Edited by: James Luke Savage, University of Sheffield, United Kingdom
Reviewed by: Elizabeth Adkins-Regan, Cornell University, United States; Simon Charles Griffith, Macquarie University, Australia
This article was submitted to Behavioral and Evolutionary Ecology, a section of the journal Frontiers in Ecology and Evolution
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Parental care is among the most widespread and variable behavioral traits between and within species, associated often both with large fitness costs and benefits. Despite its fitness consequences and evolutionary significance, we know very little about the ontogeny of this behavior, specifically, whether and how social experiences from parents contribute to the development of parental care. Here we used a split-family experimental design to produce uniparentally raised zebra finch nestlings that were provisioned either only by their mother or their father from shortly after hatching until independence. We investigated whether zebra finch nestlings pay attention to who takes care of them (short-term social effects) and whether parental sex roles, i.e., how much each parent provides to offspring, are socially learned and how these early social experiences influence negotiation rules of parental effort as adults (long-term social effects). We found pronounced short-term effects: uniparentally raised young socialized more with their “caring” than with their “non-caring” parent in a two-way choice test and begged more for food from them. When paired as adults based on their caring parent, some combinations of these uniparentally raised finches did not coordinate normally during incubation as first-time parents. By nestling provisioning (and their second breeding) even these pairs assumed normal distribution of parental effort and we therefore conclude that early social experiences influence parental sex roles and coordination, but these can be overridden by own social experiences with the mate when starting to breed.
Parental care is among the most beneficial, and, at the same time, among the costliest traits that influence fitness. The large impact on survival and future reproduction on each family member selects for coordination between parental and offspring behaviors, to balance the benefits of offspring needs being satisfied and the costs of parental effort. In species with biparental care (the prevalent type in birds, with ca. 90% of species), both parents contribute to provisioning the offspring (Cockburn,
Theoretical models distinguish two possible ways to resolve sexual conflict over care in biparental species. If parental effort has evolved to a fixed best effort in relation to the parental effort of the other sex, and pair members cannot change their effort dynamically based on the effort of their partner, the resolution is reached on an evolutionary time scale (“sealed bid” model; Houston and Davies,
Although theoretical models along with empirical studies have provided a more in-depth view at the selection pressures shaping parental care, we are far from a comprehensive understanding of how parental care patterns evolve and develop. Specifically, we know very little about how parental sex roles and negotiation rules are passed on from one generation to the next. The behavioral flexibility implied in the negotiation models suggests that learning may play an important role for parental care. This is likely to affect also offspring experience, potentially resulting in social inheritance of parental care patterns. Social inheritance can have numerous advantages over genetic inheritance, including faster response and more flexibility to environmental changes (including the social environment; Boyd and Richerson,
Choosing the zebra finch allowed us to build our study on a growing body of research that uses this species as model to understand how sex roles and sexual conflict are shaped by social experience. First, research into various aspects of sexual imprinting (i.e., the process by which young socially learn about the characteristics of its species and later sexual partners) provided insights into the significance of social learning with regards to sex roles using this small passerine (Immelmann,
We used a split-family experimental design to investigate how social experiences with parents influence from which parent offspring prefer to solicit care, which parental sex roles they assume as adults and how they coordinate parental care. Zebra finch families were divided to male-only and female-only cared half-broods shortly after hatching. Families were split so that the social structure of the family, as well as acoustic, olfactory and visual contact between parents and all offspring were maintained, although each offspring could receive care from only one of their parents (“caring parent” henceforth). We then tested whether recently fledged (i.e., still dependent), zebra finch nestlings pay attention to who takes care of them (short-term effects of uniparental care). Specifically, the experiment allowed us to answer the following questions: (1.1) do uniparentally raised offspring express preference toward their caring over their non-caring parent? We expected young to socialize more with (i.e., spend more time close to) the parent that provisioned them, and also, to expect (beg for) food from this parent. (1.2) If offspring prefer their caring parent, is this preference generalized to parental sex? We expected offspring to socialize more with and beg food from non-kin parents that are of similar sex to their social parent. (1.3) Are there sex differences in how parental sex roles are socially transferred? Parental sex roles are different and fine-tuning them to environmental changes may be more relevant to one sex than to the other. This would be reflected in offspring sex influencing preference in our experiment.
Once these experimental young fully matured, they were allowed to breed two times with other uniparentally raised birds to test how their own and their partners' social experience affected parental effort and coordination i.e., their share during incubation and offspring provisioning (long-term effects of uniparental care). The long-term experiment addressed the following specific research questions: (2.1) do early social experiences (or the lack of them) influence parental sex roles in uniparentally cared birds? If so, we expected parental effort to change based on the interaction of own sex and uniparental care type received (e.g., increased effort of a male-cared male as opposed to a female-cared male). (2.2) Does the lack of negotiation experiences from parents influence the same behavior (i.e., coordination) as adults? (2.3) If we detect differences in parental coordination, do own breeding experiences shape negotiation rules? If social experiences with the mate when breeding as adults also shape negotiation rules, we expected diminishing differences between our experimental groups from the first to the second breeding. (2.4) If we detect differences in parental coordination, do these influence reproductive success?
Our study was carried out between February 2013 and April 2015 at two locations; first, a study population of 47 breeding pairs (“parental generation” henceforth) was established from the domesticated stock of zebra finches at Bielefeld University, Germany (Forstmeier et al.,
We used a split-family design to investigate short- and long-term effects of whether nestlings experienced parental care from their mother or their father on their parental preferences as juveniles and on parental sex roles and negotiation as adults. When splitting the family at an early stage of post-hatching development, our aim was to maintain the social structure of the family as close to intact as possible. Broods, nests and cages were split in half, but separated by wire mesh so that nestlings in the adjacent nest boxes could also observe their siblings cared for by their other parent (
Split-family experimental manipulation to investigate the social effects of uniparental care in zebra finches. Following pair formation and biparental incubation, on day 8 post-hatching, a wire mesh separator was inserted that halved the cage. A parent and half of the brood were placed into each half-cage, and the nest material shared equally between two cardboard nest boxes. The back wall of the nest boxes was removed so that all family members remained in visual, acoustic, and olfactory contact with each other through the wire mesh, while offspring received provisioning from only one of their parents henceforth.
Following the establishment of random pairs in unseparated cages, zebra finches received coconut fibers as nest material and nest-building and egg-laying was monitored daily. We considered the reproductive stage as post-hatching from the date when the first egg hatched in a given clutch. On day 8 post-hatching, nestlings were individually marked by cutting their downy feathers on their wings, legs, head and back in a unique combination (Adam et al.,
When splitting the family, the wooden nest box was replaced by two cardboard nest boxes (each 12 × 12 × 12 cm), attached to the two sides of the wire mesh separator with their entrance facing toward the inside of the cage (
On day 12 post-hatching, uniparental offspring provisioning was recorded for 3 h (start of recording at 9:00) from outside the cage using digital camcorders fitted with SD cards. The camera view covered the whole cage, so that male-only and female-only care could be quantified. Nestling body mass was measured and nestlings were ringed by a numbered plastic ring for individual identification. On day 16 and 35 post-hatching body mass of nestlings were measured again.
Between day 25 and 27 post-hatching (i.e., when the offspring have already fledged but still depended on parental provisioning), we tested parental preference in a two-way choice apparatus set up in a separate room. The apparatus consisted of three compartments: one stimulus chamber (30 × 40 × 40 cm) on each side of a middle choice chamber (60 × 40 × 40 cm). Stimulus chambers contained one perch each, whereas the choice chamber contained three perches, dividing the choice chamber to three equal zones (left, neutral and right zones, with a perch indicating the center of each zone). To ensure young were hungry and parents were habituated to the choice apparatus, parents were moved to the two side chambers of the apparatus 2 h before the first preference test of the family started and food was removed from the home cages. Offspring were tested individually in a random order; the focal bird was first moved to a small start cage attached to the door of the choice chamber. After ca. 30 s acclimatization, the offspring was released into the choice chamber by remotely operating the door and was then allowed to move freely in the choice chamber for 10 min. After every offspring from a cage were tested in random order, the stimulus birds were swapped to the opposite stimulus chamber and the young were re-tested in the same order as previously to control for possible side effects.
All families (
The sexually mature birds of the second generation were allowed to breed two times. For the first breeding, pairs were formed following a randomized fractional factorial design (i.e., representing all four combinations based on own sex and sex of the caring parent, with control (biparentally cared) birds always paired with other biparentally cared birds). This resulted in the following successful breedings (own sex is given as small letters and the sex of the caring parent as capitals in parentheses, e.g., m(F)/f(M) is a pair in which the male was raised by his mother and the female by her father):
To increase statistical power, after the first successful breeding the focal male or female parent received his/her other potential partner. Pairs were formed by balancing care type to that of their first pair (e.g., a male that received a male-only cared female previously, now was allowed to pair with a female-only cared female). Similarly to their first breeding, biparentally cared control birds were allowed to pair with another biparentally cared bird. The second breeding attempt resulted in
Parental behavior of the breeding pairs was monitored using small digital cameras (Mobius Action Cam, JooVuu Store, UK) with wide-angle lenses (116° field of view) that were mounted to the nest boxes. The camera lenses could reach inside the nest through holes cut to the top of the nest boxes, providing a top view of the nest (Morvai et al.,
To assess the preference for socializing with each parent, we coded the time and frequency of visits to all three choice zones (i.e., to the male's zone, to the neutral zone and to the female's zone) from the video recordings of the preference tests using Solomon coder (Péter,
For each response variable, we calculated the relative response toward the male parent, e.g., for socializing, assessed by the relative time spent with each parent, we calculated the proportion of total time of the two (swapped) trials as:
Time spent in male parent's zone/(time spent in male parent's zone + time spent in female parent's zone)
Statistical analyses were carried out using the R statistical environment (v. 3.5.2; R Core Team,
Since relative time and relative frequency of visits to the parents (rP = 0.758,
In initial models, we tested for the two-way interactions between care type (male-only, female-only, or biparental) and offspring sex, and care type and repeat (only in the models of repeated tests). Furthermore, the possible confounding effects of season (number of days from 25 March i.e., from the start of the experiment), time of day and the exact duration of separation from the parents before the start of the test were analyzed, but since none of these had significant effects, they were excluded from the final models. Stepwise model selection was based on AIC values, and we considered a model to provide a better fit whenever its AIC was lower, and the difference was ≥2. The effects of explanatory variables were analyzed by likelihood ratio tests (LRT); we provide χ2 and the corresponding
We also investigated whether the strength of preference is predicted by the actual amount of care received from the parents using Pearson's correlation between the relative time offspring spent with the caring parent during the first preference test and nest attendance of the caring parent (proportion of time spent inside the nest) on day 12 post-hatching.
Probability to start breeding was analyzed in Cox Proportional Hazards Models (R package “survival,” Therneau,
From the within-nest box recordings taken on day 8 of incubation and day 10 post-hatching, we coded the following behaviors for each sex separately using Solomon coder: incubation, brooding, being inside the nest and feeding the nestlings (
From the behavioral codings, we calculated relative male attendance time as the proportion of observation time the male spent inside the nest divided by the sum of the time the male and female parents spent inside the nest during incubation and offspring provisioning, respectively. Relative male feeding visits and feeding time were calculated similarly. Besides individual behaviors, we also calculated joint behaviors (nest attendance and feeding); these represent events when both parents showed a given behavior at the same time.
Social learning of parental sex roles and coordination were analyzed in separate general linear models (LMs) with the above response variables (logit-transformed male parental effort relative to the sum of male and female effort). In each model, we tested for the effect of care type of the pair received as young (fixed factor with five levels [care type received by the male parent/female parent]: M/M, M/F, F/M, F/F, B/B). In addition, initial models of relative male parental effort during offspring provisioning included number of offspring.
The potential consequences of care type on reproductive success were analyzed at multiple levels; clutch size on day 8 of incubation and brood size on day 10 post-hatching were analyzed in separate ordinal logistic regressions (OLRs, R package “ordinal”; Christensen,
Parental preference of the young was influenced by the care type they received. Offspring spent more time socializing with the parent they had received care from (LMM of relative time spent in male's zone, LRT of models with and without care type:
Parental preference of zebra finch offspring based on their social experiences with each of their parents. Offspring spent more time socializing with
The actual amount of care that offspring received on day 12 post-hatching did not predict the strength of preference toward the caring parent in the first parental preference test (rP = 0.153,
Begging from each parent was also influenced by early social experiences with the parents. Offspring spent more time with begging food from the parent they received previous provisioning from (LMM of relative time spent begging in male's zone, LRT of care type:
Offspring sex did not influence socialization with or begging from parents (effect of care type × offspring sex interaction, in both above LMMs:
Repeated preference tests with non-familiar adults as stimuli in a subset of offspring revealed that the preference is not specific toward the parents, although it is more pronounced toward them (reflected in a two-way interaction between care type and repeat; LMM of relative time in male's zone, LRT of care type x repeat:
Parental preference of zebra finch offspring when offering them their own parents or non-familiar adults to choose from. Box groups of three represent relative time spent
Probability to start breeding was not different between pairs based on care type received as young (Cox model of latency to start breeding, LRT of care type:
Relative male parental effort during incubation was different between pairs of parents based on care type received as young (LMs of relative male nest attendance time, LRT of care type:
Division of parental effort and coordination in pairs of zebra finch parents during incubation based on their caring parents. The figure shows the proportion of time (mean ± SE) that parents spent inside their nest (i.e., total nest attendance with and without incubation) on day 8 of incubation. Male (filled square), female (filled circle), joint (empty diamond), and total effort (i.e., by at least one of the parents; empty triangle) are presented. Care categories are given in the order of male care/female care (e.g., B/B, biparentally cared male/biparentally cared female; F/M, female-only cared male/male-only cared female).
Relative male parental effort during offspring provisioning was not influenced by care type received as young (LMs of relative male nest attendance time, LRT of care type:
Number of offspring was not different between pairs of parents that received different types of care as young (OLRs of clutch size on day 8 of incubation, and brood size on day 10, post-hatching, effect of care type in both models:
Body mass of zebra finch offspring raised by parents that had received different type of care. Filled squares indicate average egg mass on day 8 of incubation, whereas empty symbols represent average body masses at different reproductive stages post-hatching (circle: day 10; square: day 16; triangle: day 35). Care categories are given in the order of male care/female care (e.g., B/B, biparentally cared male/biparentally cared female; F/M, female-only cared male/male-only cared female).
Probability to start the second breeding was not different between pairs based on care type received as young (Cox model of latency to start breeding, LRT of care type:
Unlike in the first breeding attempt, relative male parental effort during incubation was not different between pairs of parents based on care type received as young (LMs of relative male nest attendance time, LRT of care type:
Relative male parental effort during offspring provisioning was not different between experimental groups either (LMs of relative male nest attendance time, LRT of care type:
Number and body mass of offspring in the second families of experimental birds were not influenced by care type received as young (OLRs of offspring number in separate models for day 8 of incubation and day 10 post-hatching, LRT of care type: both
Using a split-family experimental design, we investigated in the biparental zebra finch whether early social experiences with each parent would influence offspring behavior toward each parent and, later in life, their own adult parental sex role and negotiation with their pairs. Parental preference tests of uniparentally and biparentally raised control zebra finch young revealed that they pay attention to who takes care of them. Young zebra finches discriminated between their two parents based on their social experiences with each of them, and they might have generalized their expectation to same-sex, non-familiar adults to some extent. When these manipulated birds sexually matured and bred with other manipulated birds for the first time, the typical parental sex roles and coordination of incubation effort was modified in certain experimental groups. In pairs where partners had received care from opposite-sex parents, males spent more time in the nest (both alone and together with the female) compared to pairs in which both partners had received care from the same sex (male or female) or from both parents. At the time of offspring provisioning, however, differences were no longer apparent. Also, when breeding for a second time, parental sex roles and coordination of care seemed normal even already during incubation. Although offspring body mass fluctuated over reproductive stages according to the type of care their parents had received, we found no evidence that our manipulation caused significant changes in terms of number or quality of offspring produced.
Parental preference tests revealed that splitting biparental families, and thereby changing the normal offspring experience of parental sex roles from biparental to uniparental care affects offspring parental preferences. Male-only and female-only cared zebra finch young socialized more with the parent that provisioned them. Change in their parental expectations were clearly demonstrated by their begging behavior during the preference test; beggings were directed mostly toward their caring parent. Since our experimental manipulation allowed visual, olfactory and acoustic interaction among family members, uniparentally raised young could observe their other parent while providing care for their split siblings. Changing parental expectations in our experiment, therefore, suggests that the actual provisioning experiences with individual parents (rather than merely observing their parental effort) are important cues that are taken into account by offspring in future interactions. Paying attention and adjust begging behavior to parental effort can be adaptive because of the high costs and benefits associated with begging (Kilner,
The subsequent preference tests with non-familiar adults provided us with inconclusive results. From the one hand, they suggest that zebra finch young generalize their parental expectations to a certain extent on the basis of parental sex (Jacot et al.,
When uniparentally raised birds bred with each other, long-term effects of early social experiences with parents revealed. Instead of the only effect of the care type received, however, the mechanism seems to be more complex, suggesting a combined effect of early social experiences (when receiving care) and current social experiences (when providing care with the mate). We expected young to modify their own sex roles permanently based on the care type received, so that their parental effort would reflect the combined effect of the sex of their caring parent and that of their own (e.g., we expected male effort to be higher in male-only cared males as opposed to female-only cared males and vice versa). In contrast, we found differences in incubation patterns of first-breeding pairs that are not consistent with this view. When the male and female parent had contrasting social experiences with their parents, relative male effort was higher than in the rest of the experimental groups, including the control. This suggests that similar social experiences of breeding parents are needed for normal coordination of incubation effort to develop. Differences between experimental groups appear to be driven by change in male effort. Indeed, a possible explanation is that our experimental manipulation had a more pronounced effect on one sex (males) than on the other (females). Zebra finch females contribute more to incubation likely because of their brood patch and the more effective heat transfer associated with it (Hill et al.,
Another intriguing mechanistic question raised by our results concerns the exact mechanism by which early social experiences resulted in change in adult behavior. Early experiences of the young may be transmitted to adulthood through changes in morphology (including condition) so that pair members that received the same care type might be consequently in a more similar state, allowing also a more efficient coordination between them. Another plausible explanation is that changed parental behavior as a consequence of our manipulation led to divergent, albeit transient, parental behavior of the offspring.
At the time of nestling provisioning (the second reproductive stage that needs extensive coordination in biparental families), uniparentally raised birds showed no direct effect of the experimental treatment. We have two alternative explanations for no apparent change in parenting; first, this reproductive stage involves interaction with the young, and begging of the nestlings is a very strong stimulus for the parents (Godfray,
The second alternative explanation for the lack of treatment effect during provisioning is that normal parental coordination has been established by the time of offspring provisioning. Social experiences with the mate (when providing care) may be different to that experienced with the parents (when receiving care as young) with regards to sex roles, and experience with the mate may shape establishing normal parental sex roles and coordination. This explanation assumes a similar, two-stage mechanism to those described for social learning of other traits (e.g., song learning or sexual imprinting; Price,
The relatively strong short-term effects compared to the transient long-term effects in our experiment raises the question whether applying the split-family design so that young could observe the other, non-caring parent while provisioning their siblings had different effects when they were young and when they became adults. It is possible that while the effects of such observations have been overridden by own social experiences as young, they manifested and contributed to shaping parental behavior as adults.
Furthermore, we note that a possible reason for the lack of a remarkable effect of our treatment might be the relatively weak sexual conflict in this species, coupled with an expressed synchronization between pair members during parenting. Although a laboratory study (Royle et al.,
In line with the lack of treatment effect on post-hatching parental behavior, we found no persistent consequences on reproductive success either. Although body mass of 16 day old nestlings was different based on care type (and points toward possible unrevealed differences caused by the treatment on parenting), this effect was transient. Number and body mass of offspring were similar over experimental groups by day 35 post-hatching (i.e., by the time offspring became independent). We, however, point out that consequences on reproductive success can take various forms of which we focused only on two aspects, so that differences among experimental groups might have remained unexplored in our study. For instance, finding a suitable mate, pair formation and starting to breed may already involve coordination between parents to various extents. Thus, even a temporarily effect of the early social environment can have lasting consequences in species that forms long-term pair bonds, because of, for instance, missed opportunities to find the best match to mate with. Such an effect of the early rearing environment has been demonstrated with regards to sexual preferences in zebra finches; young that were raised without adult males showed increased preference toward same-sex partners as adults (Adkins-Regan and Krakauer,
To facilitate the detection of social learning, we manipulated parental sex roles to the extremes by changing the role models' behavior from biparental to uniparental care. Our results, however, do not point to social learning of parental sex roles
We acknowledge that our sample size in the analysis of the long-term effects were moderate, especially for the second breeding. This then inevitably results in lower statistical power so that only large effects can be detected. We think the lower sample sizes in this analysis was partly due to the effects of no free mate choice in our experiment (pairings were based on uniparental care received as young), and partly due to the lack of breeding experience in our subjects. We argue, however, that our experiment excludes that parental sex roles would develop by strong, deterministic early social experiences from parents, and strongly suggests that although such experiences are important when care is received as young, these translates only to transient effects as adults.
Taken together, our results suggest that parental sex roles and coordination are perceived by zebra finch young and such early social experiences influence their own parental behavior as adults. These effects, however, are not permanent and can be overridden by own social experiences with the mate when starting to breed. A conclusive answer to the question of whether or not young generalize their parental expectations to parental sex, takes further experimenting. Further studies focusing on the exact mechanism of the described parental coordination patterns and an extended survey of the potential fitness consequences are also needed for a comprehensive understanding of the long-term effects of early social experiences with parents.
All datasets generated for this study are included in the manuscript and/or the
The study was carried out according to the German and Hungarian Laws for the experimentation with animals and with permission of the ELTE MÁB (#02/2014). Breeding and housing of the birds were done under the permission of the Veterinäramt Bielefeld (# 530.421630-1, 18.4.2002). All birds used in the experiments remained for their entire life at the Department of Ethology, Eötvös Loránd University, Budapest. All birds were visually monitored for health status on a daily basis.
ÁP and TS conceived the study with input from OK and ÁM. NvE and EKr contributed to experimental design and managing the experiments. ÁP, BM, EKi, and TB carried out the experiments and collected data. BM, EKi, TB, and TR coded video recordings. ÁP and BM managed the database, and ÁP analyzed the data. ÁP and BM wrote the manuscript with input from EKr, TR, NvE, JK, TS, ÁM, and OK. All authors contributed to the final paper. ÁP with BM revised the paper.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
We thank Joanna Rutkowska for her help with acquiring cardbox nest boxes. We thank Elizabeth Adkins-Regan, Simon Charles Griffith and James Luke Savage for their valuable comments on previous versions of the manuscript.
The Supplementary Material for this article can be found online at:
Long-term social effects dataset, incubation.
Long-term social effects dataset, offspring provisioning.
Long-term social effects dataset, reproductive success.
Short-term social effects dataset, parental preference.
Long-term effects dataset, probability to start breeding.