in the reproductive success of males, which has caused the evolution of paternity guards as well as strategies by females to increase the genetic quality of their descendants. We investigated the importance of sperm competition in the reproductive behaviour of serins, Serinus serinus. Male serins guarded their mates and also copulated frequently, indicating that sperm competition has been an important selective force affecting their mating behaviour. Females were frequently approached and chased by extrapair males that attempted extrapair copulations. However, females refused almost every attempt by extrapair males. No extrapair paternity was detected in the population, in spite of the intense extrapair behaviour of males. This supports the view that females keep strong control over paternity, and that in this population they do not seem to obtain genetic benefits from extrapair copulations. We discuss why the presence of high levels of sexual competition may not be reflected in extrapair paternity. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Ecological constraints on extra-pair paternity in the bluethroat.

The mating system of the bluethroat (Luscinia s. svecica) involves a high level of sperm competition, and consequently a high frequency of extra-pair paternity (EPP). There is considerable variation in the frequency of EPP. Over the course of ten study years in a population in Norway, the frequency has fluctuated between 7% and 33% of young, and 8% and 76% of broods. In this paper, we address the issue of whether ecological factors can explain some of the variation in EPP between years and broods. Factors include breeding density, breeding synchrony and two meteorological variables (ambient temperature and precipitation) during the period of peak female fertility. There were no significant relationships between annual averages of the four variables and the annual level of EPP, but the statistical power of these tests was low, due to a restricted sample (n=10 years). Focussing on individual broods, none of the factors had significant effects when including all broods in the analyses (including those with zero EPP). When limiting the analyses to broods with one or more extra-pair offspring, morning temperature had a significant effect on the frequency of EPP. When the temperature was low during the peak of the fertile period, EPP occurred less frequently. Male extra-pair behaviour was not generally constrained by synchrony between the fertile periods of the social mate and the extra-pair mate, but for a subgroup of males ("unattractive males") there appeared to be a trade-off between mate guarding and pursuing extra-pair copulations. Our results indicate that ecological conditions have no influence on whether or not a brood will contain extra-pair offspring, but when EPP does occur, its frequency is influenced by air temperature. Possibly, there is a causal relationship between weather conditions and the frequency of extra-pair encounters in this species. The breeding season is initiated at a phenologically early stage, when large parts of the territories are still covered with snow, and cold weather conditions may force the birds to devote most of their time to maintenance and thereby constrain sexual activities.

Male shrikes punish unfaithful females

The costs to females of participating in extrapair copulations is an interesting but hitherto neglected topic in behavioral ecology. An obvious potential cost to females is male physical sanctions. However, although retaliation and punishment by male partners has been proposed as a basic cost for female extrapair behavior in theory, it has not been experimentally demonstrated. We studied the breeding biology of the lesser gray shrike (Lanius minor) and combined field observations and a field experiment to show that (1) there is a high intrusion rate during the female's fertile period, and extrapair copulations occur in this population; (2) by detaining females during the fertile phase, males were induced to retaliate physically against their partners, thereby increasing costs related to female extrapair behavior; and (3) there were no obvious costs to males of punishing their mates. DNA fingerprinting reveals that extrapair paternity is rare or absent in this population. Although we cannot conclude that monogamy at the genetic level is the result of male retaliation, we do show that male physical sanction is a cost that deceptive females have to assume. Males' strategies based on coercion should be considered when explaining variation in extrapair paternity across species.

Extra-pair Paternity in the Dusky Warbler, Phylloscopus fuscatus: a Test of the 'Constrained Female Hypothesis'

The 'constrained-female hypothesis' (CFH) states that females risk losing their social partner's assistance in brood care when they engage in extra-pair copulations. Hence, it is predicted that individual differences in female extra-pair behaviour can be explained in terms of (1) the amount of male care that females risk to lose (2) the intrinsic ability of females to raise offspring without male help, and (3) food availability, facilitating uni-parental care. The dusky warbler, a species with a polygynous mating system and a high rate of extra-pair paternity (45% of the offspring) offers an excellent opportunity to test all these predictions. In accordance with prediction (1) I find that females in pairing situations in which they cannot expect to receive male assistance in brood care are more likely to have extra-pair young than females in situations where bi-parental care is the rule. Using age and bill morphology as predictors for a female's ability to raise nestlings alone, I find no direct support for prediction (2). Finally, variation in food availability (3) had no influence on extra-pair paternity. Overall, the CFH provides some explanation for why female promiscuity differs between situations of bi-parental and uni-parental care, but the large amount of remaining variation can neither be explained by food abundance nor by individual female characteristics.

Mate acquisition in the European blackbird and its implications for sexual strategies

Female European blackbirds, Turdus merula have been shown to engage in mixed reproductive strategies and females do not seem to gain any material benefit from their extra-pair copulation behaviour. To test the hypothesis that such behaviour arises out of constraint on their choice of social mate, I investigate if and how these females are constrained in their choice at mate acquisition. I recorded patterns of territorial distribution and interactions between resident birds both before pairing and during the breeding season. Patterns of observed behaviour agreed with earlier descriptions of winter and breeding territoriality and provided clues to the underlying mechanism of mate acquisition. I conclude that the constraint on breeding success imposed by high nest predation promotes intrasexual competition for high quality nesting habitat between females prior to pair formation. Female distribution promotes intrasexual competition between males for territorial area overlapping females or for habitat likely to be occupied by females. Mate choice during pair formation is constrained by the outcome of this intrasexual competition and, typically, overlapping territorial males and females pair into social monogamy on a shared breeding territory. Although this ultimately leads to assortitive mating by competitive ability, low quality females paired to low quality males may improve upon the quality of their genetic mate by engaging in extra-pair copulations. These data suggest that the process of mate acquisition in urban European blackbirds constrains the choice of social mate and so generates sexual selection pressures to drive mixed reproductive strategies during the breeding season.

Do female great tits (Parus major) assess males by eavesdropping? A field study using interactive song playback

Male singing behaviour correlates with extra-pair success in several passerine birds. Singing interactions during territorial contests provide relative information on the males involved. Such information may be important in female extra-pair behaviour and eavesdropping on singing interactions among males may allow females to make such relative assessments. We used interactive playback to instigate singing contests with male great tits during the peak fertile period of their mate in an attempt to alter females' assessment of mates' quality relative to neighbours (potential extra-pair partners). We escalated a contest to one male (by overlapping his songs) and then subsequently de-escalated a contest (by alternating) to a neighbour. Intrusions onto neighbouring territories by females mated to either treatment male were then monitored. Females mated to escalation treatment males were more likely to intrude following playbacks than females mated to de-escalation treatment males. Although the absolute song output of males did not differ between treatments, males produced more song relative to playback in de-escalation treatments and relative song output was positively correlated with female intrusions. Therefore, female great tits eavesdrop on singing interactions and change their visitation rates to neighbouring territories according to their mate's singing performance relative to neighbours.

Female extra–pair behaviour and environmental quality in the serin (Serinus serinus): a test of the ‘constrained female hypothesis’

Recent behavioural and molecular studies have shown that in most monogamous bird species extra-pair copulations and fertilizations outside the pair bond occur routinely. The consequences of female extra-pair behaviour might comprise effects on important life-history traits, such as the extent of male parental care. In this study we test the assumption that, within a species, females' options for extra-pair mating depend on female quality and the environments that females occupy. This 'constrained female hypothesis' predicts that females in good environments or high-quality females are able to resist males' control efforts better than females in poor environments or low-quality females. We test the idea in the socially monogamous serin. We found that the likelihood of extra-pair paternity is significantly higher in territories with high availability of food. There was a negative relationship between environmental quality (food availability) and paternity both in natural and in experimentally manipulated habitats. Male feeding rates were negatively related to food availability and positively related to paternity. These data and the additional result that in better environments all of a females' offspring were sired by one extra-pair male provide support for Gowaty's 'constrained female hypothesis'.

Sibling competition and the evolution of growth rates in birds

Variation among bird species in growth rates is traditionally attributed to differences in energy availability and developmental mode. However, the extent and form of competition among siblings for limited food resources may also be an important determinant. Kin-selection-based models of intrabrood competition suggest that nestling growth rates should be highest in those species in which siblings are likely to be less genetically related to one another (half-sibs rather than full-sibs). We test this novel prediction using the frequency of multiple paternity as an index of average sib relatedness within broods. As predicted, we find a significant positive association between the rate of multiple paternity within broods and nestling growth rates. Furthermore, this holds true when we control for the effects of variation in other factors that may be associated with variation in growth rate, such as body size, brood size, mating system and the form of parental care. We suggest, therefore, that variation in growth rate among bird species is not simply dependent on proximate ecological and developmental factors but is also strongly influenced by interactions, over an evolutionary time-scale, among kin.