AN EXPERIMENTAL STUDY OF PATERNITY AND TAIL ORNAMENTATION IN THE BARN SWALLOW (HIRUNDO RUSTICA)

Previous studies of the socially monogamous barn swallow (Hirundo rustica) have shown that males that most frequently engage in extrapair copulations and whose partners are least involved in copulations with extrapair males are those with long tail ornaments. In this study, through the use of three highly polymorphic microsatellite markers, we analyze the relationships between length of tail ornaments of male barn swallows and proportion of nestlings fathered in own broods, number of offspring fathered in broods of other pairs, and total number of offspring fathered, using both a correlational and an experimental approach. Consistent with our predictions, we show that males with either naturally long or experimentally elongated tails have higher paternity (proportion of biological offspring in own broods), and they produce more biological offspring during the whole breeding season than males with naturally short or experimentally shortened tails. Males with naturally long tails also had more offspring in extrapair broods than short-tailed males, but the effect of tail manipulation on the number of offspring fathered in extrapair broods, although being in the predicted direction, was not statistically significant. Cuckolded males that did not fertilize extrapair females had smaller postmanipulation tail length than cuckolders. We conclude that there is a causal, positive relationship between male tail length and paternity. Since female barn swallows have extensive control over copulation partners and heritability of tail length is high, this study shows that female choice is a component of selection for larger male ornaments. Benefits from extrapair fertilizations to females may arise because they acquire “good” genes for sexual attractiveness or high viability for their offspring.     

Energetic cost of tail streamers in the barn swallow (Hirundo rustica)

Different hypotheses stress the importance of natural or sexual selection to explain the evolution and maintenance of long outermost tail feathers in the barn swallow (Hirundo rustica). Since energy costs are predicted to arise from tail length manipulation, we measured the daily energy expenditure in three experimental groups (tail-shortened, tail-elongated, and control birds) with the doubly labelled water technique. Though we did not directly measure flight cost, we assumed this to be positively related to daily energy expenditure. Mass independent daily energy expenditure (kJ/mass^0.67 day) average daily metabolic rate (ml CO₂/g h), and water flux (ml H₂O/g day) did not show any significant difference among treatments in either sex. Males had higher values than females for the three parameters. Males with short original tail length experienced a higher water flux than originally long-tailed males. Females that laid more eggs during the breeding season or had heavier broods also showed higher levels of water flux which could imply a higher food intake. Our expectation of finding energetic costs of manipulated tail length in barn swallows with an integrated measure of metabolism was not fulfilled, and we did not find evidence for behavioural changes in the birds involved in the experiment.     

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     

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.     

Female Barn Swallows Gain Indirect but not Direct Benefits through Social Mate Choice

Female mate choice is responsible for the evolution of male secondary sexual ornaments. If male ornamental traits reflect indirect, genetic benefits and/or direct, material benefits to females, choosy females may benefit from their choice, indirectly and/or directly. We examined a breeding population of Japanese barn swallows Hirundo rustica gutturalis to determine whether male tail streamer length reflected indirect and/or direct benefits to females. There was no significant positive relationship between male streamer length and the number of extra-pair young (EPY) sired, suggesting that male tail streamers are not a signal of indirect benefits (i.e. good genes theory). In addition, we found no evidence that males with longer streamers fed their offspring more frequently or sired more within-pair young (WPY). The result indicates that male streamer length probably does not act as a signal of direct benefits. Our finding that the length of tail streamers in Japanese barn swallows plays no role in sexual selection is not consistent with studies on European subspecies, but is consistent with studies on North American subspecies where sexual selection on tail streamer is weak. The present study supports the recent suggestion that the pattern of sexual selection on tail streamer length in barn swallows varies geographically. Instead of tail length, males in better condition sired more EPY and WPY. Males in better condition, however, did not feed their nestling more frequently. These results indicate that females gain indirect benefits but not direct benefits, in terms of feeding of young, on choosing social mates.     

Examining the Cost of Experimentally Imitated Ornaments

Long forked tail ornament in male barn swallows (Hirundo rustica) were suggested to impose a condition‐dependent viability cost ( Møller 1989 ; reviewed in Møller 1994 ; Møller & de Lope 1994 ; Møller et al. 1995 ): long tails impair male flight and foraging ability in terms of mean size of prey captured. In a recent study, we ( Matyjasiak et al. 1999 ) showed such a foraging cost of an experimentally imitated tail ornament in the sand martin (Riparia riparia), which have no tail ornament. We lengthened the tail in females, instead of in males, and thus controlled experimentally for the possible effect of differential allocation of female parental expenditure (differential‐allocation hypothesis, Burley 1986 ). Cuervo (2000) raises important issues in his comments about our paper. He questions the method used in our study ( Matyjasiak et al. 1999 ). He points out that ‘in order to test the cost of flight of an ornament, the trait to be experimentally manipulated has to be an ornament’, and that we should have not only elongated but also shortened tail feathers. Secondly, he suggests that we did not provide, in our article, the exclusive evidence for the handicap model of sexual selection. Thirdly, he disagrees with our suggestion that the results from the barn swallow experiments could be confounded by the differential allocation of female parental expenditure. Here, we outline the areas of agreement and disagreement between Cuervo's critique and our paper. Firstly, we agree with Cuervo regarding the importance of tail shortening in studies of fully developed tail ornaments, which has already been pointed out by other authors ( Thomas & Rowe 1997 ; Evans & Thomas 1997 ). However, shortening of an ornament that is at equilibrium would always produce a decrease in costs. Therefore it will only confirm that an ornament is costly. However, if shortening is done to individuals of various, known condition, it may result in crucial information for distinguishing between hypotheses of sexual selection. We agree that for a character that is not an ornament, as in our experiments, shortening would not give new insights apart from another way of confirming the measures used in the barn swallow studies. However, we disagree with Cuervo's claims of irrelevance of our experiment to the issues of the evolution of signals. We have chosen sand martins as a model species because the shape of its tail resembles that in ancestors of modern tail‐ornamented swallows, from which tail feather elongation under sexual selection may have started ( Matyjasiak et al. 2000 ). Possible scenarios of the early evolution of a tail ornament may be examined by experimentally adding such an ornament, which requires manipulating original, non‐ornamental traits (e.g. Goötmark 1994, 1996 ). We disagree with Cuervo that the existence of traits that may reduce the costs of ornaments (e.g. Møller 1996 ) eliminates the validity of tail manipulation studies in species without ornaments. We believe that such cost‐reducing traits may not have existed during the early stages of evolution of tail ornaments (as well as other sexual traits) but may have developed later, and our experiment may represent such a situation very well. Hence, by imitating the initial development of a forked tail ornament in sand martins, we performed a biologically relevant manipulation. Secondly, we do not state in our paper that we have tested or proved the handicap principle. We only mention in the last paragraph of the Discussion, that our results are consistent with this principle. However, we do admit that mentioning only the handicap hypothesis in the Introduction and Discussion only, and omitting other processes by which costly tail ornaments might arise, was unwarranted, as Cuervo properly argued; this might have left a false impression that our goal was to test the handicap hypothesis. We do believe that we have properly measured the costs of tail elongation, and this was our goal, as stated in the Abstract and in the last paragraph of the Introduction. Nowhere in the paper did we state that we actually aimed to test the differential costs of ornaments that are crucial to the handicap hypothesis. This issue was the objective of a different paper ( Matyjasiak et al. 2000 ) in which we consider conditions important for the early evolution of tail ornaments, with special emphasis on the handicap principle. Thirdly, we are more cautious at interpreting the barn swallow studies and we do not exclude a possibility that differential allocation of parental expenditure can affect the size of prey brought by males. Differential allocation does exist in this species ( Møller 1992 ; de Lope & Møller 1993 ), as shown by the higher feeding rate by females responding to male higher attractiveness (longer tails). We believe that even though simple logical, intuitive reasoning may suggest that prey size should be unaffected by a differential allocation mechanism, it is not just reasoning but empirical proof that is needed here. Because there was no proof for a lack of the effect of differential allocation on the size of prey, we thought of an independent way of illustrating the costs of tail elongation in swallows, using a species without possible differential allocation effects. We thought that if we obtained results confirming the barn swallow studies by Møller and collaborators, we could help in validating the measures of tail elongation costs used in those studies. This was possible using the sand martin females for reasons discussed in the paper, all of which point to the lack of any differential allocation effects in this species. From this point of view, experimentally coupling tail elongation with tail shortening in our study appears unnecessary. Even though, as argued by Cuervo (2000) , it seems likely that the prey size in male swallows is unaffected by a change in feeding rate of females in response to male attractiveness (an assumption inherent in the barn swallow studies), another scenario is also possible. Imagine a female that has increased the amount of food for nestlings, in response to increased sexual attractiveness of her male partner due to experimental elongation of his tail. In such a situation the male has been relieved from a considerable duty of providing the young with a large amount of food. Hence, it is possible that such a male shifts from maximising the energy brought to nestlings per unit time (i.e. maximising foraging rate) to the criterion of obtaining the daily energetic needs at the least expense (i.e. minimising foraging costs). Such shifts may lead to including some non‐preferred, small insects that can be captured quickly and inexpensively in terms of energy, because it does not require the use of expensive flapping flight, which is required to capture larger, preferred insects ( Waugh 1978 ; Bryant & Turner 1982 ; Turner 1980, 1982 ). By including more small insects in their catch at the expense of a reduced foraging rate, attractive males could save energy for future use. Barn swallows appear to compromise between maximising their foraging efficiency (maximising foraging gains per costs) and maximising energy intake per unit time (see fig. 5.7 in Turner 1980 and table IV in Turner 1982 ). Hence, if sexually attractive males aim at minimising foraging costs rather than maximising foraging rate for nestlings, then we cannot exclude the possibility that this may result in smaller insects being caught, on average, by males with experimentally longer tails. By a similar reasoning, it is theoretically possible that differential allocation effects could lead to larger mean prey size in males with experimentally shortened tails ‐ an effect actually shown in the barn swallow studies ( de Lope & Møller 1993 ; Møller & de Lope 1994 ; Møller et al. 1995 ). Hence, whether shortening, elongating or performing both experimental manipulations, in our view we cannot be entirely sure whether the results are affected by differential allocation. This was sufficient motivation for us to investigate, independently, the usefulness of the change in prey size as an indicator of foraging costs due to elongated tails. In contrast to Cuervo's opinion, we believe that our results are relevant to the issues important for the evolution of forked tail ornaments. We have measured the costs of a character that imitates the hypothetical early stages of the evolution of sexual ornaments, and we may use these results to discuss the early evolution of sexual ornaments (see Matyjasiak et al. 2000 ). We also confirmed the validity of measures of tail elongation costs used in the barn swallow studies.     

Sexual ornamentation and immunocompetence in the barn swallow

The handicap hypothesis of honest signaling suggests that secondarysexual characters reliably reflect phenotypic or genotypic qualityof signalers. This hypothesis is based on the assumptions thatsignals are costly to produce and/or maintain and the cost ofa given level of signaling is higher for low quality than forhigh quality signalers. We tested these assumptions in a fieldexperiment in which the size of a secondary sexual character[tail length in male barn swallows (Hirundo rustica)] was experimentallymanipulated. Males were randomly assigned to tail elongation,tail shortening, or two control treatments (tail manipulation,or just capture, ringing, and handling). Male barn swallowswere challenged with an injection of sheep red blood cells,and blood was sampled on the day of first capture and after3 to 4 weeks for determination of concentrations of gamma-globulins.Tail-elongated males did not increase levels of gamma-globulinswhile males of the other three groups demonstrated increases.Analyses of variation in gamma-globulins within treatment groupsrevealed a positive correlation between gamma-globulins andoriginal tail length among males with elongated tails. Theseresults suggest that tail length imposes an immu-nocompetencecost on males, and that males with naturally long tails aredifferentially better able to cope with this cost.     

Sexual selection and tail streamers in the barn swallow

The functional significance of elongated, narrow tips of the tail feathers of certain birds, so-called tail streamers, has recently been discussed from an aerodynamic point of view, and the effects of sexual selection on such traits have been questioned. We review our long-term field studies using observational and experimental approaches to investigate natural and sexual selection in the barn swallow, Hirundo rustica, which has sexually size-dimorphic outermost tail feathers. Experimental manipulation of the length of the outermost tail feathers has demonstrated sexual selection advantages of tail elongation and disadvantages of tail shortening, with opposite effects for natural selection in terms of foraging efficiency, haematocrit and survival. These findings are contrary to the prediction of a general deterioration from both shortening and elongation, if the tail trait was determined solely by its effects on aerodynamic efficiency and flight manoeuvrability. Patterns of sexual selection in manipulated birds conform with patterns in unmanipulated birds, and selection differentials for different components of sexual selection in manipulated birds are strongly positively correlated with differentials in unmanipulated birds. Age and sex differences in tail length, and geographical patterns of sexual size dimorphism, are also consistent with sexual selection theory, but inconsistent with a purely natural selection advantage of long outermost tail feathers in male barn swallows.     

Hidden treatments in ecological experiments: re-evaluating the ecosystem function of biodiversity

Interactions between biotic and abiotic processes complicate the design and interpretation of ecological experiments. Separating causality from simple correlation requires distinguishing among experimental treatments, experimental responses, and the many processes and properties that are correlated with either the treatments or the responses, or both. When an experimental manipulation has multiple components, but only one of them is identified as the experimental treatment, erroneous conclusions about cause and effect relationships are likely because the actual cause of any observed response may be ignored in the interpretation of the experimental results. This unrecognized cause of an observed response can be considered a “hidden treatment.” Three types of hidden treatments are potential problems in biodiversity experiments: (1) abiotic conditions, such as resource levels, or biotic conditions, such as predation, which are intentionally or unintentionally altered in order to create differences in species numbers for “diversity” treatments; (2) non-random selection of species with particular attributes that produce treatment differences that exceed those due to “diversity” alone; and (3) the increased statistical probability of including a species with a dominant negative or positive effect (e.g., dense shade, or nitrogen fixation) in randomly selected groups of species of increasing number or “diversity.” In each of these cases, treatment responses that are actually the result of the “hidden treatment” may be inadvertently attributed to variation in species diversity. Case studies re-evaluating three different types of biodiversity experiments demonstrate that the increases found in such ecosystem properties as productivity, nutrient use efficiency, and stability (all of which were attributed to higher levels of species diversity) were actually caused by “hidden treatments” that altered plant biomass and productivity. Received: 16 December 1996 / Accepted: 2 March 1997     

Uninformative exaggeration of male sexual ornaments in barn swallows

Models of sexual selection suggest that mate-choice preferences are favored because differences between males in their degree of ornamental exaggeration convey useful information about the direct or indirect benefits they have to offer [1-5]. Such arguments assume that variation in male ornament size can be attributed to variation in the degree of sexually selected exaggeration. We provide the first test of this assumption by conducting tail-length experiments in male barn swallows. Over the last twenty years, a large amount of work has shown that female barn swallows are influenced by male tail length when choosing a mate [6-12]. Recent experiments have shown that a combination of natural and sexual selection results in the elongated tail streamer--a tail that is on average across the population about 12 mm (approximately 10%) longer than the aerodynamic optimum [13, 14]. We show that the aerodynamically optimal tail length varies significantly between males, whereas the extent of streamer elongation beyond the optimum does not. Similarly, the aerodynamically optimal tail length significantly predicts observed tail length and conveys information about flight performance, whereas the extent of sexually selected exaggeration of streamer length does not. Therefore, contrary to handicap models of sexual selection, the sexually selected exaggeration of this trait provides females with little information about any aspect of mate quality     

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)     

Experimental manipulation of female tail length did not cause differential allocation by males in the barn swallow

The evolution and maintenance of female ornamentation has attracted increasing attention, because the previous explanation, that is a non‐functional copy of functional male ornamentation, seems insufficient to explain female ornamentation. A post‐mating sexual selection, differential allocation, may be more common than pre‐mating sexual selection, but few studies have investigated differential allocation by males. Here, we studied differential allocation of incubation investment by male barn swallows Hirundo rustica, a model species for the study of sexual selection, because our previous correlative study demonstrated a positive relationship between female tail length and male incubation investment. We manipulated the length of the outermost tail feathers in females after clutch completion and examined whether males adjust incubation investment according to female ornamentation. Because extra‐pair paternity is virtually absent in the study population, we were able to study differential allocation based on the tradeoff between current and future reproductive investments, rather than the tradeoff between current paternal investment and additional mating effort. The experimental treatment had no significant effect on male nest attentiveness, whereas female tail length before manipulation predicted male nest attentiveness. The observed pattern is consistent with differential access; that is, well‐ornamented individuals have greater access to mates with high reproductive (parental) ability, rather than differential allocation during incubation. Alternatively, males can directly assess eggs in their nests, and thus, as seen in other species, males might adjust their incubation investment based on the egg characteristics of long‐tailed females.     

Population differences in density and resource allocation of ornamental tail feathers in the barn swallow

Many organisms show well‐defined latitudinal clines in morphology, which appear to be caused by spatially varying natural selection, resulting in different optimal phenotypes in each location. Such spatial variability raises an interesting question, with different prospects for the action of sexual selection on characters that have a dual purpose, such as locomotion and sexual attraction. The outermost tail feathers of barn swallows (Hirundo rustica) represent one such character, and their evolution has been a classic model subject to intense debate. In the present study, we examined individuals from four European populations to analyze geographical variation in the length and mass of tail feathers in relation to body size and wing size. Tail feather length differed between sexes and populations, and such variation was a result of the effects of natural selection, acting through differences in body size and wing size, as well as the effects of sexual selection that favours longer tails. The extra enlargement of the tail promoted by sexual selection (i.e. beyond the natural selection optimum) could be achieved by increasing investment in ornaments, and by modifying feather structure to produce longer feathers of lower density. These two separate processes accounting for the production of longer and more costly tail feathers and less dense feathers, respectively, are consistent with the hypothesis that both Zahavian and Fisherian mechanisms may be involved in the evolution of the long tails of male barn swallows. We hypothesize that the strength of sexual selection increases with latitude because of the need for rapid mating as a result of the short duration of the breeding season at high latitudes. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 925–936.     

The effect of mermithid parasitism on predation of nymphal Baetis bicaudatus (Ephemeroptera) by invertebrates

We investigated how infection by the mermithid nematode Gasteromermis sp. affected predation on its nymphal mayfly host, Baetisbicaudatus, by two invertebrate predators – the stonefly nymphs of Kogotusmodestus and the caddisfly larvae of Rhyacophilahyalinata. Predation trials and behavioral observations were conducted in stream-side, flow-through experimental chambers. When parasitized and unparasitized prey were offered in equal numbers, K. modestus consumed significantly more parasitized than unparasitized nymphs. R. hyalinata consumed equal numbers of both prey types. Behavioral observations of foraging K.␣modestus on parasitized and unparasitized prey suggested that the increased consumption of parasitized nymphs was due to differences in the behavior of infected mayflies in response to the predator. Specifically, parasitized nymphs drifted less often to escape an approaching predator (non-contact encounters) compared to unparasitized nymphs, which increased the number of contact encounters and attacks that occurred between K.␣modestus and parasitized prey. Because all hosts are castrated, these behavioral alterations affect only the fitness of the parasite, which is killed along with its host by invertebrate predation. We present a number of hypotheses to explain why the parasite causes increased predation on its host. These include the large size of the parasite affecting the sensory abilities of the host, the larger energetic costs of escape behavior for parasitized individuals, and natural selection from fish predation against drifting behavior by parasitized individuals. Received: 27 May 1996 / Accepted: 30 September 1996     

Parasite Infestation and Parental Care in the Barn Swallow Hirundo rustical a Test of the Resource-provisioning Model of Parasite-mediated Sexual Selection

Barn swallows, Hirundo rustica, are commonly infested by the haematophagous tropical fowl mite Omithonyssus bursa (Macronyssidae, Gamasida), which severely reduces various measures of reproductive success among the barn swallow hosts. Food provisioning rate by parent barn swallows, measured in terms of absolute feeding rate by males and females and relative feeding rate by males (percentage of food provided by the male parent), was not significantly related to natural levels of infestation of nests. Experimental manipulation of mite loads in nests during the egg-laying period of the first clutch, which also affected mite loads of parent barn swallows, significantly affected food-provisioning rates of single-brooded, but not of double-brooded barn swallows. These results suggest that effects of mites on the parenting ability of barn swallow hosts depend on host resistance towards parasites. This is consistent with the resource-provisioning hypothesis of parasite-mediated sexual selection, suggesting that females prefer parasite-free males because they are efficient parents, but also with the hypothesis that females prefer males with traits signalling genetic resistance to parasites.     

Reindeer antlers: visual indicators of individual quality?

Fluctuating asymmetry (FA) in ornamental characters may reflect developmental stability in the translation from genotype to phenotype. Antlers of reindeer show FA, are visually conspicuous ornaments and are important in intraspecific assessment. We show that there is a negative relationship between size and asymmetry in visual antler characteristics (i.e., antler length and number of tines) among free-ranging male reindeer in rut. This indicates that individuals that develop large ornaments are better able to buffer developmental stress than individuals that develop small ornaments. There is no relationship between asymmetry in antler length and asymmetry in jaw length, suggesting that symmetry in antlers does not reflect overall body symmetry. This difference may be caused by trait-specific sensitivity to developmental stress. Such stress may partly be caused by parasites, which show a positive association with asymmetry in antlers, but no relationship to asymmetry in jaws. Our results indicate that antlers may be exposed to directional selection in a visual signaler-receiver system and that information about parasite burden may be obtained from evaluation of asymmetry in antlers developed under exposure to a multitude of environmental stresses. Received: 8 October 1996 / Accepted: 13 January 1997     

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.     

Lifetime reproductive success,selection on lifespan,and multiple sexual ornaments in male European barn swallows

Natural and sexual selection arise when individual fitness varies according to focal traits. Extra‐pair paternities (EPPs) can affect the intensity of selection by influencing variance in fitness among individuals. Studies of selection require that individual fitness is estimated using proxies of lifetime reproductive success (LRS). However, estimating LRS is difficult in large, open populations where EPPs cause reallocation of biological paternity. Here, we used extensive field sampling to estimate LRS in a population of barn swallows (Hirundo rustica) to estimate selection on lifespan and ornamental traits of males. We found selection on lifespan mediated both by within‐ and extra‐pair fertilization success and selection on tail length mediated by within‐ but not extra‐pair fertilization success. In addition, we found selection on tail white spots via extra‐pair fertilization success after controlling for selection on other traits. These results were not confounded by factors that hamper studies of LRS, including nonexhaustive sampling of offspring and biased sampling of males. Hence, natural and sexual selection mediated by LRS operates on lifespan, tail length, and size of the tail white spots in barn swallows.     

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.     

Aerodynamic costs of long tails in male barn swallows Hirundo rustica and the evolution of sexual size dimorphism

Exaggerated tail feathers of birds constitute a standard exampleof evolution of extravagant characters due to sexual selection.Such secondary sexual traits are assumed to be costly to produceand maintain, and they usually are accompanied by morphologicaladaptations that tend to reduce their costs. The aerodynamiccosts for male barn swallows Hirundo rustica of having longtails were quantified using aerodynamics theory applied to morphologicaldata from seven European populations. Latitudinal differencesin tail length were positively correlated with differences inflight costs predicted by aerodynamics theory. A positive relationshipbetween aerodynamic costs of long tails and the degree of sexualsize dimorphism was found among populations. Latitudinal differencesin foraging costs may result in tail length being relativelysimilar in males and females in southern populations, whereasthe low foraging costs for males in northern populations mayallow them to cope with higher aerodynamic costs, giving riseto large sexual size dimorphism. Enlargement of wingspan inmales can alleviate but not eliminate the costs of tail exaggeration,and therefore differences in aerodynamic costs of male ornamentswere maintained among populations. Sexual size dimorphism in thebarn swallow arises as a consequence of latitudinal differencesin the advantages of sexual selection for males and the costsof long tails for males and females.