Mate switching and copulation behaviour in King Penguins

Extra‐pair paternity (EPP) in monogamous birds may result from either extra‐pair copulations (EPCs) or mate switching. In this study of King Penguins in South Georgia, we observed no EPCs at all, an effect of very efficient mate guarding. Onshore males fast and need not divert attention to foraging or to defending nest or territory, as this species has neither. However, we found that mate switching was common. On average 38% (range: 29%–56%; three years pooled) of the birds established pair bonds with at least one initial partner before switching to the partner they bred with (i.e. the “pair mate”). Of the observed copulations of 44 studied females, 22% were with initial partners and 78% with the pair mate. This and the high proportion of mate switching suggest that roughly 10% of the females could have received sperm from males other than the pair mate. The average copulation frequency was 0.026 h^?1, resulting in an estimated 8.2 copulations per clutch (which consists of one egg). That more copulations than necessary for fertilisation occur suggests that males try to protect paternity by sperm competition, and that this is a result of the potential for EPP due to mate switching in King Penguins. All observed copulations except one took place between days 13 and 5, with the peak 7.5 days prior to egg‐laying. The birds found their pair mates (often not the same as in the previous year) on average about 10 days before egg‐laying, and always established themselves at the outskirts of the colony about 8 days before egg‐laying. Thus, most copulations occurred around the time the birds joined the colony. We suggest that it is adaptive to obtain a breeding spot early, because the colony will grow and pairs joining later will protect the offspring. Additionally, we suggest that early copulation outside the colony is adaptive because of the risk of failing to fertilise the egg when copulating among aggressive neighbours inside the dense colony. Based on these two arguments we suggest a “safe place hypothesis” to explain the early copulation peak in King Penguins.     

Mate Switching in a Non-monogamous Species? The Case of the Common Quail (Coturnix coturnix)

We investigated the occutrence of mate switching in the common quail, a non-monogamous species with a temporal pair bond but without either male parental care or territoriality. The study was carried out throughout the breeding seasons of 1993–95 in Mas Esplugues (Catalonia, Spain) by monitoring 28 radio-tagged couples and 17 radio-tagged unpaired males. Agonistic interactions between males inside funnel traps containing a female were also recorded. Mate switching within the laying period occurred in 72% of the females, and new partners always had a higher body condition index than old partners. Agonistic interactions inside the funnel traps also showed that successful males had a better body condition index than losers. These results, along with the observed mate-guarding behaviour of females by their partners throughout the laying period, a highly male-biased sex ratio (five males per female), the lack of territoriality of males and the expected difficulties which unmated males experience in finding pairs, suggest that mate switching is not induced by paired males. Moreover, the constant inflow of new males observed throughout the fertile period of the female and the low costs stemming from mate change strongly support the idea that it is paired females who induce mate switching, in order to improve their fitness by mating with the best quality male available at every moment of their fertile period.     

Extra‐pair mating in a socially monogamous and paternal mouth‐brooding cardinalfish

Many vertebrates form monogamous pairs to mate and care for their offspring. However, genetic tools have increasingly shown that offspring often arise from matings outside of the monogamous pair bond. Social monogamy is relatively common in coral reef fishes, but there have been few studies that have confirmed monogamy or extra‐pair reproduction, either for males or for females. Here, long‐term observations and genetic tools were applied to examine the parentage of embryos in a paternally mouth‐brooding cardinalfish, Sphaeramia nematoptera. Paternal care in fishes, such as mouth‐brooding, is thought to be associated with a high degree of confidence in paternity. Two years of observations confirmed that S. nematoptera form long‐term pair bonds within larger groups. However, genetic parentage revealed extra‐pair mating by both sexes. Of 105 broods analysed from 64 males, 30.1% were mothered by a female that was not the partner and 11.5% of broods included eggs from two females. Despite the high paternal investment associated with mouth‐brooding, 7.6% of broods were fertilized by two males. Extra‐pair matings appeared to be opportunistic encounters with individuals from outside the immediate group. We argue that while pair formation contributes to group cohesion, both males and females can maximize lifetime reproductive success by taking advantage of extra‐pair mating opportunities.     

Does competition for nests affect genetic monogamy in Cory's shearwater Calonectris diomedea?

Most bird species are socially monogamous. However, extra‐pair copulations (EPCs), resulting in extra‐pair paternity (EPP), commonly occur. EPCs should allow females to adjust social mate choice and allow males that fail to obtain a nest a chance to avoid missing a breeding season, especially when poor nest supply constrains social mate choice. Procellariiformes (albatrosses and petrels) are socially monogamous seabirds which seldom divorce, even when nest availability constrains social mate choice. In Cory's shearwater Calonectris diomedea, a burrow‐nesting petrel, two studies conducted in the Mediterranean, where competition for nests is weak, detected no EPP. EPP remains to be investigated at localities where competition for nests is much stronger, such as Vila islet, Azores archipelago, Atlantic Ocean. We conducted a genetic (microsatellites) study over two successive years on Vila, involving the breeding pairs of the same 65 nests each year and their single chick. EPPs occurred each year, the overall rate being 11.6%. Coupling genetic analyses to a 7‐year demographic survey provided additional data on pair bonds and competition for nests. Overall, cuckoldry was unrelated to divorce, nest density and inbreeding avoidance, but was more frequent when the social male was small. Nest changes were more costly for males than for females, and some apparently unpaired males attempted to dislodge social males during within‐pair copulations. These results are compatible with the existence of a link between poor nest availability and EPP and confirm that even species considered strongly monogamous can adopt flexible mating strategies.     

Males Benefit from Mating with Outbred Females in Drosophila littoralis: Male Choice for Female Genetic Quality?

The evolution and expression of mate choice behaviour in either sex depends on the sex‐specific combination of mating costs, benefits of choice and constraints on choice. If the benefits of choice are larger for one sex, we would expect that sex to be choosier, assuming that the mating costs and constraints on choice are equal between sexes. Because deliberate inbreeding is a powerful genetic method for experimental manipulation of the quality of study organisms, we tested the effects of both male and female inbreeding on egg and offspring production in Drosophila littoralis. Female inbreeding significantly reduced offspring production (mostly due to lower egg‐to‐adult viability), whereas male inbreeding did not affect offspring production (despite a slight effect of paternal inbreeding on egg‐to‐adult viability). As inbreeding depressed female quality more than male quality, the benefits of mate choice were larger for males than for females. In mate choice experiments, inbreeding did not affect male mating success (measured as a probability to be accepted as a mate in a large group), suggesting that females did not discriminate among inbred and outbred males. In contrast, female mating success was affected by inbreeding, with outbred females having higher mating success than inbred females. This result was not explained by lower activity of inbred females. Our results show that D. littoralis males benefit from mating with outbred females of high genetic quality and suggest adaptive male mate choice for female genetic quality in this species. Thus, patterns of mating success in mate choice trials mirrored the benefits of choice: the sex that benefited more from choice (i.e. males) was more choosy.     

Sexual Isolation Between Drosophila Melanogaster, D. Simulans and D. Mauritiana: Sex and Species Specific Discrimination

The sexual isolation among the related species Drosophila melanogaster, D. simulans and D. mauritiana is asymmetrical. While D. mauritiana males mate well with both D. melanogaster and D. simulans females, females of D. mauritiana discriminate strongly against males of these two species. Similarly, D. simulans males mate with D. melanogaster females but the reciprocal cross is difficult. Interspecific crosses between several populations of the three species were performed to determine if (i) males and females of the same species share a common sexual isolation genetic system, and (ii) males (or females) use the same genetic system to discriminate against females (or males) of the other two species. Results indicate that although differences in male and female isolation depend on the populations tested, the isolation behaviour between a pair of species is highly correlated despite the variations. However, the rank order of the isolation level along the populations was not correlated in both sexes, which suggests that different genes act in male and female sexual isolation. Neither for males nor for females, the isolation behaviour of one species was paralleled in the other two species, which indicates that the genetic systems involved in this trait are species-pair specific. The implications of these results are discussed. This revised version was published online in August 2006 with corrections to the Cover Date.     

Testosterone Reduces Promiscuity of Female Blue Tits (Cyanistes caeruleus): An Experimental Study

In many animal species, extra‐pair copulations (EPCs) are common and can increase fitness in both sexes. In males, EPCs can increase total reproductive output, whereas in females benefits of EPCs can be indirect through improving the genetic quality of their offspring. Males and females of many vertebrates show an increase in levels of the hormone testosterone (T) during the mating period. In males, T plays an important role in regulating mating behaviour including increasing their EPC rate. While much is known about the role of T in male mating behaviour, the role of T in female reproduction remains unclear. To study the influence of T on extra‐pair paternity rates in females in a field setting, we created three experimental groups of female blue tits (Cyanistes caeruleus): treated with either T, flutamide (Flu; an androgen receptor blocker) or empty implants before egg laying. Subsequently, we scored the number of extra‐pair offspring (EPO) in their broods. We also assessed the attractiveness of females treated with either T or Flu to males in mate choice trials in the laboratory. The overall proportion of EPO was lower for the T‐implanted group compared with the control group, whereas Flu had no effect. Given that males did not show a preference for Flu‐ vs. T‐treated females in the mate choice trials, it appears less likely that the reduction in EPO in the T‐implanted females was due to a reduction in their attractiveness. T levels may have negatively influenced EPO rate by affecting female within‐pair and/or extra‐pair mating behaviour. Future behavioural studies should investigate how elevated T levels reduce the number of EPO.     

Coloration,Paternity, and Assortative Mating in Western Bluebirds

Coloration in birds can act as an important sexual signal in males, yet in many species, both sexes display bright colors. Social selection may account for this pattern, with more brightly colored individuals pairing together on the best territories. Mutual mate choice may also explain this, as males investing a great deal of parental care in the offspring should be choosy about their social mates. It is less clear whether this pattern of mate choice can apply to extra‐pair partners as well. We examined western bluebirds (Sialia mexicana) to determine whether more colorful individuals tended to pair with one another, both in social pairs and between females and their extra‐pair partners. Both male and female western bluebirds display both UV‐blue structural plumage and a melanin‐based chestnut breast patch, although females are duller than males. Social pairs mated assortatively with regard to UV‐blue brightness, but not chestnut coloration. There was no evidence that extra‐pair partners mated assortatively, but males with brighter UV‐blue coloration had fewer extra‐pair offspring in their nests. Older males were more successful at siring extra‐pair offspring, despite displaying no differences in coloration compared to younger males. Coloration did not play a role in determining extra‐pair male success. These results suggest that coloration plays a role in the formation of social pairs, but not mate choice for extra‐pair partners.     

Different ornaments signal male health and MHC variation in two populations of a warbler

Male traits that signal health and vigour are used by females to choose better quality mates, but in some cases the male trait selected by females differs among populations. Multiple male traits can be maintained through female mate choice if both traits are equally honest indicators of male quality, but tests of this prediction are rare. By choosing males based on such traits, females could gain direct benefits from males (assistance with parental care), but when females choose extra‐pair mates based on these traits, females gain only male sperm, and potentially indirect genetic benefits for their offspring. In common yellowthroats (Geothylpis trichas), female choice of extra‐pair mates targets two different plumage ornaments: the black mask in a Wisconsin population and the yellow bib in a New York population. Previously, we found that the black mask in Wisconsin is related to greater major histocompatibility complex (MHC) class II variation, which in turn signals better survival and disease resistance. In this study, we examined the signalling function of the yellow bib in New York to test whether it signals the same aspects of male quality as the black mask in Wisconsin. As predicted, we found that the yellow bib in New York is most closely associated with MHC variation, which also signals survival and resistance to blood parasites. Thus, the ornament preferred by females differs between the two populations, but the different ornaments signal similar aspects of male health and genetic quality, specifically information regarding MHC variation and potential indirect genetic benefits to females.     

Mating with sperm-depleted males does not increase female mating frequency in the parasitoid Lariophagus distinguendus

Sexual conflicts due to divergent male and female interests in reproduction are common in parasitic Hymenoptera. The majority of parasitoid females are monandrous, whereas males are able to mate repeatedly. Thus, accepting only a single mate might be costly when females mate with a sperm‐depleted male, which may not transfer a sufficient amount of sperm. In the present study, we investigated the reproductive performance in the parasitoid Lariophagus distinguendus Först. (Hymenoptera: Pteromalidae) and studied whether mating with experimentally sperm‐depleted males increases the tendency of females to remate. Males were able to mate with up to 17 females offered in rapid succession within a 10‐h test period. The resulting female offspring, as an indirect measure of sperm transfer, remained constant during the first six matings and then decreased successively with increasing number of copulations by the males. Experimentally sperm‐depleted males continued to mate even if they transferred only small amounts or no sperm at all. Unlike males, the majority of females mated only once during a 192‐h test period. A second copulation was observed only in a few cases (maximum 16%). The frequency of remating was not influenced by the mating status of the first male the females had copulated with, suggesting that these events are not controlled by sperm deficiency of the females. Furthermore, we investigated male courtship behaviour towards mated females. Male courtship intensity towards mated females decreased with increasing time. However, females that had mated with an experimentally sperm‐depleted male did not elicit stronger or longer‐lasting behavioural responses in courting males than those that had mated with a virgin male. As the observed behaviours in L. distinguendus are known to be elicited by a courtship pheromone, these results suggest that females no longer invest in pheromone biosynthesis after mating (as indicated by ceasing behavioural responses of courting males), irrespective of whether they have received a sufficient amount of sperm or not. We discuss the results with respect to a possible mating strategy of sperm‐depleted males.     

Monogynous Mating Behaviour and its Ecological Basis in the Golden Orb Spider Nephila fenestrata

Males, especially in species where they provide little or no parental investment, usually have high potential reproductive rates and are expected to maximize their fitness by mating with several females. This view is challenged, however, by species in which males provide no parental investment, but nevertheless mate with one female only. Male monogamy (monogyny), associated with an extreme investment in paternity protection, appears to be comparatively common in web‐building spiders, and has recently been subject to experimental and theoretical studies. To date, however, studies approaching this issue from an ecological perspective are rare. Theory predicts that the evolution of a monogynous mating strategy is favoured by a male‐biased sex ratio, but not necessarily by a high mortality risk for mate‐searching males. To test these predictions, we conducted a field study on the golden orb spider Nephila fenestrata, which has a mating system with potentially cannibalistic, polyandrous females, and males that are often functionally sterile after mating with one female only. Based on daily observations of marked individuals, we confirm that, consistent with laboratory findings, monogyny is common in N. fenestrata. Nevertheless, observations of male movements between females raise the possibility that a proportion of males may mate with two females. We show that the sex ratio in our study population is male‐biased, and that males incur only a relatively moderate mortality risk during mate‐search. These findings provide insights into the ecological basis for the evolutionary maintenance of monogyny.     

Differences between the sexes in direction and duration of response to seeing a potential sex partner mate with another

We have shown previously that: (1) female Japanese quail, Coturnix japonica, increase and male Japanese quail decrease their tendencies to affiliate with potential sex partners after seeing them mate, and (2) in both sexes of quail, affiliative preferences and choice of a sex partner are highly correlated. Here we predict that because effects of a prior male's sperm on a second male's probability of fertilizing a female are relatively brief, a male's avoidance of whichever member of a pair of females he has seen mating should be transitory. Conversely, because female quail seek high-quality males as mates and quality is a relatively permanent characteristic, females' preferences between males should remain constant over time. We found, as predicted, that the durations of effects on affiliation of seeing a potential sex partner mate differed in male and female quail. Forty-eight hours after male quail saw a female mate, they no longer avoided her, whereas 48 h after female quail saw a male mate, his attractiveness remained enhanced. We conclude by suggesting that both the direction and the duration of responses of male and female Japanese quail to seeing a member of the other sex mating enhance the fitness of members of each sex. Copyright 2000 The Association for the Study of Animal Behaviour.     

Female mate choice in relation to heterozygosity in Tribolium castaneum

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

Interactive vocal communication at the nest by parent Great Tits Parus major

Although most bird species show monogamous pair bonds and bi‐parental care, little is known of how mated birds coordinate their activities. Whether or not partners communicate with each other to adjust their behaviour remains an open question. During incubation and the first days after hatching, one parent – generally the female – stays in the nest for extended periods, and might depend on acoustic communication to exchange information with its mate outside. The Great Tit Parus major is an interesting study system to investigate intra‐pair communication at the nest because males address songs to their mate while she is in the nest cavity, and females answer the male from the cavity with calls. However, the function of this communication remains unknown. In this study, we recorded the vocalizations and observed the resulting behaviour of Great Tit pairs around the nest at different breeding stages (laying, incubation and chick‐rearing). We observed vocal exchanges (vocalization bouts, alternated on the same tempo, between the female inside the nest and her male outside) in three contexts with different outcomes: (1) the female left the nest, (2) the male entered the box with food, and the female then used specific call types, (3) mates stopped calling but did not leave or enter the nest. The structure of vocal exchanges was globally stable between contexts, but females used calls with an up‐shifted spectrum during exchanges, at the end of which they left the nest or the male entered the nest. Birds vocalized more and at higher tempo during exchanges that ended up in feeding inside the nest. Birds also vocalized more during exchanges taking place during laying – a period of active mate guarding – than during incubation. We conclude that vocal exchanges could signal the females’ need for food and the males’ mate guarding behaviour, and discuss other possible functions of this communication.     

Interspecific Mate Choice Following Cross-fostering in a Mixed Colony of Greylag Geese (Anser anser) and Canada Geese (Branta canadensis). A Study on Development and Persistence of Species Preferences1

The role of early experience in mate choice and species preference of geese was studied in an experiment where young greylag geese (Anser anser) were cross-fostered by Canada geese (Branta canadensis). In two successive years, all eggs from 9 nests of wild Canada geese were removed and replaced by greylag goose eggs. The young greylag geese then followed their Canada goose foster parents on their southward migration in autumn, to return with them in spring. Of 35 returning birds, all 16 females paired with greylag goose males (100%) whereas of 19 males 5 paired with Canada goose females (14%) and the remaining 14 with greylag goose females (74%). The pair bonds generally persisted as long as both birds were present, but after loss of a partner, the remaining bird usually re-mated. Even when this happened several times during the lifetime of a male, the new mate was always a Canada goose female, showing that the males were sexually imprinted to this species. The Canada goose females which had mated with the greylag ganders also remated when widowed, but their new mate could be either a Canada goose or a greylag goose.     

The role of the model in mate‐choice copying in female zebra finches

Previous studies have shown that zebra finch females copy the mate choice of other females by choosing a mate of the same phenotype as the one chosen by another female (model). Little is known about the influence of the model female on the mate choice of the observing female. Therefore, we investigated the role of the model female in mate‐choice copying by manipulating her phenotype. Test females could choose between an unadorned male and an artificially adorned male, that is, wearing a red feather on the forehead. During a 2h observation period, test females could observe a single male in one cage and a male–female pair in another cage. In treatment one, the single male was unadorned and both the male and the female of the pair (model female) were adorned. In treatment two, the single male was adorned, the male of the pair unadorned and the model female adorned. Afterwards, test females could again choose between two new males, one adorned and one unadorned. In treatment one, test females first showed no preference for one of the two males, but avoided adorned males after the observation period. In treatment two, test females lost an initial preference for unadorned males after the observation period. In both treatments, test females did not copy the mate choice of the adorned model female. Adorned model females seemed to have a negative influence on the attractiveness of their mates' phenotype. Test females might have recognised model females as females of a different phenotype within their species which are adapted to different environmental conditions, or even have recognised model females as a female of another species. Our study demonstrates the important role of the model female in the complex public information network in zebra finches.     

Mated pairs of owl monkeys (Aotus nancymaae) exhibit sex differences in response to unfamiliar male and female conspecifics

In socially monogamous species, mate‐guarding could be a reproductive strategy that benefits both males and females, especially when males contribute to parental care. By actively guarding mates, males may reduce their chances of being cuckolded, whereas females that mate‐guard may reduce the likelihood that their mates will desert them or acquire additional mates, and hence limit or reduce paternal care of offspring. Owl monkeys (Aotus spp.) are socially monogamous with biparental care of young and, hence, potential beneficiaries of mate‐guarding. We presented mated pairs of captive owl monkeys (A. nancymaae) with unfamiliar male and female conspecifics, to determine if either member of the pair exhibits intraspecific aggression toward an intruder or stays close to its mate, behaviors indicative of mate‐guarding. Male mates were more responsible for the maintenance of close proximity between mates than females. Male mates also exhibited elevated levels of behavior that signify arousal when presented with a male conspecific. These responses by mated male owl monkeys are consistent with patterns that may help prevent cuckoldry. Am. J. Primatol. 72:942–950, 2010. © 2010 Wiley‐Liss, Inc.     

MHC-associated mating strategies and the importance of overall genetic diversity in an obligate pair-living primate

Mate choice is one of the most important evolutionary mechanisms. Females can improve their fitness by selectively mating with certain males. We studied possible genetic benefits in the obligate pair-living fat-tailed dwarf lemur (Cheirogaleus medius) which maintains life-long pair bonds but has an extremely high rate of extra-pair paternity. Possible mechanisms of female mate choice were investigated by analyzing overall genetic variability (neutral microsatellite marker) as well as a marker of adaptive significance (major histocompatibility complex, MHC-DRB exon 2). As in human medical studies, MHC-alleles were grouped to MHC-supertypes based on similarities in their functional important antigen binding sites. The study indicated that females preferred males both as social and as genetic fathers for their offspring having a higher number of MHC-alleles and MHC-supertypes, a lower overlap with female’s MHC-supertypes as well as a higher genome wide heterozygosity than randomly assigned males. Mutual relatedness had no influence on mate choice. Females engaged in extra-pair mating shared a significant higher number of MHC-supertypes with their social partner than faithful females. As no genetic differences between extra-pair young (EPY) and intra-pair young (IPY) were found, females might engage in extra-pair mating to ‘correct’ for genetic incompatibility. Thus, we found evidence that mate choice is predicted in the first place by the ‘good-genes-as-heterozygosity hypothesis’ whereas the occurrence of extra-pair matings supports the ‘dissassortative mating hypothesis’. To the best of our knowledge this study represents the first investigation of the potential roles of MHC-genes and overall genetic diversity in mate choice and extra-pair partner selection in a natural, free-living population of non-human primates.     

Females of the Cellar Spider Discriminate Against Previous Mates

Mate choice for novel partners should evolve when remating with males of varying genetic quality provides females with fitness‐enhancing benefits. We investigated sequential mate choice for same or novel mating partners in females of the cellar spider Pholcus phalangioides (Pholcidae) to understand what drives female remating in this system. Pholcus phalangioides females are moderately polyandrous and show reluctance to remating, but double‐mated females benefit from a higher oviposition probability compared to single‐mated females. We exposed mated females to either their former (same male) or a novel mating partner and assessed mating success together with courtship and copulatory behaviours in both sexes. We found clear evidence for mate discrimination: females experienced three‐fold higher remating probabilities with novel males, being more often aggressive towards former males and accepting novel males faster in the second than in the first mating trial. The preference for novel males suggests that remating is driven by benefits derived from multiple partners. The low remating rates and the strong last male sperm precedence in this system suggest that mating with novel partners that represent alternative genotypes may be a means for selecting against a former mate of lower quality.     

Are extra‐pair males different from cuckolded males? A case study and a meta‐analytic examination

Traditional models for female extra‐pair matings assume that females benefit indirectly from extra‐pair mating behaviour. Under these so‐called adaptive models, extra‐pair males are hypothesized to have more compatible genotypes, larger body size, exaggerated ornaments or to be older than cuckolded males. Alternatively, (‘nonadaptive’) models that consider female extra‐pair matings to be a by‐product posit that female extra‐pair mating can be maintained even if there is no benefit to females. This could happen if, for example, males gained fitness benefits from extra‐pair mating, while female and male extra‐pair mating behaviours were genetically correlated. Extra‐pair males are also expected to be older and larger if this improves their ability to convince or coerce females to mate. We investigated whether a female's extra‐pair mates differed from her cuckolded mate in both genetic and phenotypic traits by analysing data from an insular house sparrow population. We found that extra‐pair males were older than cuckolded males, consistent with both models. However, in contrast to the expectations from from adaptive models, extra‐pair and cuckolded males were of similar genetic relatedness, and hence expected compatibility, with the female, and had comparable body size and secondary sexual traits. We also updated previous meta‐analyses examining differences between extra‐pair and cuckolded males. The meta‐analytic results matched results from our house sparrow case study. Although we cannot completely exclude indirect benefits for females, nonadaptive models may better explain female extra‐pair matings. These neglected alternative models deserve more research attention, and this should improve our understanding of the evolution of mating systems.