Eszter Szász

Among-year variation in the repeatability, within- and between-individual, and phenotypic correlations of behaviors in a natural population

When mean behaviors correlate among individuals, they form behavioral syndromes. One way to understand the evolution of such a group-level phenomenon is to compare horizontally patterns of correlations among populations (or species) or follow longitudinally the same population over years in the light of parallel differences in the environment. We applied the longitudinal approach to 8-year field data and analyzed phenotypic correlations, and their within- and between-individual components, among three behaviors (novelty avoidance, aggression, and risk-taking) in male collared flycatchers, Ficedula albicollis, in a meta-analytic framework. The phenotypic correlation between novelty avoidance and aggression varied heterogeneously (it was positive in some years, while it was negative in other years), while the other pair-wise correlations were consistently positive over the study period. We investigated four potential socio-ecological factors, and found evidence that the among-year alterations in the demographic structure of the population (density, age composition) can be responsible for the heterogeneous effect sizes. Comparing within- and between-individual correlations across pairs of traits, we found that the correlation between aggression and risk-taking at the among-individual level was the strongest suggesting that this relationship has the highest potential to form a behavioral syndrome. Within-year repeatabilities varied among traits, but were systematically higher than between-year repeatabilities. Our study highlights on an empirical basis that there can be several biological and statistical reasons behind detecting a phenotypic correlation in a study, but only few of these imply that fixed behavioral syndromes are maintained in a natural population. In fact, some correlations seem to be shaped by environmental fluctuations.

The relationship between DRD4 polymorphisms and phenotypic correlations of behaviors in the collared flycatcher

There is increasing evidence that the genetic architecture of exploration behavior includes the dopamine receptor D4 gene (DRD4). Such a link implies that the within-individual consistency in the same behavior has a genetic basis. Behavioral consistency is also prevalent in the form of between-individual correlation of functionally different behaviors; thus, the relationship between DRD4 polymorphism and exploration may also be manifested for other behaviors. Here, in a Hungarian population of the collared flycatcher, Ficedula albicollis, we investigate how males with distinct DRD4 genotypes differ in the consistent elements of their behavioral displays during the courtship period. In completely natural conditions, we assayed novelty avoidance, aggression and risk-taking, traits that were previously shown repeatable over time and correlate with each other, suggesting that they could have a common mechanistic basis. We identified two single-nucleotide polymorphisms (SNP554 and SNP764) in the exon 3 of the DRD4 gene by sequencing a subsample, then we screened 202 individuals of both sexes for these SNPs. Focusing on the genotypic variation in courting males, we found that “AC” heterozygote individuals at the SNP764 take lower risk than the most common “AA” homozygotes (the “CC” homozygotes were not represented in our subsample of males). We also found a considerable effect size for the relationship between SNP554 polymorphism and novelty avoidance. Therefore, in addition to exploration, DRD4 polymorphisms may also be associated with the regulation of behaviors that may incur fear or stress. Moreover, polymorphisms at the two SNPs were not independent indicating a potential role for genetic constraints or another functional link, which may partially explain behavioral correlations.

Aggressive behavior of the male parent predicts brood sex ratio in a songbird

Brood sex ratio is often affected by parental or environmental quality, presumably in an adaptive manner that is the sex that confers higher fitness benefits to the mother is overproduced. So far, studies on the role of parental quality have focused on parental morphology and attractiveness. However, another aspect, the partner’s behavioral characteristics, may also be expected to play a role in brood sex ratio adjustment. To test this hypothesis, we investigated whether the proportion of sons in the brood is predicted by the level of territorial aggression displayed by the father, in the collared flycatcher (Ficedula albicollis). The proportion of sons in the brood was higher in early broods and increased with paternal tarsus length. When controlling for breeding date and body size, we found a higher proportion of sons in the brood of less aggressive fathers. Male nestlings are more sensitive to the rearing environment, and the behavior of courting males may often be used by females to assess their future parental activity. Therefore, adjusting brood sex ratio to the level of male aggression could be adaptive. Our results indicate that the behavior of the partner could indeed be a significant determinant in brood sex ratio adjustment, which should not be overlooked in future studies.

Sex ratio adjustment in birds

Abstract In a number of bird species, the sex ratio of the broods is not random, instead it is related to parental quality and environmental conditions. Several hypotheses have been proposed to explain this phenomenon, the so called sex ratio adjustment. According to these hypotheses, sex ratio adjustment is expected to evolve when the fitness benefit an offspring confers to the parents changes with ecological or social factors in a sex-specific way. Though many correlative and experimental studies support these hypotheses, there are still unresolved problems. In our paper, we provide details on the hypotheses related to sex ratio adjustment and explanations for the differences observed in sex ratio patterns between populations and years. Finally, we discuss the importance of sex ratio adjustment for species conservation. Összefoglalás Számos madárfajnál kimutatták, hogy a fészekaljak ivararánya nem véletlenszerű, hanem a szülői vagy környezeti tulajdonságok függvényében változik. Az ivararány-manipuláció néven ismert jelenség magyarázatára számos elméletet dolgoztak ki. Ezek szerint az ivararány-manipuláció azokban az esetekben alakulhat ki az evolúció során, amikor a hím és tojó utódok túlélése, várható szaporodási sikere vagy felnevelési költsége eltér. Bár számos korrelatív és kísérletes vizsgálat támogatja ezeket a hipotéziseket, vannak még az ivararány-manipulációval kapcsolatban megoldatlan kérdések. Cikkünkben részletesen tárgyaljuk az ivararány-manipulációt magyarázó elméleteket, valamint az ivararány-mintázatok populációk és vizsgálati évek közötti eltéréseinek lehetséges okait. Kitérünk a jelenség természetvédelmi jelentőségére is.

Escape ability and risk-taking behaviour in a Hungarian population of the collared flycatcher ( Ficedula albicollis )

Risk-taking decisions in front of a predator are crucial for the fitness of the animals. Risk-taking behaviour can be hypothesised to depend on escape ability, which is difficult to study in the wild. In this field study, we investigated whether escape ability (i) is a consistent individual-specific characteristic and (ii) can explain between-individual variation in risk-taking behaviour in male collared flycatchers (Ficedula albicollis). We estimated escape ability by the time that was needed to capture individuals by hand in an outdoor aviary during both the courtship and the nestling feeding phases. We estimated risk-taking by human-induced flight initiation distance (FID) and parental nest-defence behaviour. We also measured variables that reflect individual quality and condition to assess how these affect escape ability. Time to capture was weakly repeatable in the within- and between-season contexts, but was considerably repeatable within a day. We found that time to capture decreased between courtship and nestling feeding phases, probably due to parallel changes in body condition (as shown by the systematic decline of individual body mass between phases correlating with within-individual changes in time to capture). Overall, time to capture was not significantly related to risk-taking behaviour, but we found a negative correlation between time to capture and FID in yearlings. In conclusion, escape ability in flycatchers seems to be a condition-dependent plastic trait, and it has the potential to affect immediate risk-taking decisions.Significance statementWe investigated the proximate determinants of escape ability in collared flycatcher males and whether this trait can be a potential driver of risk-taking behaviour, which is a rarely considered issue. We measured escape ability as time needed to capture birds in an outdoor aviary by hand. We found that escape ability was repeatable only in a short-term context, and differed between the courtship and chick-feeding periods, probably due to parallel changes in body condition. Furthermore, escape ability in yearlings (but not in adults) correlated with an estimate of risk-taking in the wild indicating that males with better ability to escape take higher risk. Our findings highlight that individual decisions about risk-taking might partially rely on how individuals assess their potential escape success.

Unravelling the relationships between life history, behaviour and condition under the pace-of-life syndromes hypothesis using long-term data from a wild bird

The hypothesis of pace-of-life syndromes (POLS) predicts relationships between traits including life history traits and risk-taking behaviour that can be mediated by the trade-off between current and future reproductive value. However, alternative causal mechanisms may also generate covariance among these traits without trade-offs. We investigated the relationships between survival to the next year, current reproductive investment and risk-taking behaviour (flight initiation distance) in male collared flycatchers, Ficedula albicollis, using long-term data. We used structural equation modelling (SEM) to uncover whether the associations among traits are mediated by a common latent factor that determines how individuals balance the trade-off between current and future reproductive value. As trade-offs could be concealed when there are differences in resource acquisition between individuals, we also included potential causes of these differences, body mass and body size, in the analysis. We found that risk-taking behaviour was positively related to reproductive investment and negatively to survival to the next year as could be predicted if investment into a risky behaviour is traded against future prospects. However, the most supported SEM model also suggested that survival to the next year was positively related to current reproductive investment, contrary to predictions of a hypothesis based on trade-off. These results remained qualitatively similar when controlling for body condition. In conclusion, we only could derive partial support for the POLS hypothesis. We suggest that aspects of individual quality, and not only trade-offs, should also be considered when interpreting the relationships between life history and behavioural traits.Significance statementWe investigated the association between two life history components (survival to the next year and current reproductive effort) and risk-taking behaviour, relying on long-term records from a passerine bird, to investigate the predictions of the pace-of-life syndrome (POLS) hypothesis. Using structural equation modelling, we found support for a causal model that implies that risk-taking negatively affects survival to the next year and that survival to the next year and current reproductive effort are strongly and positively associated. Controlling for the effect of body condition did not fundamentally change these relationships. We could not find conclusive evidence for the investigated traits being mediated by a common underlying factor, as generally predicted by the POLS hypothesis. However, the sign of the relationship between risk-taking behaviour and survival to the next year was as predicted by the POLS hypothesis.

Rearing conditions have long-term sex-specific fitness consequences in the collared flycatcher

Lay Summary Early-life conditions have stronger effects on the fitness of male than female collared flycatchers. Male nestlings from experimentally enlarged broods had fewer eggs from their mates during their life than male nestlings from reduced broods, which was a consequence of their shorter breeding lifespan. In females, rearing conditions had no effect on fitness. Together with earlier results, we show that although sex differences in growth disappear by fledging, the greater sensitivity of males had lifelong consequences.

A test on within-individual changes in risk-taking behaviour due to experience to predation in the Collared Flycatcher (Ficedula albicollis)

Summary Different experiences from the past may have influence on individual’s behaviour through feedback mechanisms that can weaken or preserve the within-individual consistency of behavioural traits. Here, we aimed to find evidence for such feedback mechanisms that may operate on risk-taking behaviour via the effect of former experience to potential predation events in male Collared Flycatchers (Ficedula albicollis). We predicted that risk-taking of males would decrease after experiencing a predator’s attack in previous breeding seasons (negative feedback). We assessed risk-taking by flight initiation distance (FID) that is the distance at which an individual flees from an approaching predator, which was estimated for 234 individuals from different breeding seasons. Information on predation experience (i.e. occurrence of nest predation, the incidence of capture by human observers) was available from our long-term database on individual life histories. In a horizontal approach, we found no difference in FID when comparing males with former experience to predation with males naive to predators. A longitudinal approach relying on the repeated tests of the same individuals from different years yielded analogous results, we could not show a significant change in the risk-taking behaviour of the males as a consequence of experience to predation in past years. However, we found that individuals systematically took less risk over the years, which might be a consequence of acquiring general experience with age.