Bateman gradients in field and laboratory studies: a cautionary tale

Since tools of molecular genetics became readily available,our understanding of bird mating systems has undergone a revolution.The majority of passerine species investigated are sociallymonogamous, but have been shown to be genetically polygamous.Data sets from natural populations of juncos suggest that multiplemating by females results in a sexual selection gradient assteep for females as for males (a result that does not supportBateman's predictions). However, in males, fitness is enhanceddirectly through fertilization success with multiple matings;in females fitness benefits may be enhanced immediately throughdirect access to food, protection against predators, or otherresources received from males, or they may be delayed throughimprovement in offspring quality (e.g., through good genes,or greater genetic compatibility between the female and theextra-pair male). But a steep sexual selection gradient forfemales can be difficult to interpret. If all females copulatewith multiple partners that are equally likely to fertilizeeggs, then females that produce larger clutch sizes, for anyreason, will appear to have copulated with more males. Thatis, multiple sires have a higher probability of detection inlarger clutches than in smaller ones, giving the impressionthat females that mate with multiple males increase their reproductivesuccess. Yet, in most studies in which there is a correlationbetween number of offspring produced by females and number ofextra-pair males, causation has not been clearly establishedand other factors may explain the results. Additional complicationsin understanding male and female reproductive strategies are:(1) Molecular studies cannot detect extra-pair copulations thatdid not result in fertilizations; yet if a female acquires foodor other resources from extra-pair males, such extra-pair matingsmay have significant effects on female fitness. Thus, molecularstudies provide only a conservative estimate of the number ofextra-pair copulations or "mates" that a female has. (2) Clutchsize affects the probability that any given male will be successfulin fertilizing a female's eggs. Specifically, at any given point,a male's chances of fertilizing at least one egg in the female'sclutch will be greater as clutch size increases. We predictthat in avian species with small clutch sizes, males may beselected to be choosy and avoid extra-pair copulations, whilefemales should be selected to be less discriminating. Moreover,if extra-pair males provide resources that increase female fitness,the females should seek extra-pair copulations, whether or notthe males are likely to fertilize any of her eggs. Laboratory studies with insects have yielded clearer evidenceof the causal relationship between multiple mating and increasedfemale fitness. We review studies on a tenebrionid beetle inwhich female fecundity increases directly with number of mates.In these experiments, the nutritive value of the spermatophoresdoes not fully explain the increase in female reproductive success.     

Sperm Competition and Copulation Intervals of the White Spoonbill (Platalea leucorodia,Aves, Threskiornithidae)

Some aspects of sperm competition were studied in the white spoonbill (Platalea leucorodia) breeding in Doñana National Park (SW Spain). Shorter pair copulation intervals occurred during the prelaying period, when females were subjected to a relatively high frequency of extra-pair copulations. Pair copulation intervals with an intermediate extra-pair copulation by the male mate were longer than those without extra-pair copulation. This result indicates that males need a time of recovery between copulations before they can perform another. Extra-pair copulations by the females did not affect the length of intervals between pair copulations. There were no differences between the lengths of the intervals between an extra-pair copulation by the female and the following pair copulation for cases in which the male mate detected an intruder male attempting copulation with his mate and those in which the intruder remained undetected. However, the correlations obtained between copulatory intervals for detected and undetected cases suggest a copulatory response by their mates, although affected by the required recovery time between copulations by the males. Finally, since extra-pair copulations mainly occurred while male mates were collecting nest material, they engaged in this activity shortly after pair copulations, probably to avoid a last-male advantage under the sperm competition pressure.     

Reproductive Synchrony and Extra-pair Copulation in Birds

We present a model which explores the idea that females may reduce their risk of suffering a forced extra-pair copulation, by breeding synchronously with other females in the population. Information from three bird species with contrasting ecology and behaviour shows that synchrony does not automatically confer an advantage on females: synchrony is only advantageous to females if certain conditions pertain. We identify three main factors which influence female extra-pair copulation risk, these are: (i) whether or not males can identify fertile females, (ii) male and female ‘availability’ (e.g. in some seabirds copulation and extra-pair copulations occur only at the colony: females may be absent for long periods and hence are unavailable for extra-pair copulations), (iii) the timing of extra-pair copulations by males, relative to when their partners lay.     

Immune defence,extra-pair paternity,and sexual selection in birds

Secondary sexual characters have been suggested to reliably reflect the ability of individuals to resist debilitating parasites, and females may gain direct or indirect fitness benefits from preferring the most extravagantly ornamented males. Extra-pair paternity provides an estimate of an important component of sexual selection in birds. Species with a high frequency of extra-pair paternity have a variance in realized reproductive success that is greater than the variance in apparent reproductive success, and extra-pair copulations and hence extra-pair paternity by females are often directly associated with the expression of male secondary sexual characters. If sexually dichromatic species have experienced a long period of antagonistic coevolution with their parasites, such species should have evolved larger immune defence organs than sexually monochromatic species. Bird species with sexual dichromatism had larger spleens for their body size than monochromatic species in a comparative analysis. Furthermore, species with a high frequency of extra-pair paternity were sexually dichromatic and had large spleens for their body size. These results are consistent with the hypothesis that females of dichromatic bird species seek extra-pair copulations to obtain indirect fitness benefits in terms of superior resistance of their offspring to virulent parasites.     

Why Do Female Birds Reject Copulations from their Mates?

Female birds frequently reject copulations from their mates, suggesting a conflict between the sexes. This study analyses behavioural data of socially monogamous razorbills, Alca torda, to examine whether females rejected their mates because of conflicts over fertilization or the pair bond. Among pairs, females rejected 9–70 % of their mates’ copulation attempts and prevented their mates from completing 42–100 % of successful copulations. Copulations terminated by females were half the duration of those terminated by males, and females terminated fewer first copulations than subsequent ones on the same day. These findings indicate that females were motivated to copulate less frequently and for shorter durations than their mates. The sperm competition hypothesis predicts that females reject their mates to increase the probability of being fertilized by extra-pair males. This hypothesis was not supported because females rejected extra-pair males similarly to their mates. The female-mate-guarding hypothesis predicts that females guard their pair bond by copulating frequently with their mates, thereby depriving the males of time and energy to copulate with and form bonds with other females. This prediction was consistent with a significant negative correlation between the percentage of copulation attempts that females accepted from their mates, and the number of extra-pair copulations that their mates attempted. However, this correlation was not caused by a trade-off of males copulating with their mates instead of attempting extra-pair copulation because males attempted most extra-pair copulations on days when their mates were absent. A new hypothesis is proposed, namely, that females reject their mates to test the male's commitment to provide essential parental contributions after egg-laying. The ‘testing-of-the-bond’ hypothesis is consistent with the findings but requires testing.     

Extra-Pair Mating and Evolution of Cooperative Neighbourhoods

A striking but unexplained pattern in biology is the promiscuous mating behaviour in socially monogamous species. Although females commonly solicit extra-pair copulations, the adaptive reason has remained elusive. We use evolutionary modelling of breeding ecology to show that females benefit because extra-pair paternity incentivizes males to shift focus from a single brood towards the entire neighbourhood, as they are likely to have offspring there. Male-male cooperation towards public goods and dear enemy effects of reduced territorial aggression evolve from selfish interests, and lead to safer and more productive neighbourhoods. The mechanism provides adaptive explanations for the common empirical observations that females engage in extra-pair copulations, that neighbours dominate as extra-pair sires, and that extra-pair mating correlates with predation mortality and breeding density. The models predict cooperative behaviours at breeding sites where males cooperate more towards public goods than females. Where maternity certainty makes females care for offspring at home, paternity uncertainty and a potential for offspring in several broods make males invest in communal benefits and public goods. The models further predict that benefits of extra-pair mating affect whole nests or neighbourhoods, and that cuckolding males are often cuckolded themselves. Derived from ecological mechanisms, these new perspectives point towards the evolution of sociality in birds, with relevance also for mammals and primates including humans.     

Paternal care declines with increased opportunity for extra-pair matings in fairy martins

Following the discovery that extra-pair fertilizations are common in many birds, it has been predicted that male participation in parental care may be influenced by their opportunity for extra-pair copulations. However, such a trade-off between male contribution to parental care and the availability of fertile females has not been confirmed. Here we use a novel remote monitoring technique to show that participation in incubation by male fairy martins, Hirundo ariel, declines with the increasing availability of fertile females in the breeding colonies. Furthermore, male contribution to incubation is most responsive to change in the availability of fertile females in the early morning, when most copulations occur, and also if their clutches are smaller than average. Both of these patterns support the presence of a trade-off between parental and extra-pair copulation effort. We suggest that this trade-off may be widespread among the 90% of bird species where males contribute to parental care.     

Sperm competition and sexually size dimorphic brains in birds

Natural selection may favour sexually similar brain size owing to similar selection pressures in males and females, while sexual selection may lead to sexually dimorphic brains. For example, sperm competition involves clear-cut sex differences in behaviour, as males display, mate guard and copulate with females, while females choose among males, and solicit or reject copulations. These behaviours may require fundamentally different neural government in the two sexes leading to sex-dependent brain evolution. Using two phylogenetic approaches in a comparative study, we tested for roles of both natural and sexual-selection pressures on brain size evolution of birds. In accordance with the natural-selection theory, relative brain size of males coevolved with that of females, which may be the result of adaptation to similar environmental constraints such as feeding innovation. However, the mode of brain size evolution differed between the sexes, and factors associated with sperm competition as reflected by extra-pair paternity may give rise to sexually size dimorphic brains. Specifically, species in which females have larger brains than males were found to have a higher degree of extra-pair paternity independently of potentially confounding factors, whereas species in which males have relatively larger brains than females appeared to have lower rates of extra-pair paternity. Hence, the evolution of sperm competition may select for complex behaviours together with the associated neural substrates in the sex that has a higher potential to control extra-pair copulations at the observed levels. Brain function may thus be affected differently in males and females by sexual selection.     

An alternative route to coloniality in the bearded tit: females pursue extra-pair fertilizations

We combine behavioral studies with DNA-fingerprinting of a populationof bearded tits Panurus biarmicus and test the idea that thepursuit of extra-pair copulations by females acts as selectivepressure that may contribute to the formation of colonies inthis socially monogamous species. We show that the rate of extra-pairpaternity in colonial breeding pairs is very high, whereas noextra-pair chicks were detected in solitary nests. We foundno cases of extra-pair maternity and intraspecific brood parasitismin solitary nests, whereas it did occur in dense breeding situations.We further found no difference in the quality of males betweencolonial and solitary individuals. However, colonial femaleswere of significantly higher quality in terms of body size andcondition. We propose that high-quality females settle in coloniesto increase their opportunities to adjust the choice of theirsocial partner by obtaining extra-pair copulations. We suggestthat colony formation enables high-quality females to incitemale-male competition for extra-pair copulations and consequentlysecure extra-pair fertilizations by high-quality males and thathigh-density nesting is controlled by female bearded tits     

Sexual selection in the monogamous barn swallow (Hirundo rustica). II. Mechanisms of sexual selection

Mechanisms of sexual selection in the monogamous, sexually dimorphic barn swallow (Hirundo rustica) were studied during a seven-year period. First, the sex ratio of reproducing adults was male-biased, and mated males had significantly longer tail ornaments than unmated males. Secondly, some of the unmated individuals later committed infanticide and became mated with the mother of the killed brood. Fathers of killed broods had significantly shorter tails than other males, and there was a tendency for infanticidal males to have longer tail ornaments than other unmated males. Thirdly, long-tailed male barn swallows were more successful in acquiring extra-pair copulations than other males, and females involved in extra-pair copulations, as compared to females not involved in such copulations, had mates with shorter tail ornaments. Fourthly, male barn swallows having long tails as compared to short-tailed males acquired mates in better body condition. Females mated to long-tailed males reproduced earlier, laid more eggs and were more likely to have two clutches than were females mated to short-tailed males. Finally, females mated to long-tailed males put more effort into reproduction than did other females, as evidenced by their relatively larger contribution to feeding of offspring. Thus, at least five different components of sexual selection affected male reproductive success. Selection arising from differential success during extra-pair copulations, differential reproductive success and differential male reproductive effort thus accounted for most of the selection on tail ornaments in male barn swallows.     

Extra-pair matings and mate guarding in the common murre Uria aalge

Forced extra-pair copulations (FEPC) are frequent and mate guarding well developed among common murres. Male murres were at the colony almost continuously through the pre-laying period, but females were present only infrequently, and the frequency of FEPCs was significantly correlated with the relative number of males present. Males vigorously defended their partners from other males and females attempted to resist extra-pair matings. Females whose mates were absent were particularly vulnerable to FEPCs. The number of extra-pair copulations performed by males was estimated to vary between 0–32/season. The reproductive successes of males not performing FEPC, and those performing at the mean and maximum rate are estimated. Males most active in FEPC may substantially increase their reproductive success compared with males not performing FEPC. Ecological conditions in the common murre probably favour prolonged sperm storage, which in turn provides opportunities for sperm competition and favours both effective mate guarding and extra-pair copulations.     

Coevolution of male and female genital morphology in waterfowl

Most birds have simple genitalia; males lack external genitalia and females have simple vaginas. However, male waterfowl have a phallus whose length (1.5->40 cm) and morphological elaborations vary among species and are positively correlated with the frequency of forced extra-pair copulations among waterfowl species. Here we report morphological complexity in female genital morphology in waterfowl and describe variation vaginal morphology that is unprecedented in birds. This variation comprises two anatomical novelties: (i) dead end sacs, and (ii) clockwise coils. These vaginal structures appear to function to exclude the intromission of the counter-clockwise spiralling male phallus without female cooperation. A phylogenetically controlled comparative analysis of 16 waterfowl species shows that the degree of vaginal elaboration is positively correlated with phallus length, demonstrating that female morphological complexity has co-evolved with male phallus length. Intersexual selection is most likely responsible for the observed coevolution, although identifying the specific mechanism is difficult. Our results suggest that females have evolved a cryptic anatomical mechanism of choice in response to forced extra-pair copulations.     

Cere Colour as a Basis for Extra-pair Preferences of Paired Male Budgerigars (Melopsittacus undulatus: Psittacidae: Aves)

Male budgerigars may be limited in the time they have available to pursue extra-pair copulations because of conflicts with other reproductive behaviour. If males could selectively court only immediately fertilizable extra-pair females they should do so. The cere colour of a female budgerigar may be used as a cue to her reproductive readiness. We experimentally tested the hypothesis that males prefer females with dark ceres, which are indicative of developed ovaries, over females with light-coloured ceres, characteristic of birds with undeveloped ovaries. In a pairwise choice experiment between females that had their cere colour artificially manipulated, pair-bonded males were more likely to choose the female with the dark-coloured cere.     

Restrictive mating by females on black grouse leks

In bird species with pair bonds, extra-pair matings could allow females to choose genetically superior males. This is not needed in lekking species because female choice is not constrained by pairing opportunities. However, polyandry has been reported in most lekking species studied so far. Using 12 microsatellite loci, we determined the paternity of 135 broods of black grouse sampled between 2001 and 2005 (970 hatchlings and 811 adult birds genotyped). The paternity assignments were combined to lek observations to investigate the mating behaviour of black grouse females. About 10% of the matings seemed to take place with males displaying solitarily. Forty per cent of the copulations between males displaying on the studied leks and radio-tagged females were not recorded. This was due to difficulties in identifying the females and because our observations did not cover all the possible time for matings. However, females of the undetected copulations had chosen males that were already known to be successful on the leks. There was a strong consistency between the observations and true paternity, even when the copulation was disturbed by a neighbouring male. Multiple mating and multiple paternities were rare. We can now confidently ascertain that most females mate only once with one male for the whole clutch. This mating behaviour requires that a single insemination is sufficient to fertilize a clutch and that females can determine whether the sperm has been successfully transferred. Grouse Tetraoninae with many lekking species may be the only bird taxon that has evolved these traits.     

Strategic allocation of ejaculates by male Adélie penguins

Sperm competition theory suggests that males should strategically allocate sperm to those females that will bring them the best possible genetic returns. Although males of a number of species of insects and fishes have been shown to allocate sperm strategically, we provide, to our knowledge, the first evidence that an avian species is also capable of allocating ejaculates. Male Adélie penguins (Pygoscelis adeliae) are more likely to transfer sperm during extra-pair copulations (EPCs) than during pair copulations. We investigated the question of how males allocate ejaculates within the constraints of limited sperm availability and found (i) that males that engaged in EPC attempts ejaculated less often when copulating with their social partner than males that made no EPC attempts, and (ii) that there was no difference between males that were involved in failed EPC attempts and those that were involved in successful EPCs in the proportion of copulations that resulted in sperm transfer. These results indicate that males achieve strategic allocation of sperm within the constraints of limited sperm availability by withholding ejaculates from their social partners.     

Explicit experimental evidence for the role of mate guarding in minimizing loss of paternity in the Seychelles warbler

Extra-pair copulations (EPCs) (copulations outside the pair bond) resulting in extra-pair fertilizations (EPFs) are widespread in birds. To increase reproductive success, males should not only seek EPCs, but also prevent their females from having EPFs. Male Seychelles warblers (Acrocephalus sechellensis) follow their partner closely during the period when these females are most receptive (fertile period). The Seychelles warbler is the first species to offer explicit experimental evidence that mate guarding functions as paternity guarding: in territories where free-living males were induced to stop mate guarding during the pair female''s fertile period, the rates of intrusions by other males and successful EPCs (male mounting female) were significantly higher than those observed in the control group and in the absence of mate guarding the frequency of successful EPCs increased significantly with local male density. Male warblers do not assure their paternity through frequent copulations to devalue any sperm from other males: males do not copulate with their partners immediately following a successful EPC obtained by their partners, the frequency of successful within-pair copulations does not increase with the frequency of successful EPCs and females initiate all successful copulations and are capable of resisting copulation attempts.     

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.     

Extra-pair paternity in the strongly monogamous Wandering Albatross Diomedea exulans has no apparent benefits for females

Although 92% of avian species are socially monogamous, extra-pair copulation (EPC), resulting in extra-pair paternity (EPP), is a common reproductive strategy in birds. Among seabirds, in which the rate of social monogamy reaches 100%, Procellariiformes (albatrosses and petrels) show low EPP rates, with the noticeable exception of the only albatross investigated in this regard, the Waved Albatross Phoebastria irrorata . This species, in which forced copulations are known to occur, showed a surprisingly high rate of EPP (25% of chicks). We investigate here EPP rates in another albatross species, the Wandering Albatross Diomedea exulans , subject to a demographic survey conducted for 38 years. We combined data on pair bonds with analysis of ten microsatellite loci and found that 10.7% of 75 chicks had an extra-pair sire. Although there was some evidence for inbreeding avoidance, within-pair and extra-pair chicks showed similar levels of heterozygosity, and the incidence of EPP was independent of age, experience or past reproductive success. Hence, we found no evidence that females benefit from EPCs. Owing to the male-biased sex ratio in adults, widowed and divorced males required more time to find a new mate (+28 and +72%, respectively) than did females. Combined with high sexual size dimorphism, this phenomenon might promote the forced copulations observed in this species. Our data therefore suggest that EPC is beneficial to unpaired males but occurs at random in females, consistent with the hypothesis that EPP results solely from forced EPCs. However, the importance of the latter for EPP and the part played by solitary males require further investigation.     

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.     

Female ground tits prefer relatives as extra‐pair partners: driven by kin‐selection?

Socially monogamous female birds routinely mate with males outside the pair bond. Three alternative hypotheses consider genetic benefits as the major driver behind the female strategy. The inbreeding avoidance hypothesis predicts that females paired with closely related males should seek copulations with distantly related extra-pair partners to avoid fitness loss from inbreeding depression; the outbreeding avoidance hypothesis predicts the opposite; the kin-selection hypothesis suggests that regardless of social mate relatedness, females should give related males extra-pair fertilization opportunities to gain inclusive fitness if the costs from inbreeding are minor. We test these hypotheses with a facultative cooperative breeder, the ground tit (Parus humilis). Social pairs of ground tits formed randomly with respect to genetic relatedness. In both bi-parental and cooperative groups, a female's engaging in extra-pair mating was independent of relatedness to her social mate; however, females preferred extra-pair sires to which they were more related than to their social mates. Moreover, females had higher relatedness with either their extra-group extra-pair sires in both bi-parental and cooperative groups, or within-group helper sires in cooperative groups, than expected by chance. When more than one potential extra-pair partner was available around a female's nest, she tended to select a relative. There was no indication of fitness reduction from extra-pair mating, which occurred at an intermediate level of inbreeding. These data support the kin-selection hypothesis, although there might be alternative nongenetic reasons associated with the extra-pair mating preference. Our finding offers a new explanation for why female birds pursue extra-pair mating. It also may broaden our understanding of the role of kin-selection in the evolution of cooperative society.