What makes a nest-building male successful? Male behavior and female care in penduline tits

Why do females increase parental effort when caring for theoffspring of attractive males? First, attractive males may bepoor fathers so that their females are compelled to increasetheir own contribution in order to fledge some young (the partner-compensationhypothesis). Second, females mated to attractive males may bewilling to increase their parental effort to reap high indirectbenefits for their offspring, and in turn males can decreasetheir own contribution (the differential allocation hypothesis[DAH]). We investigated these hypotheses in the penduline titRemiz pendulinus, a small passerine bird that has sequentialpolygamy by both sexes and strict uniparental care either bythe male or the female. We focused on two sexually selectedmale traits: nest size and nest-building behavior. We show thatmale care is unrelated to nest-building behavior, whereas femalesare more likely to care for the offspring of those males thatspend more time nest building. Females also more likely carefor the offspring of males that build large nests. Consequently,the reproductive success of males increases with nest size andnest-building behavior. Our results are consistent with theDAH and suggest that nest-building behavior and nest size areunder postmating sexual selection in penduline tits.     

Rapid evolutionary change in a secondary sexual character linked to climatic change

The ability of organisms to respond evolutionarily to rapid climatic change is poorly known. Secondary sexual characters show the potential for rapid evolutionary change, as evidenced by strong divergence among species and high evolvability. Here we show that the length of the outermost tail feathers of males of the socially monogamous barn swallow Hirundo rustica, feathers that provide a mating advantage to males, has increased by more than 1 standard deviation during the period from 1984 to 2003. Barn swallows from the Danish population studied here migrate through the Iberian Peninsula to South Africa in fall, and return along the same route in spring. Environmental conditions on the spring staging grounds in Algeria, as indexed by the Normalized Difference Vegetation Index, predicted tail length and change in tail length across generations. However, conditions in the winter quarters and at the breeding grounds did not predict change in tail length. Environmental conditions in Algeria in spring showed a temporal deterioration during the study period, associated with a reduction in annual survival rate of male barn swallows. Phenotypic plasticity in tail length of males, estimated as the increase in tail length from the age of 1 to 2 years, decreased during the course of the study. Estimates of directional selection differentials for male tail length with respect to mating success, breeding date, fecundity, survival and total selection showed temporal variation, with the intensity of breeding date selection, survival selection and total selection declining during the study. Response to selection as estimated from the product of heritability and total selection was very similar to the observed temporal change in tail length. These findings provide evidence of rapid micro-evolutionary change in a secondary sexual character during a very short time period, which is associated with a rapid change in environmental conditions.     

Male reproductive success and sexual selection in northern water snakes determined by microsatellite DNA analysis

Male northern water snakes (Nerodia sipedon) have high variancein reproductive success relative to females. We used DNA-basedpaternity analyses from a 3-year study of two marsh populationsof water snakes to investigate the factors that contributeto variation in male success. Male traits investigated includedbody size, condition, tail length, home range size, activityduring the mating season, and genetic profile (genetic similarityto females, heterozygosity, and genetic variability [d²]).We successfully assigned > 80% of offspring to sires froma sample of 811 offspring from 45 litters. Male reproductivesuccess did not vary significantly with body size, tail length,condition, home range size, or the number of microsatelliteloci at which males were heterozygous, nor with other featuresof their genetic profiles. However, we found evidence of positive assortative mating by size in the marsh in which receptive femaleswere not spatially clumped. Also, males that were most activeduring the mating season were more successful, particularlywhere females were not clumped. We failed to find evidenceof selection acting on male size through variance in reproductivesuccess, indicating that sexual selection does not have an important influence on sexual size dimorphism in this species(males are smaller than females). We propose that males aresmaller than females because the lack of advantage to largesize allows males to adopt a low-energy, low-growth strategythat reduces their risk of predation outside the mating season.     

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.     

Rapid temporal change in frequency of infanticide in a passerine bird associated with change in population density and body condition

Sexually selected infanticide, whereby unmated males obtaina mate by killing the dependent offspring of an already matedfemale, is a common alternative reproductive strategy in manyanimals. I estimated the frequency of infanticide in a populationof barn swallows, Hirundo rustica, during the period 1977–2002.Population size decreased by more than a factor 10 during thisperiod, and this decrease was associated with an increase inmortality, selecting for adults with better body condition.Density-dependent effects acted on infanticide through the relationshipbetween the relative number of unmated males and populationsize. Because males in prime condition are better able to defendtheir nests against infanticidal males, the frequency of infanticidedecreased as mean tail length and mean body condition of malesincreased during the study period. Therefore, a rapid decreasein population size, a decrease in the abundance of unmated males,and a concomitant increase in body condition have changed theimportance of infanticide from being a major cause of mortalityaccounting for more than 25% of all nestling mortality to beingalmost completely absent during a period of 25 years.     

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.     

SEXUAL SELECTION IN THE BARN SWALLOW HIRUNDO RUSTICA. III. FEMALE TAIL ORNAMENTS

Male secondary sexual characters are often expressed in females, and the maintenance of the character in females can be due to either direct selection on females favoring the maintenance of the trait, or a correlated response to selection in males. Here I report on determinants of and phenotypic selection on tail length of female barn swallows Hirundo rustica. The homologous trait in males is under strong directional sexual selection. Female tail length was positively associated with several reproductive parameters including total seasonal reproductive success, even when controlling for year and age effects. A change in female tail length from one year to another was often associated with a change in the reproductive parameters correlated with absolute tail length. There was little evidence for an association between female tail length and the duration of the incubation period (only females incubate) and absolute and relative female provisioning rates of offspring, and subsequent size of offspring. Tail length of female barn swallows was positively correlated with that of their mates. Female tail length was a heritable trait as determined from regression of the tail trait of offspring on that of their mother and their father, and there was a positive genetic correlation between the tail trait in males and females. In conclusion, female tail length reliably reflects female reproductive potential, and the trait appears to be under directional selection, which may result in an evolutionary response to selection because of the heritability of the tail trait.     

Sexual selection in a moth: effect of symmetry on male mating success in the wild

Sexual selection is generally caused by female choice and male–malecompetition. In female choice process, female preference isfavored indirectly and/or directly by sexual selection. In indirectselection, females expressing the preference might gain indirectgenetic benefits. In direct selection, females expressing thepreference might gain direct benefits or avoid male-imposedcosts. The white-tailed zygaenid moth Elcysma westwoodii ismonandrous, and males often gather around a female to mate withher, suggesting a high opportunity for sexual selection on maletraits. We quantified phenotypic selection on male morphologyin this species in the field. The morphological characters analyzedincluded body weight, antenna length, forewing length, hindwing length, hind wing tail length, genital clasper length,and the fluctuating asymmetry (FA) of these bilateral traits.In E. westwoodii, selection favored males with more symmetricgenital claspers, as well as longer and more symmetrical hindwings and antennae. Negative correlations between FA and sizewere also detected in the clasper and the antenna. Our resultssuggest that FAs of male traits, in particular the genital clasper,may have indirect and direct influences on mating success. Duringa copulatory attempt, an E. westwoodii male will try to graspthe female's abdominal tip with his claspers but often failto do so because of the female's reluctance to mate. The femaleabdominal tips are smooth and strongly sclerotized and couldthus be difficult for males to grasp. We hypothesize that moresymmetrical male claspers are more efficient in overcoming femalereluctance.     

Mate preference for multiple cues: interplay between male and nest size in the sand goby, Pomatoschistus minutus

Female mating preferences are often based on more than one cue.In empirical studies, however, different mate choice cues aretypically treated separately ignoring their possible interactions.In the current work, we studied how male body size and sizeof the male's nest jointly affect mate preferences of femalesand gobies, Pomatoschistus minutus. The females were givena binary choice between males that differed either in body sizeor size of their nest or both. We found that neither body sizenor size of the nest alone affected male attractiveness, buttogether these 2 cues had a significant effect. Specifically,large males were more popular among females when they had alarge nest than when they occupied a small nest. The resultssuggest that if interaction effects between multiple mate choicecues are not considered, there is a danger of ignoring or underestimatingthe importance of these cues in sexual selection by female choice.     

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.     

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.     

Within‐season variation in sexual selection in a fish with dynamic sex roles

The strength of sexual selection may vary between species, among populations and within populations over time. While there is growing evidence that sexual selection may vary between years, less is known about variation in sexual selection within a season. Here, we investigate within‐season variation in sexual selection in male two‐spotted gobies (Gobiusculus flavescens). This marine fish experiences a seasonal change in the operational sex ratio from male‐ to female‐biased, resulting in a dramatic decrease in male mating competition over the breeding season. We therefore expected stronger sexual selection on males early in the season. We sampled nests and nest‐holding males early and late in the breeding season and used microsatellite markers to determine male mating and reproductive success. We first analysed sexual selection associated with the acquisition of nests by comparing nest‐holding males to population samples. Among nest‐holders, we calculated the potential strength of sexual selection and selection on phenotypic traits. We found remarkable within‐season variation in sexual selection. Selection on male body size related to nest acquisition changed from positive to negative over the season. The opportunity for sexual selection among nest‐holders was significantly greater early in the season rather than late in the season, partly due to more unmated males. Overall, our study documents a within‐season change in sexual selection that corresponds with a predictable change in the operational sex ratio. We suggest that many species may experience within‐season changes in sexual selection and that such dynamics are important for understanding how sexual selection operates in the wild.     

Adaptive Offspring Sex Ratio Depends on Male Tail Length in the Guppy

A biased sex ratio in a brood is considered to be an adaptive strategy under certain circumstances. For example, if the expected reproductive success of one sex is greater than that of the other, parents should produce more offspring of the former sex than the latter. A previous study has documented that in the guppy, Poecilia reticulata, the female offspring of males possessing proportionally longer tails exhibit smaller body sizes and show decreased reproductive outputs than those of males having shorter tails. On the other hand, the total lengths of the male offspring of the long‐tailed males are larger because of their longer tails; consequently, they exhibit greater sexual attractiveness to females. Therefore, it has been hypothesized that this asymmetry in the expected reproductive success between the male and female offspring of long‐tailed males may result in a biased sex ratio that is dependent on the tail lengths of their fathers. This hypothesis was tested in the present study. The results showed that the females that mated with long‐tailed males produced more male offspring than those that mated with short‐tailed males. Logistic regression analysis showed that the ratio of tail length to the standard length of the fathers is a determinant factor of the sex of their offspring. These results suggest that the manipulation of the offspring sex ratios by parents enhances the overall fitness of the offspring.     

The function of long tails in female barn swallows (Hirundo rustica): an experimental study

The outermost tail feathers in male barn swallows (Hirundo rustica)are the target of a strong directional female mate preference.The tail ornament is also expressed in females, since femaleshave considerably longer tails than juveniles, either due to(1) a strong genetic correlation between the characters in thetwo sexes, or (2) direct sexual selection on females. To discriminatebetween these two hypotheses, we manipulated the length of theoutermost tail feathers in female barn swallows shortly afterarrival by either shortening or elongating the outermost tailfeathers, or maintaining their length among control individuals.Start of laying of the first clutch, reproductive performance,or provisioning of offspring did not show any significant differencesamong treatments. Original female tail length before manipulationwas unrelated to reproductive performance, while male tail lengthexplained some variation in the number of clutches and, to someextent, the total number of eggs laid per year. Females withlonger tails arrived earlier at the breeding grounds. Manipulatedfemale tail length was positively correlated to the tail lengthof their mates. Our results support the correlated responsehypothesis but do not support the sexual selection explanationfor the existence of exaggerated tail feathers in female barnswallows.     

Spatial and temporal patterns of nest distribution influence sexual selection in a marine fish

In many species, the natural distribution of material resources important for reproduction can profoundly impact reproductive success among individuals and, hence, the opportunity and intensity of sexual selection. Here, we report on a field‐based experiment investigating the effects of nest aggregation on sexual selection in a fish, the sand goby Pomatoschistus minutus. We found that the distribution of potential nests (sparse versus aggregated nest treatments) affected patterns of nest colonization and reproductive success. Specifically, in the treatment with aggregated nesting resources, a greater proportion of nests remained unoccupied by sand goby males. Although the size of nesting males did not differ between treatments, eggs accumulated more rapidly when nests were sparsely distributed. We found that the opportunity for selection decreased over time with the accumulation of eggs in the nests in both the aggregated and sparse treatments. Moreover, the effect of male size on reproductive success was influenced by an interaction between nest distribution and time, with the selection gradient being highest right after nest colonization when nests were aggregated, while the opposite pattern was observed in the sparse nest treatment. Such findings highlight the vital role that environmental and social factors can play in determining the importance of male phenotypic traits (in this case, male size). More broadly, our results also underscore how the natural distribution of resources, both in space and time, can impact the strength of sexual selection acting on wild animal populations.     

Nests as ornaments: revealing construction by male sticklebacks

Nests are built by animals from a variety of taxa, and serveas receptacles for eggs and developing offspring. Where nestsare built solely or mainly by one sex, they also have the potentialto serve as extended ornaments, because aspects of constructionpotentially reveal or amplify characteristics of the builderto prospective mates. Here, we develop novel indices to quantifynest structure and examine variation in temporal and structuralaspects of nest construction in relation to morphological,immunological, and physiological traits in male three-spinedsticklebacks, Gasterosteus aculeatus. Wild-caught male sticklebacksthat began construction within 3 days of being transferredto the laboratory built "neater" nests than fish that tooklonger to start, and we present alternative testable hypothesesthat could explain this pattern. Various characteristics ofnest-building males correlated with nest structure. The relativeweight of the building male's kidney—which secretes aglue-like protein used in nest building and whose developmentis androgen-dependent—correlated positively with nest "neatness." We also found males with enlarged spleens (an indicatorof immune stress) to construct less "compact" nests. The structureof a nest may therefore be important not only in determiningits functional capacity, but may also act as a quality-revealingornament. We suggest that females may gain valuable informationregarding male health status and androgen levels from nestinspection.     

Maternal investment in a bee species with facultative nest guarding and males heavier than females

1. Maternal investment can be influenced by several factors, especially maternal quality and possibilities for future reproduction. Mass provisioning Hymenoptera are an excellent group for measuring maternal investment because mothers distribute food sources to each brood cell for each offspring separately. Generally in aculeate Hymenoptera, larger females produce larger offspring and invest more in female offspring than in male offspring. 2. This study investigated patterns of maternal investment in Ceratina chalcites, which has an uncommon type of sexual size dimorphism in Hymenoptera: on average, males are heavier than females. It was found that larger females produce a significantly higher proportion of male offspring, as males are the costlier sex in this species. 3. Facultative nest guarding by females was observed. Females can guard offspring until adulthood, as is typical for bees of genus Ceratina (34.43% of nests); however, in the majority of cases (65.56% of nests), females plug and abandon the nest. Significant differences were found in the amount of investment between guarded and unguarded nests. Guarded nests had a greater number of provisioned brood cells and a higher proportion of male offspring. It is suggested that mothers have two facultative strategies – either she makes a large investment in the offspring of one nest or she abandons the first nest and carries out a second nesting elsewhere.     

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     

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.     

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.