Female collared flycatchers adjust yolk testosterone to male age, but not to attractiveness

The differential allocation hypothesis predicts that femalesinvest more resources into reproduction when mating with attractivemales. In oviparous animals this can include prefertilizationdecisions such as the production of larger eggs and the depositionof hormones, such as the steroid testosterone, into yolks. Onthe other hand, a compensatory hypothesis posits that femalesallocate more resources into the eggs when mated with malesof inferior quality. In the present study, we show that free-livingfemales of the collared flycatcher (Ficedula albicollis), asmall passerine bird, do not produce larger eggs or depositmore testosterone into eggs when mating with attractive malesreflected by a large forehead patch size, which is contraryto the prediction of the differential allocation hypothesis.However, we found higher yolk testosterone concentrations ineggs laid for young than older males. Because in young malesgenetic quality, parental experience, or willingness to investinto paternal care is likely to be low, high yolk testosteronelevel in their clutches may indicate that their females followa compensatory tactic. They may elicit more paternal care fromyoung, inexperienced males by hormonally increasing nestlingbegging. Laying date was also correlated with yolk testosteronelevel; however, when we controlled for it, male age still remaineda strong determinant of testosterone allocation.     

Female pied flycatchers trade between male quality and mating status in mate choice

According to mate choice theory, females should consider both male quality and mating status when choosing a mate. In birds, strong experimental evidence indicates that females prefer males with elaborate traits. No comparable evidence exists to determine whether females take male mating status into account or how they may trade between male quality and male mating status. We studied mate choice of female pied flycatchers (Ficedula hypoleuca) in outdoor aviaries where the effect of territory quality could be eliminated and where we could control which males were mated and which were unmated. We used male plumage colour as our measure of male quality. In the aviaries, focal females could easily compare males and assess their plumage colour and mating status, and resident females were prevented from attacking prospecting females because of separation in different compartments. The study provided evidence for a trade-off in mate choice. Females may compromise by choosing an already mated male if he is more brightly coloured and, presumably, of higher quality than available unmated males. The study did not support the idea that polygyny is based on male deception of females, but the results were consistent with the female aggression hypothesis.     

Paternal effort related to experimentally manipulated paternity of male collared flycatchers

The way that variation in paternity affects the optimal level of paternal effort has been a contentious issue, both in terms of theory and the empirical data needed to test competing theories. Clarification of the theoretical issues has led to the prediction that a reduction in paternal effort should only be expected when (i) there are substantial costs of paternal care and (ii) males have available some cue to their share of paternity in the current brood. Previous work on the collared flycatcher, Ficedula albicollis, has shown that the first condition is supported because of trade-offs between paternal effort and secondary sexual character size. We carried out experimental manipulations of pairs of collared flycatchers (temporary male removal), which were effective in causing variation in paternity in the current brood. Male responses to these manipulations were studied by quantifying levels of paternal care. All males reared nestlings cross-fostered from non-experimental nests at the egg stage, thus ruling out the possibility that they responded to direct cues about paternity. The timing of male removal predicted the male''s share of paternity, suggesting that males had a clear cue to their share of paternity, thereby fulfilling the second condition. As expected, the male''s share of care, and rate of provisioning, were positively related to his share of paternity. The suggestion that the timing of removal was the cue used by males to predict their share of paternity was supported, since after the influence of this variable was controlled, there was no longer any relationship between paternity and paternal care. These data provide qualitative support for optimality models of paternal care in relation to certainty of paternity, and suggest that quantitative tests of the models are possible in well-characterized systems.     

A role for female ornamentation in the facultatively polygynous mating system of collared flycatchers

In a polygynous mating system, females settling with alreadymated males often experience low mating success due to the reducedparental contribution of the male. However, there are numerousfactors that may still make it advantageous for some femalesto choose this mating status. Facultative polygyny is believedto be dominated by male advertisement and female choice. Althoughquality differences and competition among females are increasinglyrecognized as important determinants of polygynous settlementpatterns, the importance of signals of female quality in thismating system is largely unknown. Here we examined the relationshipof the white wing patch size (WPS) of female collared flycatchers,a phenotypically plastic and age-dependent ornament, with socialmating status, while controlling for settlement date and age.At the population level, monogamous, primary, and secondaryfemales did not differ in WPS. However, the primary female ofindividual males was more ornamented than the secondary female,and this difference declined with increasing distance betweenprimary and secondary nests. Secondary female ornamentationincreased, whereas that of the primary female did not changewith nest distance. These results suggest a subtle role forfemale ornamentation at polygynous mating. Future studies shouldtherefore take into account mating status when assessing thecosts and benefits of female signals. Moreover, patterns inquality-indicating female traits may contribute to the explanationof differences in reproductive success among females of differentmating status.     

A sexual conflict in collared flycatchers,Ficedula albicollis: early male moult reduces female fitness

A sexual conflict over levels of parental care occurs in most animals with biparental care, and studies of sexual differences in levels of parental care have usually focused on its intra-annual fitness consequences. We investigated inter-annual fitness consequences of a sexual difference in timing of feather replacement (moult) in collared flycatchers (Ficedula albicollis). In this study, males overlapped reproduction and moult more often than females, they also initiated their moult at an earlier stage of breeding than females. Females mated to males with a moult-breeding overlap had significantly lowered survival chances than females mated with males initiating moult after breeding. Furthermore, females mated with moulting males risked a lowered future fecundity in terms of a delayed start to breeding in the following season. However, early moulting males achieved a similar reproductive success as males initiating moult after breeding. Likewise, male survival probability to the following breeding season did not differ between early and late moulting individuals, nor was there any evidence that males gained or lost in future mating advantages by moulting early. These results show not only that a sexual conflict over timing of moult may operate, but also that it can impose severe fitness consequences, in terms of reduced future fecundity and survival probability, upon the ''losing'' sex.     

Different reproductive tactics in male collared flycatchers signalled by size of secondary sexual character

Most studies of variation in male reproductive tactics have focused on conspicuous categorical differences in mating behaviour (i.e. variation in mating strategies). However, in the presence of trade-offs between investment in competition over matings, parental care and survival, a male''s optimal allocation rule might vary according to his physiological condition and social or ecological environment. Thus, there may also be more subtle variation in male reproductive tactics. Here, I show that the reproductive effort (estimated as residual change in condition) of male collared flycatchers was affected by the size of their forehead patch (a secondary sexual character), age and date of arrival at the breeding grounds. Among early males (i.e. males with a high likelihood of both attracting more than one female and obtaining extra-pair copulations), large-patched males made a relatively large reproductive effort and as a result were in worse condition at the time of feeding offspring as compared to small-patched males. Furthermore, among early breeders, young males and males with experimentally increased forehead patch size made a relatively high effort. By contrast, regardless of age and badge size, there were no such patterns observed among late breeders. These results suggest that collared flycatchers use different reproductive tactics depending on both internal and external factors, and that the size of a secondary sexual trait may not only indicate variation in individual condition but also predict how resources will be allocated between pre- and post-mating reproductive activities.     

MHC diversity, malaria and lifetime reproductive success in collared flycatchers

Major histocompatibility complex (MHC) genes encode proteins involved in the recognition of parasite-derived antigens. Their extreme polymorphism is presumed to be driven by co-evolution with parasites. Host-parasite co-evolution was also hypothesized to optimize within-individual MHC diversity at the intermediate level. Here, we use unique data on lifetime reproductive success (LRS) of female collared flycatchers to test whether LRS is associated with within-individual MHC class II diversity. We also examined the association between MHC and infection with avian malaria. Using 454 sequencing, we found that individual flycatchers carry between 3 and 23 functional MHC class II B alleles. Predictions of the optimality hypothesis were not confirmed by our data as the prevalence of blood parasites decreased with functional MHC diversity. Furthermore, we did not find evidence for an association between MHC diversity and LRS.     

Depigmented wing patch size is a condition-dependent indicator of viability in male collared flycatchers

Honesty of sexual advertisement is thought to be the resultof signalling costs. Because production costs of depigmentedplumage patches are probably very low, their role as honestsignals of individual quality has been questioned. Costs ofbearing these traits, however, should also be taken into account.Studies on proximate determination and possible informationcontent of white badges are very rare. We investigated repeatability,sensu lato heritability, and condition- and age-dependence ofwhite wing patch size, a male display trait in a populationof collared flycatchers (Ficedula albicollis), based on 4 yearsof data. By comparing relationships between age and wing patchsize (1) within individuals among years versus (2) among individualswithin years, we could address the viability indicator valueof the trait. Wing patch size approximately doubled at the transitionfrom subadult to adult plumage, and its change was significantlyrelated to body condition the previous season. Repeatabilityand heritability values suggest that the trait is informativealready in subadult plumage, and that genetic and early environmentaleffects are important in its determination, the latter onlyduring the first year of life. Thus, wing patch size can actas a condition-dependent signal of genetic quality. Indeed,discrepancy between results from the horizontal and verticalage-dependence approaches shows that the trait was positivelyrelated to expected lifespan. After examining several alternativeexplanations, we conclude that wing patch size indicates geneticallybased viability. This is the first study to demonstrate a goodgenes viability benefit conferred by a depigmented plumage patch.     

Predation by sparrowhawks Accipiter nisus on male and female pied flycatchers Ficedula hypoleuca in relation to their breeding behaviour and foraging

Bright plumage, song display, and aggressive resource defence in males may cause higher predation on males than on females during the breeding season. However, in birds, higher predation on females is sometimes observed. Parental investment may be high in females (egg-laying, incubation and feeding of offspring), which might lead to a high risk of predation. We studied predation by sparrowhawks Accipiter nisus in relation to behaviour in pied flycatchers Ficedula hypoleuca where breeding males are more conspicuous than females in plumage and behaviour. Male pied flycatchers generally occupied more exposed perches than females. Females were more mobile and foraged more than males, especially prior to and during incubation. During the incubation and nestling stages, when predation on the sexes could be directly compared, sparrowhawks took about the same number of male and female pied flycatchers. During incubation, however, females spent about 77% of the day in the nest and were 4.7 times more vulnerable than males per unit of time available (i.e. outside the nest). A comparison with the chaffinch Fringilla coelebs , where hawks took more females than males, indicates that timing of breeding, foraging behaviour and parental roles of males and females affect predation risk.     

A test of the "sexy son" hypothesis: sons of polygynous collared flycatchers do not inherit their fathers' mating status

According to the original "sexy son" hypothesis, a female may benefit from pairing with an already-mated male despite a reduction in fecundity because her sons inherit their father's attractiveness. We used data from a long-term study of collared flycatchers (Ficedula albicollis) collected during 24 years to test this prediction. Our results show that the sons of polygynously mated females fledged in poor condition and therefore did not inherit their father's large forehead patch (a condition-dependent display trait) or mating status. From the female's perspective, polygynous pairing resulted in fewer recruited grandchildren than did a monogamous pairing. The reproductive value of sons did not outweigh the fecundity costs of polygyny because the low paternal care reduced the attractiveness of sons. When there are long-lasting parental effects on offspring attractiveness, costs of polygyny may include the production of nonsexy sons.     

Nestling immune response to phytohaemagglutinin is not heritable in collared flycatchers

The response to intradermally injected phytohaemagglutinin (PHA-response) is a commonly used quantification of avian immunocompetence (the ability to resist pathogens). Parasite-mediated sexual selection requires heritable immunocompetence, but evidence for heritability of PHA-response in birds largely stems from full-sib comparisons. Using an animal model approach, we quantified the narrow-sense heritability of PHA-response in 1626 collared flycatcher (Ficedula albicollis) nestlings from 332 families, most of which were cross-fostered. Nestling PHA-response was not significantly heritable (h2=0.06+/-0.10), but was subject to non-heritable nest-of-origin effects (10% of variation). Our findings illustrate that full-sib comparisons of immunological measures may lead to an inflated estimate of heritability and also reveal a limited role of nestling PHA-response for sexual selection in this population.     

Maternal effects due to male attractiveness affect offspring development in the zebra finch

Maternal effects occur when offspring phenotype is influenced by environmental factors experienced by the mother. Mothers are predicted to invest differentially in offspring in ways that will maximize offspring fitness depending on the environment she expects them to encounter. Here, we test for maternal effects in response to mate attractiveness on offspring developmental traits in the zebra finch Taeniopygia guttata. We controlled for parental genetic quality by manipulating male attractiveness using coloured leg rings and by randomly assigning mating pairs. The potential confounding effect of differential nestling care was controlled for by cross-fostering clutches and by allowing for variance due to foster father attractiveness in general linear models. We found a difference in egg mass investment between attractiveness groups and, importantly, we found that all of the offspring traits we measured varied with the attractiveness of the father. This provides strong evidence for maternal effects in response to mate attractiveness. Furthermore, due to the experiment design, we can conclude that these effects were mediated by differential investment of egg resources and not due to genetic differences or differences in nestling care.     

Patterns of extrapair mating in relation to male dominance status and female nest placement in black-capped chickadees

In sexually promiscuous animals, females may benefit by nestingclose to the edge of their partner's territory to facilitateextrapair copulations. In the present study, we describe theextrapair mating system of black-capped chickadees, Poecileatricapillus, and test whether nest locations are influencedby conspecific attraction to extrapair partners. We conducteda spatial analysis of female mating strategies by using microsatellitepaternity analysis in conjunction with geographic informationsystem (GIS) analysis of nest and territory locations. Extrapairoffspring comprised 52 of 351 offspring (14.8%) and were presentin 19 of 57 broods (33.3%). Females paired to males with lowdominance status in the previous winter's flock hierarchy weremore likely to engage in a mixed reproductive strategy thanwere females paired to males with high dominance status. Femaleshad extrapair copulations and extrapair fertilizations withhigh-ranking males more often than with low-ranking males. Notall extrapair copulations resulted in extrapair fertilizations.Females constructed their nests within 16.8 ± 1.0 m ofthe edge of their partner's territory, significantly closerto the edge of their nearest neighbor's territory than to thecenter of their own partner's territory. Extrapair males usuallyshared territory boundaries with cuckolded males. Females pairedto low-ranking males constructed nests near the territory edgesof neighboring high-ranking males. However, females did nothave extrapair copulations with the neighbor nearest to theirnest or even with the high-ranking neighbor nearest to theirnest. We conclude that conspecific attraction to neighbors mayinfluence nesting location in black-capped chickadees; however,it does not operate by facilitating extrapair copulations.     

Incubation effort in relation to male attractiveness in zebra finches Taeniopygia guttata

The division of labour in parental care between the two sexes varies between and within species. In birds, parents have been shown to invest more into egg production and nestling care when paired with an attractive rather than an unattractive mate, as predicted by the differential allocation hypothesis. Here we investigate variation in the female's and male's share of incubation behaviour, a vital, and costly, period of parental care during which the embryo is vulnerable to perturbations in developmental conditions. We manipulated the attractiveness of male zebra finches Taeniopygia guttata , using red or green leg-rings. To simulate their natural social environment we allowed them to breed in outdoor aviaries. All males within an aviary were given the same coloured ring to avoid ring-colour related assortative mating. Males within a colony, however, were still expected to show some variation in attractiveness with the earliest laying females possibly pairing with the most attractive males. Indeed we found that both factors played a role in explaining female incubation effort. Among females mated to red ringed males, earlier laying females contributed significantly more to incubation than late laying females, but no such pattern was found in females mated to green ringed males. Overall, there were no differences in the level of incubation provided by both parents between treatment groups, suggesting some compensation within the pair. Hatching success was correlated with a pair's total incubation effort. These results suggest that variation in the division of parental care between the sexes is in agreement with both increased effort of females mated with attractive males, and females compensating for the reduced effort of attractive males seeking further mating opportunities. These two factors can act at the same time in natural populations and both should be considered when explaining variation in division of labour between the sexes.     

Cytoplasmic male sterility in relation to hybrid wheat breeding

Summary The method of substitution and restoration of nucleus is briefly described.Three species, Aegilops caudata, Ae. ovata and Triticum timopheevi, were used as donors of male sterility cytoplasms.The characteristics of these three cytoplasms are summarized as follows:Caudata-cytoplasm: This cytoplasm has in many respects deleterious effects on the manifestation of alien genomes. Substitution lines having hexaploid wheat genome constitution are mostly male sterile while the female organ is normal. Some lines set frequently germless seeds. Haploid and twin seedlings are of common occurrence in other lines. Pistillody is common in the substitution lines with tetraploid wheat genomes.Ovata-cytoplasm: No pistillody was found in the substitution lines, both with hexaploid and tetraploid wheats. Male sterility is always complete in the substitution lines of hexaploid wheats with the exception of P 168, a variety of common wheat having a pair of satchromosomes of Ae. caudata. This variety restores male fertility completely. No effective restorers were found for the substitution lines of emmer wheat. Delayed heading is common in the 4x substitution lines.Timopheevi-cytoplasm: Substitution lines of 6x wheats are mostly male sterile, while those of 4x wheats are more or less male fertile. Only the genome of T. spelta duhamelianum restores completely pollen fertility.Among the indispensable factors for the success of hybrid wheat, five were discussed. They were (1) hetero sis, (2) selection of male sterile cytoplasms, (3) discovery of restoring genes, (4) production of hybrid seeds and (5) quality.

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Zusammenfassung Die Methode der Substitution und Restoration des Nucleus wird kurz beschrieben.Drei Arten, Aegilops caudata, Ae. ovata und Triticum timopheevi, wurden als Donor cytoplasmatisch bedingter männlicher Sterilität verwendet. Die Charakteristika der jeweiligen Cytoplasmen lassen sich wie folgt zusammenfassen:Caudata-Cytoplasma: Dieses Cytoplasma hat in vieler Hinsicht einen schädlichen Einfluß auf die Manifestation fremder Genome. Substitutionslinien mit einem hexaploiden Weizengenom sind meist männlich steril, das weibliche Organ ist normal. Einige Linien bringen häufig keimlose Samen; in anderen Linien treten haploide und Zwillingssamen auf. Bei Substitutionslinien mit tetraploiden Weizengenomen werden häufig andere Blütenorgane in Karpelle umgewandelt.Ovata-Cytoplasma: In den Substitutionslinien sowohl der hexaploiden wie tetraploiden Weizen wurden keine anderen Blütenorgane in Karpelle umgewandelt. Die Substitutionslinien der hexaploiden Weizen sind stets vollkommen männlich steril mit Ausnahme von P 168, einer Weizenvarietät, die ein Paar Sat-Chromosomen von Ae. caudata besitzt. Diese Varietät stellt die männliche Fertilität vollkommen wieder her. In den Emmer-Substitutionslinien wurden keine wirksamen Restorer gefunden. Bei den 4x-Substitutionslinien zeigt sich häufig verzögertes Ährenschieben.Timopheevi-Cytoplasma: Die Substitutionslinien der 6x-Weizen sind meist männlich steril, die von 4x-Weizen dagegen mehr oder weniger männlich fertil. Nur das Genom von T. spelta duhamelianum stellt die Pollenfertilität völlig wieder her.Von den für den Erfolg der Hybridweizenzüchtung unabdingbaren Faktoren wurden die folgenden 5 besprochen: 1. Heterosis, 2. Selektion männliche Sterilität bedingender Cytoplasmen, 3. Auffinden von Restorergenen, 4. Produktion von Hybridsaatgut und 5. Qualität.

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Dedicated to Professor Hans Stubbe on the occasion of his 65^th birthday.

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Contribution from the National Institute of Genetics, Japan, No. 636. This paper has been prepared for a lecture delivered July 18, 1966, at the Lenin All-Union Academy of Agricultural Science. This work has been supported by the Rockefeller Foundation, Grant GA AGR 65111.     

Eggshell coloration in relation to male ornamentation, female condition and egg quality in the collared flycatcher Ficedula albicollis

The blue-green eggshell pigment biliverdin is an efficient antioxidant, the deposition of which may be costly and act as a handicap to the female's antioxidant capacity. Thus, it is hypothesized that there exists a positive correlation between the degree of eggshell coloration and the condition and health state of the mother. In this study, we measured the blue-green chroma of collared flycatcher Ficedula albicollis eggs, and investigated the associations between egg colour and parental characteristics, laying date, clutch size and laying order. We also analysed the possible correlations between egg size, yolk carotenoid and antibody levels and eggshell pigmentation. Our results revealed no significant relationships between egg colour and female age, morphological and serological variables. Blue-green colour intensity of eggs increased throughout the breeding season, which could be the result of either a proximate constraint or an adaptive strategy. We found a positive association between egg colour saturation and yolk lutein concentration. This relationship could be the result of the seasonal improvement of caterpillar supply, which could influence the deposition of both components into the egg. Furthermore, we found that females mated to lower-quality males produced eggs with higher biliverdin pigmentation. It is possible that deposition of biliverdin is correlated to some unmeasured aspect of egg quality that could enhance the viability of offspring of lower-quality fathers. We found that intensity of blue-green coloration increased with laying order between the first and fifth eggs.     

Behavioral attributes influence annual mating success more than morphological traits in male collared lizards

Traits that potentially influence mating success (MS) may be"static" with low lability once they develop or "dynamic" withhighly modifiable expression. We used principal components (PCs)analyses of dynamic behavioral and morphological traits thatare static over the short term to determine their relative contributionsto the ability of territorial male collared lizards to acquireaccess to females and obtain high MS. We estimated annual MSof males as the relative frequency with which they engaged incourtship with reproductively active resident females. ThreePCs explained statistically significant phenotypic variationamong males. Morphological traits loaded significantly on 2PCs that explained 26.3% and 13.0% of the variance, respectively,whereas behavioral variables loaded significantly on a differentcomponent that explained 15.7% of the variance in male traits.The frequency with which males initiated aggressive encounterswith same-sex competitors did not load significantly on thesePC axes. Males having behavioral PC scores above the mean hadsignificantly higher MS than those with behavioral scores belowthe mean, whereas male MS was not related to component scoresfor either of the axes describing static morphological variables.Results indicate that in our population behavior patterns associatedwith advertisement, particularly to females, influence maleMS more strongly than morphological traits or the initiationof direct aggression with same-sex competitors.     

Breeding experience and the heritability of female mate choice in collared flycatchers

Background

Heritability in mate preferences is assumed by models of sexual selection, and preference evolution may contribute to adaptation to changing environments. However, mate preference is difficult to measure in natural populations as detailed data on mate availability and mate sampling are usually missing. Often the only available information is the ornamentation of the actual mate. The single long-term quantitative genetic study of a wild population found low heritability in female mate ornamentation in Swedish collared flycatchers. One potentially important cause of low heritability in mate ornamentation at the population level is reduced mate preference expression among inexperienced individuals.

Methodology/Principal Findings

Applying animal model analyses to 21 years of data from a Hungarian collared flycatcher population, we found that additive genetic variance was 50 percent and significant for ornament expression in males, but less than 5 percent and non-significant for mate ornamentation treated as a female trait. Female breeding experience predicted breeding date and clutch size, but mate ornamentation and its variance components were unrelated to experience. Although we detected significant area and year effects on mate ornamentation, more than 85 percent of variance in this trait remained unexplained. Moreover, the effects of area and year on mate ornamentation were also highly positively correlated between inexperienced and experienced females, thereby acting to remove difference between the two groups.

Conclusions/Significance

The low heritability of mate ornamentation was apparently not explained by the presence of inexperienced individuals. Our results further indicate that the expression of mate ornamentation is dominated by temporal and spatial constraints and unmeasured background factors. Future studies should reduce unexplained variance or use alternative measures of mate preference. The heritability of mate preference in the wild remains a principal but unresolved question in evolutionary ecology.     

Flight muscle changes in male pine engraver beetles during reproduction: the effects of body size, mating status and breeding failure

Abstract. In a pattern that is typical for bark beetles, the lateralis medius flight muscle of male pine engravers, Ips pini Say (Coleoptera: Scolytidae), was found to decrease four-fold in volume (from mean ± SE = 1.36 ± 0.06 × 10^?2 mm³ to 0.34 ± 0.06 × 10^?2 mm³) within five days of the initiation of breeding galleries, and then to regenerate gradually to functional capacity during subsequent weeks. Although there was considerable variation in the timing and extent of flight muscle regeneration in males, this variation was not a consequence of differences between small (length < 4.0 mm) and large (length ≥ 4.0 mm) males. Two subsequent experiments revealed that male pine engravers can control the timing of flight muscle regeneration. In the first experiment, the flight muscles of males that were denied mates degenerated within 5 days of gallery initiation, but then showed complete regeneration 5 days later. In the second experiment, mated males that were removed from their breeding galleries (to simulate breeding failure) also showed extensive muscle degeneration 5 days after gallery initiation, but then regenerated their flight muscles to functional capacity by the tenth day. The ability of males to regenerate their flight muscles in response to conditions at the gallery is probably adaptive because it allows them to fly in search of new breeding opportunities when they are unable to attract mates or when breeding attempts fail.