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.     

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     

Testosterone effects on the immune system and parasite infestations in the barn swallow (Hirundo rustica): an experimental test of the immunocompetence hypothesis

The immunocompetence hypothesis predicts that testosterone (T)enhances the expression of male secondary sexual characterswhile exerting a suppressive effect on the immune system therebyexposing hosts to higher intensities of parasite infestations.In a natural population of barn swallow (Hirundo rustica) males,the intensity of infestation by some ectoparasites was negativelycorrelated with tail length and was positively correlated withimmunoglobulin levels, but no clear relationship was observedbetween immune responses (leukocyte counts, immunoglobulins)and tail length. Males implanted with T had higher intensitiesof parasite infestations at the time of recapture than controlmales, and T-implanted males experienced an increase in countsof eosinophils. In T-implanted males, immunoglobulin levelsinitially decreased and then increased as time from implantationelapsed. Among T-implanted males, those with longer tails hada smaller increase in eosinophil counts, tended to experiencea smaller increase of parasite infestations, and were more likelyto survive until the following breeding season than those withshorter tails. The relationships between parasite burden, immunesystem, and exaggeration of tail length in the natural populationof males are consistent with some aspects of the immunocompetencehandicap hypothesis. The results from the manipulation of Tplasma levels are also partly consistent with the hypothesis,since T-implantation resulted in higher levels of parasite infestations,but contradict the assumption of an obligatory immunosuppressiveeffect of T. Higher activation of the immune system of T-implantedmales indicate that high T plasma levels imposed a two-foldcost because of the effects on parasites and the immune responseto parasites, and this suggests that the effect of T on parasitesmight not be mediated by the immune system of the host. Theresults of the manipulation of T plasma levels support the handicapversion of the immunocompetence hypothesis since high quality,long-tailed males paid less in terms of activation of the immunesystem, change in parasite infestations, and chances of survivalthan low-quality, short-tailed males.     

Phenotypic quality and molt in the barn swallow, Hirundo rustica

Phenotypic quality may determine the development and expressionof secondary sexual characters. We studied the relationshipbetween molt and several measures of phenotypic quality in thesexually size-dimorphic barn swallow (Hirundo rustica) in itswinter quarters in Namibia. Males were in a more advanced stageof molt than females and juveniles, and the speed of molt asdetermined from the residual of the regression of the size ofthe gap in wings caused by missing and growing feathers on wingmolt score (residual wing raggedness) was also higher in malesthan in females and juveniles. Male barn swallows with longand symmetric tail feathers had a more advanced stage of moltand molted at a higher speed than males with short and asymmetrictails. Long-tailed females had a delayed molt, and females withasymmetric tails had less advanced molt and lower rates of feathergrowth than females with symmetric tails. Molt of secondariesin juveniles also appeared to be less advanced if they had longtails. Adult barn swallows molted their tail feathers in anirregular sequence with the longest, outermost tail featherusually replaced before the second or the third outermost feathers.Good body condition was positively associated with a high moltscore for some feather tracts and a rapid wing molt in adultfemales and tail molt in juveniles. Mallophaga were only weaklynegatively associated with primary and secondary molt scorein adult females and speed of wing molt in adult males. In conclusion,phenotypic quality of adult male barn swallows as reflectedby the expression of their secondary sexual character duringthe previous molt reliably reflected stage and speed of currentmolt.     

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.     

Sexual selection in the barn swallow Hirundo rustica. VI. Aerodynamic adaptations

Secondary sexual characters are assumed to be costly to produce and maintain, and this will select for morphological modifications that reduce the magnitude of such costs. Here we test whether a feather ornament, the sexually exaggerated outermost tail feathers of male barn swallows Hirundo rustica, a trait currently subject to a directional female mate preference, and other aspects of the morphology used for flight have been modified to increase aerodynamic performance. This was done by making comparisons among sexes within populations, among individuals varying in tail length within populations, and among populations from different parts of Europe. Male barn swallows experienced reduced drag from their elongated tail feathers by morphological modifications of the ornamental feathers as compared to females. Morphological features of the outermost tail feathers were unrelated to tail length in both males and females within populations. Wing and tail morphology (length of central tail feathers and wings, wing span, wing area, wing loading, and aspect ratio) was modified in males compared to females. Barn swallows with long tails had morphological tail and wing modifications that reduced the cost of a large ornament, and similar modifications were seen among populations. The costs of the exaggerated secondary sexual character were therefore reduced by the presence of cost-reducing morphological modifications. The assumptions of reliable signalling theory, that signals should be costly, but more so to low than to high quality individuals, were not violated because long-tailed male barn swallows had the largest cost-reducing morphological characters.     

Female choice, male interference, and sperm precedence in the red-spotted newt

Darwin first identified female choice and male—male competitionas forms of sexual selection resulting in the evolution of conspicuoussexual dimorphism, but it has proven challenging to separatetheir effects. Their effects on sexual selection become evenmore complicated when sperm competition occurs because spermprecedence may be either a form of cryptic female choice ora form of male—male competition. We examined the effectsof tail height on male—male competition and female choiceusing the sexually dimorphic red-spotted newt (Notophthalmusviridescens viridescens). Experiment 1 examined whether maletail height influenced male mating success. Males with deeptails were more successful at mating with females than thosewith shallow tails. Successful, deep-tailed males also were bigger(snout-vent length; SVL) than unsuccessful, shallow-tailed males,but they did not vary in tail length or body condition. Of these,only tail height and tail length are sexually dimorphic traits.Experiment 2 tested the hypothesis that the differential successof males with deeper tails was due to female choice by examiningboth simultaneous female preference for association and sequentialfemale choice. We found no evidence of female choice. When maleswere not competing to mate with females, tail height did notinfluence male mating success. Successful males did not havedifferent SVL and tail lengths than unsuccessful males. Thus,tail height in male red-spotted newts appears to be an intrasexuallyselected secondary sexual characteristic. Experiment 3 usedpaternity exclusion analyses based on molecular genetic markersto examine the effect of sperm precedence on sperm competitionin doubly-mated females. Sperm precedence likely does not havea pervasive and consistent effect on fertilization success becausewe found evidence of first, last, and mixed sperm usage.     

Rapid change in nest size of a bird related to change in a secondary sexual character

Among bird species in which males contribute to nest building,sexual selection has favored larger nests. I investigated determinantsof nest size in the barn swallow Hirundo rustica and how nestsize changed during the period 1977–2003, when tail length(a male secondary sexual character) increased by more than 1.2standard deviations. Males with short tails contributed moreto nest building than long-tailed males, signaling their futureinvestment in food provisioning of offspring. Pairs of barnswallows were consistent in nest size when build ing new neststhe same or different years, and level of phenotypic plasticityin nest size was small and could not account for temporal patternsin nest size. Offspring resembled their parents with respectto nest size, indicating a significant heritability of nestsize, independent of whether offspring were reared by theirparents or by foster parents, and there was a significant negativegenetic correlation between male tail length and outer nestvolume and amount of nest material. The temporal increase inmale tail length was associated with a decrease in nest size,with the amount of nest material in 2003 on average being lessthan a third of the amount used in 1977. Temporal change innest size could be accounted for by indirect selection on taillength causing change in nest size to match that predicted fromchange in tail length and the genetic correlation between maletail length and nest size.     

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.     

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.