Ákos Pogány

Individual variation and the resolution of conflict over parental care in penduline tits

Eurasian penduline tits (Remiz pendulinus) have an unusually diverse breeding system consisting of frequent male and female polygamy, and uniparental care by the male or the female. Intriguingly, 30 to 40 per cent of all nests are deserted by both parents. To understand the evolution of this diverse breeding system and frequent clutch desertion, we use 6 years of field data to derive fitness expectations for males and females depending on whether or not they care for their offspring. The resulting payoff matrix corresponds to an asymmetric Snowdrift Game with two alternative evolutionarily stable strategies (ESSs): female-only and male-only care. This, however, does not explain the polymorphism in care strategies and frequent biparental desertion, because theory predicts that one of the two ESSs should have spread to fixation. Using a bootstrapping approach, we demonstrate that taking account of individual variation in payoffs explains the patterns of care better than a model based on the average population payoff matrix. In particular, a model incorporating differences in male attractiveness closely predicts the observed frequencies of male and female desertion. Our work highlights the need for a new generation of individual-based evolutionary game-theoretic models.

Sexual conflict and consistency of offspring desertion in Eurasian penduline tit Remiz pendulinus

BackgroundThe trade-off between current and future parental investment is often different between males and females. This difference may lead to sexual conflict between parents over care provisioning in animals that breed with multiple mates. One of the most obvious manifestations of sexual conflict over care is offspring desertion whereby one parent deserts the young to increase its reproductive success at the expense of its mate. Offspring desertion is a wide-spread behavior, and its frequency often varies within populations. We studied the consistency of offspring desertion in a small passerine bird, the Eurasian penduline tit Remiz pendulinus, that has an extremely variable breeding system. Both males and females are sequentially polygamous, and a single parent (either the male or the female) incubates the eggs and rears the young. About 28–40% of offspring are abandoned by both parents, and these offspring perish. Here we investigate whether the variation in offspring desertion in a population emerges either by each individual behaving consistently between different broods, or it is driven by the environment.ResultsUsing a three-year dataset from Southern Hungary we show that offspring desertion by females is consistent between nests. Male desertion, however, depends on ambient environment, because all males desert their nests early in the season and some of them care late in the season. Therefore, within-population variation in parental care emerges by sexually different mechanisms; between-individual variation was responsible for the observed pattern of offspring desertion in females, whereas within-individual variation was responsible for the observed pattern in males.ConclusionTo our knowledge, our study is the first that investigates repeatability of offspring desertion behavior in nature. The contrasting strategies of the sexes imply complex evolutionary trajectories in breeding behavior of penduline tits. Our results raise an intriguing question whether the sexual difference in caring/deserting decisions explain the extreme intensity of sexual conflict in penduline tits that produces a high frequency of biparentally deserted (and thus wasted) offspring.

Nest desertion is not predicted by cuckoldry in the Eurasian penduline tit

Engagement in extra-pair copulations is an example of the abundant conflicting interests between males and females over reproduction. Potential benefits for females and the risk of cuckoldry for males are expected to have important implications on the evolution of parental care. However, whether parents adjust parental care in response to parentage remains unclear. In Eurasian penduline tits Remiz pendulinus, which are small polygamous songbirds, parental care is carried out either by the male or by the female. In addition, one third of clutches is deserted by both male and female. Desertion takes place during the egg-laying phase. Using genotypes of nine microsatellite loci of 443 offspring and 211 adults, we test whether extra-pair paternity predicts parental care. We expect males to be more likely to desert cuckolded broods, whereas we expect females, if they obtain benefits from having multiple sires, to be more likely to care for broods with multiple paternity. Our results suggest that parental care is not adjusted to parentage on an ecological timescale. Furthermore, we found that male attractiveness does not predict cuckoldry, and we found no evidence for indirect benefits for females (i.e., increased growth rates or heterozygosity of extra-pair offspring). We argue that male Eurasian penduline tits may not be able to assess the risk of cuckoldry; thus, a direct association with parental care is unlikely to evolve. However, timing of desertion (i.e., when to desert during the egg-laying phase) may be influenced by the risk of cuckoldry. Future work applying extensive gene sequencing and quantitative genetics is likely to further our understanding of how selection may influence the association between parentage and parental care.

Parental Behavior and Reproductive Output in Male-Only Cared and Female-Only Cared Clutches in the Eurasian Penduline Tit (Remiz pendulinus)

ABSTRACT. Diverse patterns of parental care, including uniparental care by either the male or the female, provide excellent opportunities to investigate how variation in social traits is maintained in wild populations. Coexistence of different parental strategies within the same population is expected when they exhibit similar cost-benefit ratios. We investigated one of the most diverse avian breeding systems and compared parental behavior and reproductive output between nests that are uniparentally cared for by male or female Eurasian Penduline Tits (Remiz pendulinus). In this small passerine bird, full care (incubation and brood care) is provided by the male only (7–18% of nests) or the female only (48–65% of nests). Additionally, a third of all nests are deserted by both parents as a result of intense sexual conflict over care. We show that parental effort is similar between male and female parents, and they achieve similar offspring survival after controlling for clutch-size differences. Females care for larger clutches than males (5.7 ± 0.1 [SE] and 3.5 ± 0.2 eggs, respectively), and they produce more nestlings (3.6 ± 0.2 and 2.4 ± 0.3 nestlings, respectively), although this difference is not significant at fledging of the chicks (3.1 ± 0.2 and 2.4 ± 0.3 young, respectively). Therefore, sex difference in care does not explain the bias toward female-only care in Eurasian Penduline Tits. We propose that the differential benefits of desertion and/or the differential costs of care for males and females facilitate the existence of both uniparental care types in the population.

Sexual conflict predicts morphology and behavior in two species of penduline tits

BackgroundThe evolutionary interests of males and females rarely coincide (sexual conflict), and these conflicting interests influence morphology, behavior and speciation in various organisms. We examined consequences of variation in sexual conflict in two closely-related passerine birds with contrasting breeding systems: the Eurasian penduline tit Remiz pendulinus (EPT) exhibiting a highly polygamous breeding system with sexually antagonistic interests over parental care, and the socially monogamous Cape penduline tit Anthoscopus minutus (CPT). We derived four a priori predictions from sexual conflict theory and tested these using data collected in Central Europe (EPT) and South Africa (CPT). Firstly, we predicted that EPTs exhibit more sexually dimorphic plumage than CPTs due to more intense sexual selection. Secondly, we expected brighter EPT males to provide less care than duller males. Thirdly, since song is a sexually selected trait in many birds, male EPTs were expected to exhibit more complex songs than CPT males. Finally, intense sexual conflict in EPT was expected to lead to low nest attendance as an indication of sexually antagonistic interests, whereas we expected more cooperation between parents in CPT consistent with their socially monogamous breeding system.ResultsConsistent with our predictions EPTs exhibited greater sexual dimorphism in plumage and more complex song than CPTs, and brighter EPT males provided less care than duller ones. EPT parents attended the nest less frequently and less simultaneously than CPT parents.ConclusionsThese results are consistent with sexual conflict theory: species in which sexual conflict is more manifested (EPT) exhibited a stronger sexual dimorphism and more elaborated sexually selected traits than species with less intense sexual conflict (CPT). Our results are also consistent with the notion that EPTs attempt to force their partner to work harder as expected under sexual conflict: each member of the breeding pair attempts to shift the costs of care to the other parent. More brightly colored males benefit more from desertion than dull ones, because they are more likely to remate with a new female. Taken together, the comparison between two closely related species with contrasting breeding systems suggest that sexual conflict over care has influenced the evolution of behavior and morphology in penduline tits.

Mate preference does not influence reproductive motivation and parental cooperation in female zebra finches

In socially monogamous species, low availability of sexually active unpaired individuals in the local population may constrain mate choice, resulting in mating with sub-optimal partners. Here we experimentally investigate whether female reproductive behaviour is different when paired with a preferred or a non-preferred male in the zebra finch (Taeniopygia guttata). First, we assessed female mating preferences using a four-way choice apparatus, then females were caged together with either their preferred or least-preferred male. Female reproductive motivation, assessed by the propensity of laying eggs within two weeks from pairing and clutch mass, did not differ between the two experimental groups. Females responded to mate removal by either increasing their care, so as to compensate for the lost care of their mate, or by significantly reducing incubation. This bimodal response was not explained by mate preference, nevertheless, we found that females with lower baseline (i.e., pre-manipulation) incubation effort were more likely to cease incubation during mate removal. Taken together, we found no evidence that female reproductive behaviour varies along with mate preference.

Zebra finch nestlings, rather than parents, suffer from raising broods under low nutritional conditions

In sexually reproducing species, parents and offspring have different optima in terms of the amount of parental investment. For offspring, higher investment than the parental optimum generally increases their fitness. However, such higher investment will, in theory, result in net parental fitness loss because increased benefits from current offspring will be more than offset by a potential decrease in parental survival or future reproduction. Whether and how parents respond to a shortfall in resources might therefore have important fitness consequences. Here, we manipulate the nutritional condition of captive zebra finch families to investigate how variation in environmental conditions influences parental resource allocation between themselves and their offspring. By allowing the same zebra finch pairs to raise one brood under high and another brood under low nutritional conditions, we found that parents lost more body mass and their offspring grew at slower rates under low nutritional conditions. Therefore, both parents and their offspring were affected by the nutritional treatments. Offspring incurred greater costs, because slower growth rates under low nutritional conditions resulted in an overall lower body mass of nestlings after reaching independence. Nutritional treatments had sex-specific effects on parental body mass, because, in contrast to fathers, only mothers recouped their losses under high nutritional conditions. Furthermore, both parents spent less time brooding their nestlings under low nutritional conditions. Parental strategies hence vary with the nutritional quality of their food, even in captivity, supporting the idea that parental resource allocation may be driven by the expected costs and benefits from current offspring.Significance statementParental care is among the most influential traits affecting fitness in many sexually reproducing animals. The more care offspring receive, the higher their chances of survival and reproduction. However, caring for their young does not only provide benefits for parents: all costs of parental care are paid by them. Parental resource allocation is therefore expected to be optimised. But how should parents respond to changing environmental conditions when they are already breeding? By manipulating nutritional conditions in a captive population of zebra finches Taeniopygia guttata, we show that both parents and their offspring lose body mass under low nutritional conditions. The effect on offspring was more pronounced and long lasting, and parents also decreased their parental effort. Our results show plasticity in parental investment of zebra finches in response to nutritional conditions and reproductive value of their offspring.

Differences in pre-sleep activity and sleep location are associated with variability in daytime/nighttime sleep electrophysiology in the domestic dog

The domestic dog (Canis familiaris) is a promising animal model. Yet, the canine neuroscience literature is predominantly comprised of studies wherein (semi-)invasive methods and intensive training are used to study awake dog behavior. Given prior findings with humans and/or dogs, our goal was to assess, in 16 family dogs (1.5–7 years old; 10 males; 10 different breeds) the effects of pre-sleep activity and timing and location of sleep on sleep electrophysiology. All three factors had a main and/or interactive effect on sleep macrostructure. Following an active day, dogs slept more, were more likely to have an earlier drowsiness and NREM, and spent less time in drowsiness and more time in NREM and REM. Activity also had location- and time of day-specific effects. Time of day had main effects; at nighttime, dogs slept more and spent less time in drowsiness and awake after first drowsiness, and more time in NREM and in REM. Location had a main effect; when not at home, REM sleep following a first NREM was less likely. Findings are consistent with and extend prior human and dog data and have implications for the dog as an animal model and for informing future comparative research on sleep.

Social learning from conspecifics and humans in dog puppies

Social learning is especially advantageous for young individuals because it reduces the risks of trial-and-error learning, while providing an efficient way of acquiring information. Whereas adult dogs are known to excel in social learning skills, the ontogeny of this process has been mainly overlooked. The focus of our study was to investigate whether the capacity of social learning is already developed in dogs at an early age. We tested 8-week-old dog puppies on their ability to learn socially to open a puzzle box baited with food and on their capacity to retain the acquired information in their memory. Puppies were tested with conspecific and human demonstrators. We further investigated on whether demonstrations performed by their mother or by an unfamiliar conspecific model affected puppies’ learning trend differently. We found that social learning skills are present in 8 weeks old puppies and they remembered this experience for 1 hour. Puppies learned to solve the task from both conspecific and human demonstrators, thereby endorsing dogs’ flexibility in learning from different social partners. Unexpectedly, puppies were more likely to learn from unfamiliar conspecifics than from their mother, probably as a result of greater attention payed to the demonstration performed by the unfamiliar model.

Diurnal and Reproductive Stage-Dependent Variation of Parental Behaviour in Captive Zebra Finches

Parental care plays a key role in ontogeny, life-history trade-offs, sexual selection and intra-familial conflict. Studies focusing on understanding causes and consequences of variation in parental effort need to quantify parental behaviour accurately. The applied methods are, however, diverse even for a given species and type of parental effort, and rarely validated for accuracy. Here we focus on variability of parental behaviour from a methodological perspective to investigate the effect of different samplings on various estimates of parental effort. We used nest box cameras in a captive breeding population of zebra finches, Taeniopygia guttata, a widely used model system of sexual selection, intra-familial dynamics and parental care. We investigated diurnal and reproductive stage-dependent variation in parental effort (including incubation, brooding, nest attendance and number of feedings) based on 12h and 3h continuous video-recordings taken at various reproductive stages. We then investigated whether shorter (1h) sampling periods provided comparable estimates of overall parental effort and division of labour to those of longer (3h) sampling periods. Our study confirmed female-biased division of labour during incubation, and showed that the difference between female and male effort diminishes with advancing reproductive stage. We found individually consistent parental behaviours within given days of incubation and nestling provisioning. Furthermore, parental behaviour was consistent over the different stages of incubation, however, only female brooding was consistent over nestling provisioning. Parental effort during incubation did not predict parental effort during nestling provisioning. Our analyses revealed that 1h sampling may be influenced heavily by stochastic and diurnal variation. We suggest using a single longer sampling period (3h) may provide a consistent and accurate estimate for overall parental effort during incubation in zebra finches. Due to the large within-individual variation, we suggest repeated longer sampling over the reproductive stage may be necessary for accurate estimates of parental effort post-hatching.