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     

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)