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.     

Antagonistic natural selection revealed by molecular sex identification of nestling collared flycatchers

Natural selection may act in different directions during different life-history stages, or in different directions on different classes of individuals. Antagonistic selection of this kind may be an important mechanism by which additive genetic variation for quantitative traits is maintained, and can prevent populations or species reaching local adaptive peaks. This paper reports the results of a study of viability selection on morphological traits of nestling collared flycatchers Ficedula albicollis . Analyses performed without knowledge of the sex of nestlings suggested that no selection was occurring on these traits. However, using molecular sex identification with the avian CHD gene, it is shown that selection acts in different directions on male and female body size from fledging to breeding, apparently favouring relatively small males and large females. The results suggest that differential selection on male and female nestlings may contribute to purely phenotypic sexual size dimorphism in this species. These findings highlight the potential of newly developed molecular sexing techniques to reveal the consequences of an individual's gender for many aspects of its life history in taxa where gender cannot be determined on the basis of external appearance.     

Territory quality drives intraspecific patterns of extrapair paternity

Despite the potential reproductive benefits of extrapair matings,extrapair paternity rates in many avian species often vary greatlyamong populations. Although ecological factors have been shownto influence intraspecific patterns of extrapair paternity insome species, for cooperatively breeding species living in familygroups, social/demographic factors may also play a role. Thisstudy examined how ecological factors related to territory quality(vegetation cover, insect abundance) and social/demographicfactors (group size, number of breeding pairs, genetic relatedness)influenced intraspecific patterns of extrapair paternity incooperatively breeding superb starlings, Lamprotornis superbus.Superb starlings inhabit spatiotemporally variable African savannaswhere high temporal variability drives reproductive decisions(adoption of breeding roles, offspring sex allocation) and whereterritories suitable for breeding are limited. Although extrapairpaternity rates were only 14% of offspring and 25% of nests,they varied greatly among groups, ranging from 4% to 32% ofoffspring and from 7% to 60% of nests. These among-group differencesin extrapair paternity were not related to social/demographicfactors but instead to territory quality; extrapair paternitywas higher on lower quality territories (lower vegetation coverand grasshopper abundance) than on higher quality territories(higher vegetation cover and grasshopper abundance). These resultssuggest that even in a heterogeneous landscape where suitablebreeding territories are limited, subtle differences in habitatquality can have profound effects on reproductive decisionsand patterns of extrapair paternity. Understanding the interactionbetween spatial (habitat heterogeneity) and temporal (temporalvariability) environmental variation will be important for determininghow environmental and social factors drive avian reproductiveand mating decisions.     

Song discrimination by nestling collared flycatchers during early development

Pre-zygotic isolation is often maintained by species-specific signals and preferences. However, in species where signals are learnt, as in songbirds, learning errors can lead to costly hybridization. Song discrimination expressed during early developmental stages may ensure selective learning later in life but can be difficult to demonstrate before behavioural responses are obvious. Here, we use a novel method, measuring changes in metabolic rate, to detect song perception and discrimination in collared flycatcher embryos and nestlings. We found that nestlings as early as 7 days old respond to song with increased metabolic rate, and, by 9 days old, have increased metabolic rate when listening to conspecific when compared with heterospecific song. This early discrimination between songs probably leads to fewer heterospecific matings, and thus higher fitness of collared flycatchers living in sympatry with closely related species.     

Severe inbreeding depression in collared flycatchers (Ficedula albicollis)

The causes and magnitude of inbreeding depression are of considerable importance for a wide range of issues in evolutionary and conservation biology, but we have only a limited understanding of inbreeding depression in natural populations. Here, we present a study of inbreeding in a large wild population of collared flycatchers (Ficedula albicollis). Inbreeding was rare, to the extent that we detected only 1.04% of 2139 matings over 18 years that resulted in offspring with a non-zero inbreeding coefficient, f > 0. When it did occur, inbreeding caused a significant reduction in the egg-hatching rate, in fledgling skeletal size and in post-fledging juvenile survival, with the number of offspring being recruited to the breeding population from a nest of f = 0.25 being reduced by 94% relative to a non-inbred nest. A maximum-likelihood estimate of the number of lethal equivalents per gamete was very high at B = 7.47, indicating a substantial genetic load in this population. There was also a non-significant tendency for inbreeding depression to increase with the strength of selection on a trait. The probability of mating between close relatives (f = 0.25) increased throughout the breeding season, possibly reflecting increased costs of inbreeding avoidance. Our results illustrate how severe inbreeding depression and considerable genetic load may exist in natural populations, but detecting them may require extensive long-term datasets.     

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.     

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.     

Fertility assurance through extrapair fertilizations and male paternity defense

Extrapair paternity has been observed in many formally monogamous species. Male pursuit of extrapair fertilizations is explained by the advantages of having offspring that receive essential paternal care from other males. Since females are capable of exercising a degree of control over the post-copulatory sperm competition, extrapair paternity cannot persist unless it confers fitness benefits on cuckolding females. Thus, extrapair paternity involves cooperation between mated females and extrapair males. On the other hand, paired males frequently exhibit strategies that minimize their loss of paternity and/or conserve paternal investment if paternity is lost. Hence, extrapair attributes of diverse species and populations reported in the literature are particular solutions of evolutionary games involving gender-specific cuckolding/anti-cuckolding strategies. Here we use methods of evolutionary game theory to study the role of male paternity guarding strategies in situations where females seek extrapair fertilizations for reasons of genetic compatibility and/or in pursuit of genetic diversity for their offspring. Our results indicate that in these circumstances pursuit of extrapair fertilizations is the only evolutionary stable female strategy. Males, on the other hand, have two, mutually exclusive, evolutionary stable strategies: full time pursuit of extrapair fertilizations and a compromise strategy wherein they protect in-pair paternity during their mate's fertile periods and pursue extrapair paternity the rest of the time. The relative merits of these two strategies are determined by the efficiency of male in-pair paternity defense, breeding synchrony, fitness advantages of extrapair over in-pair offspring, and the intensity of competition for extrapair fertilizations from floater males.     

Certainty of paternity and paternal effort in the collared flycatcher

Models of optimal parental investment predict that variationin certainty of paternity can affect the optimal level of paternalinvestment when a male's expected paternity in different nestingattempts is not fixed throughout his lifetime. Several attemptsto test this prediction experimentally in monogamous birds havefailed to induce a reduction in care by males. This may be becausethe method used, detaining males, is a poor model for what happenswhen a male's certainly of paternity is naturally reduced. Wecaught and detained female collared flycatchers Ficedula albicollisfor 1 h immediately after laying on one or two occasions inan attempt to induce variation in certainty of paternity forthe males they were mated to. By capturing females immediatelyafter laying we hoped to exploit the existence of an "inseminationwindow" since males should be very sensitive to female absenceduring this period. The general effect of the experimental manipulationwas consistent with reduced certainty of paternity: males respondedby reducing their level of paternal care to nestlings, and malesmated to females that had been caught on one morning fed nestlingssignificantly less often and made a smaller share of feedingvisits than males mated to control females. The effects of theexperiment were generally weak, however, and we argue that certaintyof paternity may be fixed well before egg laying, in which caseexperimental manipulations are unlikely to have large effects.It is difficult to predict die effects of natural variationin certainty of paternity on levels of male paternal care becausedifferential allocation by females mated to attractive malesmay act in the opposite direction     

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.     

Degree of protandry reflects level of extrapair paternity in migratory songbirds

Males of most migratory organisms, including many birds, precede female conspecifics on their journey to the breeding areas. Several hypotheses have been proposed to explain the evolution of protandrous migration, yet they have rarely been tested at the interspecific level. Here, we provide correlational support for the “mate opportunity” hypothesis, which assumes that selection favours protandry in polygynous species where males gain significant fitness benefits from arriving earlier than females. Drawing on phenological data collected at two northern European stopover sites, we show that the time-lag in spring passage between males and females of five Palearctic migratory songbird species is positively associated with levels of extrapair paternity available from the literature. This suggests that males arrive relatively more in advance of females in species with high sperm competition where sexual selection through female choice is intense. Thus, protandry may arise from selection on the relative arrival timing of males and females rather than from selection within one of the sexes.     

Food supplementation affects extrapair paternity in house sparrows (Passer domesticus)

Extrapair paternity (EPP) is common among birds, but the reasonswhy it varies within and among species are less clear. In particular,few studies have experimentally examined how food availabilityinfluences paternity and sexual behavior. We manipulated foodsupply in a nest-box population of house sparrows, Passer domesticus,a colonial passerine with extensive biparental care. Duringthree successive breeding attempts, we changed food availabilityat nest sites and examined behavior and genetic parentage. DNAfingerprinting revealed that the level of EPP within broodswas five times lower in pairs nesting at sites continuouslysupplied with extra food. With extra food, mates spent longertime together at the nest, but this was mainly due to a changein female behavior; females but not males increased total nestattendance. Moreover, we found that individual males did notchange within-pair copulation frequency across treatments, suggestingthat our experiment did not influence male control over fertilizationsthrough copulation behavior. Instead, our study shows that ecologicalfactors can have a strong influence on the time budgets of malesand females, which consequently affects the occurrence of EPP.     

Female collared flycatchers learn to prefer males with an artificial novel ornament

We experimentally investigated whether learning from previousexperiences can lead to the establishment of a new mate preferencein a wild population of birds. During year one (2001), 63 femalecollared flycatchers (Ficedula albicollis) bred together withmales that we had provided with a novel trait, a red stripeon their white forehead patch (a sexually selected trait). Somecolor patterns of birds are largely determined by a few genes,and this experiment was designed to mimic the occurrence ofmutations in such genes. In the subsequent year (2002), we foundthat females with previous experience with red-striped maleswere more likely to pair with red-striped males (76%) than withcontrol males. By contrast, naïve females (i.e., with noprevious experience with red-striped males) were not more likelyto pair with red-striped males (44%) than with control males.Females paired with red-striped males produced more offspringthan females paired with control males, suggesting that maleswith the novel trait had become favored by selection. Thus,female collared flycatchers appear to quickly learn to associatea novel trait with a suitable mate that, in turn, leads to assortativemating between local mates (i.e., males with the new trait andfemales with previous experience of the new trait). Our resultsprovide support for the notion that learning may play an importantrole when the co-evolution of preferences and preferred traitstakes different routes in different populations of the samebird species.     

Male parental care, female reproductive success, and extrapair paternity

Birds differ considerably in the degree of male parental care,and it has been suggested that interspecific variation in extrapairpaternity is determined by the relative importance of benefitsto females from male parental care and good genes from extrapairsires. I estimated the relationship between extrapair paternityand the importance of male parental care for female reproductivesuccess mainly based on male removal studies, using a comparativeapproach. The reduction in female reproductive success causedby the absence of a male mate was positively correlated withthe male contribution to feeding offspring. The frequency ofextrapair paternity was negatively related to the reductionin female reproductive success caused by the absence of a mate.This was also the case when potentially confounding variablessuch as developmental mode of offspring and sexual dichromatismwere considered. A high frequency of extrapair paternity occursparticularly in bird species in which males play a minor rolein offspring provisioning and in which attractive males providerelatively little parental care. Bird species with frequentextrapair paternity thus appear to be those in which directfitness benefits from male care are small, females can readilycompensate for the absence of male care, and indirect fitnessbenefits from extrapair sires are important.     

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.     

Male reed buntings do not adjust parental effort in relation to extrapair paternity

Parental effort is considered to be costly; therefore, malesare expected to provide less care to unrelated offspring. Theoreticalmodels suggest that males should either reduce their care tothe entire brood or alternatively distinguish between relatedand unrelated nestlings and direct provisioning to kin whenpaternity is in doubt. Reed buntings (Emberiza schoeniclus)have been found to have high levels of extrapair paternity (EPP,i.e., offspring of a male other than the male attending thenest; 55% of offspring), and males are therefore under strongselection pressure to adjust their parental effort accordingto the proportion of EPP in their brood. In this study, we investigatedwhether male reed buntings exhibit a reduction in paternal care(incubation and provisioning nestlings) in relation to decreasedpaternity. We also assess whether males bias their provisioningtoward kin. We measured incubation time, provisioning rates,and food allocation to individual nestlings using video recordingsat the nests. Microsatellite DNA analysis was used to analyzethe paternity of offspring. In direct contrast to a previousstudy on the same species, our results provided no indicationthat males lowered their effort with decreased paternity. Furthermore,in nests of mixed paternity, males did not bias their provisioningbehavior to kin. It remains to be investigated whether the absenceof a relationship between paternity and paternal care can beascribed to absence of reliable paternity cues or whether thebenefits of reducing paternal care did not outweigh the costsin our study population. We found no evidence that the levelof paternal care affected male survival or offspring mass, suggestingthat both the benefits and costs of any reduction in paternalcare would have been low.