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.     

Extrapair paternity in relation to sexual ornamentation, arrival date, and condition in a migratory bird

We tested the novel hypothesis that arrival date in migratorybirds represents a reliable indicator of male quality that canbe used by females as a cue in extrapair mating decisions. Secondarysexual characters are often condition-dependent, and competitionfor early arrival leads to condition-dependent migration. Hence,both secondary sexual characters and arrival date are predictedto be condition-dependent indicators of male phenotypic quality.We studied the relationship between expression of a secondarysexual character, arrival date, and condition, respectively,and extrapair paternity in a Spanish population of barn swallows,Hirundo rustica. By using microsatellite markers to determinepaternity, we showed that 17.8% of all offspring (N = 674) and32.4% of all broods (N = 170) were due to extrapair paternity.Quasi-parasitism (in which the male nest owner fathered theoffspring, but the eggs were laid by another female) occurredin 2.6% of all nestlings and 2.9% of all broods. Individualswere consistent in the frequency of extrapair paternity amongfirst, second, and third broods. Males with long outermost tailfeathers, arriving early and in prime body condition, had littleextrapair paternity in their nests. This was also the case whencontrolling for the confounding effects of male age. Partialcorrelation analysis was used to investigate the direct andindirect effects of tail length, arrival date, and body conditionon extrapair paternity. Body condition accounted for most ofthe variance in extrapair paternity, whereas tail length andarrival date accounted for a smaller proportion of the variance.Body condition was strongly correlated with tail length andarrival date. However, because females cannot directly assesscondition or arrival date (males arrive before females), femalesmay obtain an indirect measure of condition and migration abilityfrom tail length and other phenotypic traits of males. Thissuggests that extrapair paternity depends on the effects ofcondition, through its indirect effects on arrival date, taillength, and other variables.     

Extrapair paternity and egg hatchability in tree swallows: evidence for the genetic compatibility hypothesis?

Tree swallows (Tachycineta bicolor) show one of the highestlevels of extrapair paternity in birds, and there is evidencethat females have control over who fathers their offspring.However, it is unclear which benefits female tree swallows obtainfrom mating with multiple males. Using microsatellite DNA fingerprinting,we studied extrapair paternity in relation to nesting successand male, female, and offspring characteristics. More than 70%of all nests contained extrapair young, and more than half ofall offspring were extrapair. Within broods, the extrapair youngwere often fathered by several males. Despite screening allresident and some floater males, we could identify the biologicalfather of only 21% of all extrapair offspring. All identifiedextrapair males were close neighbors. Extrapair males did notdiffer from within-pair males in any of the measured characteristics,except that the former had larger cloacal protuberances than thelatter. Extrapair males were equally successful in gaining paternityin their own broods as males that did not father extra young.In nests with mixed paternity, extrapair young did not differfrom within-pair young in body size or mass. However, nestswith extrapair young had higher hatching success than nestswithout extrapair young. All examined unhatched eggs were fertilizedand thus hatch failure resulted from embryo mortality. The availabledata are in accordance with the genetic diversity and the geneticcompatibility hypothesis, but not with the good genes hypothesis.     

No evidence for adjustment of sex allocation in relation to paternal ornamentation and paternity in barn swallows

Sex allocation theory predicts that parents should adjust investment in sons and daughters according to relative fitness of differently sexed offspring. In species with female preference for highly ornamented males, one advantage potentially accruing to parents from investing more in sons of the most ornamented males is that male offspring will inherit characters ensuring sexual attractiveness or high-quality genes, if ornaments honestly reveal male genetic quality. Furthermore, in species where extra-pair fertilizations occur, offspring sired by an extra-pair male are expected to more frequently be male than those of the legitimate male if the latter is of lower quality than the extra-pair male. We investigated adjustment of sex ratio of offspring in relation to ornamentation of the extra-pair and the social mate of females by direct manipulation of tails of male barn swallows Hirundo rustica . Molecular sexing of the offspring was performed using the W chromosome-linked avian chromo-helicase-DNA-binding protein (CHD) gene while paternity assessment was conducted by typing of hypervariable microsatellite loci. Extra-pair offspring sex ratio was not affected by ornamentation of their biological fathers relative to the experimental ornamentation of the parental male. Experimental ornamentation of the parental males did not affect the sex ratio of nestlings in their broods. Female barn swallows might be unable to bias offspring sex ratio at hatching according to the quality of the biological father. Alternatively, fitness benefits in terms of sexual attractiveness of sons might be balanced by the cost of compensating for little parental care provided by highly ornamented parental males, if sons are more costly to rear than daughters, or the advantage of producing more daughters, if males with large ornaments contribute differentially more to the viability of daughters than sons.     

Symmetrical male sexual ornaments, paternal care, and offspring quality

Simultaneous manipulation of tail length and tail asymmetryin male barn swallows (Hirundo rustica) has revealed that femalesprefer maJes with both long and symmetrical tail ornaments overmales with short and asymmetrical ornaments. Fluctuating asymmetryin tail length has a negative effect on the maneuvering abilityof male barn swallows, and females may prefer males with symmetricaltail ornaments because they thereby acquire more direct fitnessbenefits in terms of paternal care. The least preferred maleswith short tails with high asymmetry performed an absolutelyand relatively larger share of feeding of nestlings than themost preferred males. However, the combined feeding rate ofthe pair was not statistically significantly different betweentreatment groups. Fully grown tarsus length and body mass ofoffspring on day 15 did not differ between treatments. Theseresults indicate that females do not prefer males with symmetricaltail ornaments because such males contribute a relatively orabsolutely larger share of parental duties. Although these resultsdo not explain the basis of female choice for long and symmetricaltails, the results are consistent with a hypothesis that femalesof species with biparental care should invest differentiallyin their offspring relative to the quality of their mates. Theresults are also consistent with a hypothesis that preferredmales have access to mates with superior parenting abilities     

Extrapair paternity in the Hoopoe Upupa epops: an exploration of the influence of interactions between breeding pairs, non-pair males and strophe length

Previous studies of the Hoopoe Upupa epops have shown that the strophe length of male songs influences female mate choice, and is correlated with female reproductive rates and male production of fledglings in the male’s own brood. However, frequent interactions between breeding pairs and non‐pair males suggests that extrapair copulations could occur and could affect the real number of fledglings sired by males, and therefore the relationship between strophe length and breeding success. Here we analyse the incidence of interactions between breeding pairs and non‐pair males, and of extrapair paternity, the interrelation of these parameters, the influence of male strophe length on them, and whether extrapair fertilizations affect the correlation between strophe length and breeding success of males, in a colour‐ringed population of Hoopoes in south‐eastern Spain. Multilocus DNA‐fingerprinting revealed that 10% of the broods contained offspring sired by extrapair males, representing 7.7% of the chicks. However, the interactions between pairs and non‐pair males were more frequent, with more than 25% of broods being visited by non‐pair males, and about 10% being helped (fed or defended) by males other than the nest owner. Most of these relationships were apparently attempts by visitor males to obtain copulations with paired females, or to obtain access to such females or nests in future breeding attempts. However, there was no significant link between the detection of interactions with alien males in a nest and the occurrence of extrapair paternity in it, indeed extrapair paternity was found in only 30% of the nests with interactions, and therefore the detection of visits or helping by non‐pair males cannot be considered evidence of extrapair paternity in visited or helped broods. Males that sang with long strophes never suffered losses of paternity within their broods, while 25% of males that sang with short strophes did. However, these differences were not significant. Nevertheless, strophe length of males was significantly positively correlated with per brood and seasonal production of fledglings after accounting for losses of paternity within their own broods.     

THE EVOLUTION OF PLUMAGE BRIGHTNESS IN BIRDS IS RELATED TO EXTRAPAIR PATERNITY

A positive association between plumage brightness of male birds and the degree of polygyny may be the result of sexual selection. Although most birds have a socially monogamous mating system, recent paternity analyses show that many offspring are fathered by nonmates. Extrapair paternity arises from extrapair copulations which are frequently initiated by females. Not all females will be able to mate with a male of the preferred phenotype, because of the mating decisions of earlier paired females; extrapair copulations may be a means for females to adjust their precopulation mate choice. We use two comparative analyses (standardized linear contrasts and pairwise comparisons between closely related taxa) to test the idea that male plumage brightness is related to extrapair paternity. Brightness of male plumage and sexual dimorphism in brightness were positively associated with high levels of extrapair paternity, even when potentially confounding variables were controlled statistically. This association between male brightness and extrapair paternity was considerably stronger than the association between male brightness and the degree of polygyny. Cuckoldry thus forms an important component of sexual selection in birds.     

Survival of extrapair and within-pair young in tree swallows

In monogamous species, it is generally accepted that males seekextrapair matings to increase their reproductive success withoutadditional parental investment; however, the benefits of extrapairmatings to females are much less clear. One possibility isthat females obtain genes for enhanced offspring viabilityfrom the extrapair sires. If this is the case, then the increasedviability of extrapair young may be evident throughout the periodof embryonic development as well as later in life. Tree swallows(Tachycineta bicolor) have one of the highest known levelsof extrapair mating in birds, and females have substantialcontrol over the paternity of their offspring. We used moleculartechniques to determine the parentage of nestlings and unhatchedembryos to examine the possibility that female tree swallowsgain viability benefits for their extrapair offspring. Althoughboth extrapair paternity and mortality of embryos and nestlingswere high (89% and 54% of broods respectively), we found nodifference in the viability of within-pair and extrapair youngprior to fledging. In addition, extrapair young were not morelikely to be male. There was no bias in the sex of young atfledging, but unhatched embryos were more likely to be male.Our results do not support the idea that female tree swallowsengage in extrapair mating to increase offspring viability,at least early in life.     

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

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

The function of extrapair paternity in blue tits and great tits: good genes or fertility insurance?

DNA fingerprinting of an island population of blue tits andgreat tits in southeast Norway revealed that extrapair paternityaccounted for 36% (17/47) and 27% (15/55) of broods and for7% (31/466) and 8% (33/408) of young in the two species, respectively.Cuckolded males did not differ from noncuckolded males withrespect to morphology, age, or survival. There was no seasonalpattern in the frequency of extrapair paternity, and males showedno individual consistency in paternity loss over multiple broods.Extrapair offspring did not grow faster, they did not fledgewith a higher body mass, and they did not show a higher localsurvival rate than their half siblings. Hence, there was noevidence of any association between extrapair paternity andmale phenotypic or genotypic quality. Extrapair offspring wererandomly distributed among broods, with the only exceptionsof one blue tit and two great tit broods in which all young(six to nine) were sired by an extrapair male. This patternis best explained by a small proportion of males (2%–4%)being infertile and by most females performing a few extrapaircopulations as insurance against laying infertile eggs. We concludethat the results suggest a role for fertility insurance butthat alternative functional explanations to extrapair paternityin these populations cannot yet be ruled out.     

Male "mixed" reproductive strategies in biparental species: Trivers was probably right, but why?

Trivers proposed that, if parental care by both sexes is advantageous, males should practice a "mixed" strategy of seeking extrapair copulations, while restricting their parental investment to offspring of social mates. We explore circumstances under which males should limit their parental care in the predicted manner. We find that Trivers's "mixed" strategy will generally be evolutionarily stable so long as either socially monogamous or polygynous males usually sire more offspring per brood from a social mate than they typically sire in broods of extrapair mates. Polygynous males should spread investment across their home nests unless the expected number of chicks sired in them differs widely. Whether polygynous males should restrict paternal care to social mates' offspring hinges additionally on resident male investment in broods containing extrapair young: if resident males contribute minimally, some investment by a polygynous extrapair male becomes more advantageous. Recently reviewed data on extrapair fertilization distributions within monogamous and polygynous passerines suggest that extrapair offspring often predominate numerically within their broods, consistent with sperm expenditure theory. Nevertheless, most species conform to the model's criterion regarding relative parentage levels in broods of social versus extrapair mates. Patterns of extrapair parentage thus appear sufficient to stabilize biparental care systems.     

Parentage in the cooperative breeding system of long-tailed tits, Aegithalos caudatus

In cooperatively breeding birds multiple maternity and paternity of broods is not uncommon, reproduction often being shared among group members as well as with extragroup members. We investigated the extent of extrapair paternity and intraspecific brood parasitism in a population of cooperatively breeding long-tailed tits. Our aim was to determine the frequency and cause of mixed parentage and to investigate whether shared maternity or paternity was associated with decisions made by helpers. Genetic analyses using eight microsatellite loci showed that extrapair paternity was low (2.4-6.9% of nestlings in 16-29% of broods), and that intraspecific brood parasitism was negligible. Mate switching and extrapair copulations were both observed, but mate switching was not responsible for the mixed paternity we recorded. Some extrapair offspring were assigned to males that became helpers at the nest containing their extrapair young, but these males were also close neighbours of the cuckolded males and so were the most likely males to gain extrapair paternity. There was no evidence that the existence of a direct reproductive stake in a brood played an important role in the helping decisions of either male or female helpers. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Experimental manipulation of tail length in female barn swallows (Hirundo rustica) affects their future reproductive success

Previous studies have shown no significant effect of experimentaltail length manipulation in female barn swallows (Hirundo rustica)at the beginning of a breeding season on reproductive successor behavior during that breeding season. In the present study,we investigate if tail length manipulation had any effect onreproductive performance the following year, the so-called long-termeffect, in contrast to the short-term effects already studied.We found that females with experimentally elongated externaltail feathers at the beginning of a breeding season producedless offspring during the breeding season the following yearthan did females with shortened or unmanipulated tails. Theseresults suggest that tail elongation caused flight deficienciesthat deteriorated the condition of females and eventually reducedreproductive success. The finding of long-term effects but nosignificant short-term effects for female tail elongation suggeststhat female barn swallows have the ability to adjust immediateparental investment. Detrimental effects of long tails in femalesin terms of decreased reproductive success might explain whyfemale tails are not as long as those of males. Finally, femalesmated to long-tailed (sexually attractive) males decreased theirreproductive success the following year more than did femalesmated to short-tailed males, possibly owing to differentialparental effort causing a deterioration of their condition.     

Experimental manipulation of tail ornament size affects the hematocrit of male barn swallows (Hirundo rustica)

Ornamental tail feathers of male barn swallows (Hirundo rustica) confer an advantage in sexual selection because long-tailed males are preferred by females. However, the size of tail ornaments exceeds the natural selection optimum and males are predicted to pay an energetic cost for flying, directly related to tail length. An increase in hematocrit is an adaptive response to enhance oxygen uptake, for example during periods of intense locomotory activity. In this study, we analyzed the effect of experimental manipulation of tail length on the hematocrit of male barn swallows from an Italian and a Spanish population. We predicted that the natural decrease in hematocrit during the breeding season would be reduced by experimental elongation and enhanced by experimental shortening of tail ornaments. The results showed that the decrease in hematocrit was significantly different among tail treatments, and tail-elongated males had the smallest hematocrit reduction. In Italy, the hematocrit of tail-elongated males did not change after tail manipulation, while that of two control groups and tail-shortened males decreased. A comparatively high hematocrit in males with experimentally enlarged tail ornaments may be a response to increased energetic requirements and, hence, to oxygen demands for flying imposed by their tail morphology. Received: 22 June 1996 / Accepted: 23 October 1996     

Female Cape sugarbirds (Promerops cafer) modify egg investment both for extra‐pair mates and for male tail length

The differential allocation hypothesis predicts that females should invest more in reproduction when paired with attractive males. We measured egg volume in Cape sugarbirds (Promerops cafer), a sexually dimorphic passerine, in relation to paternity of the offspring and in response to an experimental tail length treatment. We manipulated tail length, after pair formation, but before egg laying: males had their tails either shortened or left unmanipulated. Our manipulation was designed to affect female allocation in a particular breeding attempt rather than long‐term mate choice: males with shortened tails would appear to be signalling at a lower level than they should given their quality. We found that egg volume was smaller in the nests of males with experimentally shortened tails but larger when the offspring were the result of extra‐pair matings. Both these findings are consistent with the differential allocation hypothesis. We suggest that tail length may be used by females as a cue for mate quality, eliciting reduced female investment when breeding with social mates; and with males with shortened tails.     

DIFFERENTIAL COSTS OF A SECONDARY SEXUAL CHARACTER: AN EXPERIMENTAL TEST OF THE HANDICAP PRINCIPLE

The evolution of reliable signaling can be explained by the handicap principle, which assumes that (1) the cost of a signal guarantees its reliability, and (2) cheating is prevented because the cost of a unit of display is greater for low-quality than for high-quality individuals. A test of these two assumptions was performed using manipulations of the length of the outermost tail feathers of male barn swallows Hirundo rustica, a trait currently subject to a directional female mate preference. We found that survival decreased with tail elongation and increased with tail shortening of males, supporting the assumption that the secondary sexual character is costly. Naturally long-tailed males were better able to survive with an elongated tail, whereas naturally short-tailed males improved their survival following tail shortening. This observation supports the second assumption of a differential cost of a signal. One mechanism imposing differential costs on sexually signaling barn swallows is foraging. Males with elongated tails captured smaller, less profitable Diptera, whereas males with shortened tails captured large, profitable prey items. The conditions for reliable sexual signaling by the tail ornament of male barn swallows are thus fulfilled.     

Extrapair paternity in the blue tit (Parus caeruleus) : female choice, male charateristics, and offspring quality

Extrapair paternity is common in many birds, and it is now generallyaccepted that female choice plays an important role. However,die benefits that females obtain from extrapair paternity aremuch less dear. To test the hypothesis that females obtain indirectfitness benefits, we studied paternity in a blue tit populationover 4 years. Extrapair paternity occurred in 31-47% of allnests and accounted for 11-14% of all offspring. Most malesthat fathered extrapair young did not lose paternity themselves,males never "exchanged" paternity, and within nests the extrapairoffspring were usually fathered by a single male. Comparisonsbetween males that did and did not lose paternity and pairwisecomparisons between the extrapair male(s) and the within-pairmale showed that successful males had longer tarsi and sangon average longer strophes during the dawn chorus. Successfulmales weighed less (relative to their size) during the nettlingstage, but nevertheless they survived better. Male age did notinfluence their likelihood of losing paternity, but extrapairmales were usually older than the within-pair male they cuckolded.Within nests with mixed paternity, extrapair young were morelikely to survive than within-pair young in cases of partialbrood mortality. Our data also suggest that extrapair offspringwere more likely to be males. Because extrapair males were usuallyclose neighbors, male quality should be considered relativeto the quality of the neighbors. Despite this, we found consistencyin female choice over years. Our observations provide supportfor the hypothesis that female blue tits engage in extrapaircopulations to obtain good genes for their offspring.     

Genetic monogamy in the Common Crossbill ( Loxia curvirostra )

Extrapair paternity seems to be common in socially monogamous passerines, but the genetic mating system of most species is currently unknown. Here, we report the first study of paternity in the socially monogamous Common Crossbill (Loxia curvirostra). We found no evidence of extrapair paternity among 96 offspring in 34 examined broods. An upper 95% confidence limit of 3.1% suggests that extrapair fertilizations were truly infrequent in our study population. Common Crossbills thus seem to represent an exception to the rule of extrapair mating among socially monogamous passerine bird species. A potentially important selective pressure preventing promiscuity in Common Crossbills is the harsh environmental conditions experienced during breeding at wintertime, which may increase the importance of paternal care and limit the time available for seeking extrapair copulations.     

Effects of breeding density, synchrony, and experience on extrapair paternity in tree swallows

Breeding density, synchrony, and experience are expected toinfluence the frequency of extrapair paternity in birds. UsingDNA fingerprinting, we examined the effect of these factorson tree swallows nesting at relatively high (grids of nest-boxes)and low (solitary boxes at least 100 m from the nearest neighbor)densities and in relatively synchronous (Alberta) and asynchronous(Ontario) populations in Canada. The mean percentage of extrapairoffspring per nest did not differ significantly between birdsnesting in grids (43%, n = 22 families) and solitary boxes (57%,n = 12 families). Similarly, there was no significant differencein the mean percentage of extrapair offspring per nest betweenrelatively synchronous (60%, n = 12 Alberta families) and asynchronous(41%, n = 22 Ontario families) populations. We also found noconsistent pattern between extrapair paternity and breedingexperience among seven males and seven females examined overtwo to three breeding seasons. Female tree swallows can influencethe fertilization success of extrapair males by active selectionand rejection of copulation partners. We suggest that this abilitylimits the predicted effect of various ecological factors onthe frequency of extrapair paternity     

DNA fingerprinting reveals relation between tail ornaments and cuckoldry in barn swallows, Hirundo rustica

In an experimental study in Denmark, it was previously foundthat male barn swallows (Hirundo rustica) with elongated tailstreamers obtained an apparent fitness advantage through earlierpairing, an increased frequency of second clutches, and highertotal reproductive success per season. In a parallel study offive barn swallow colonies in Ontario, Canada, we also foundthat elongated males paired earlier and thus were apparentlypreferred by females. Now, using DNA fingerprinting on familiesfrom two of those Ontario colonies, we show that five elongatedmales fathered only 59% of the offspring in their nests, whereassix shortened males fathered 96% of their nestlings. Thus, althoughelongated males were clearly preferred by females at the timeof pair formation, tail elongation may have hampered the abilityof a male to guard his mate, resulting in an increase in extrapairfertilizations (EPFs). A significant negative correlation betweenthe number of EPFs and natural tail length in this experimentalstudy also suggests that tail streamer length may reflect malequality. (Behav Ecol 1990; 2: 90–98)