Camilla A. Hinde

Negotiations within the family over the supply of parental care

Adults provisioning dependent young are in conflict with their partners, who would prefer a greater level of effort, and with their offspring, who would prefer a greater supply of food. To what extent, then should adults negotiate their provisioning behaviour with other family members? We used experimental manipulations of brood size, and targeted playback of begging calls to determine the extent to which adult great tits Parus major adjust their provisioning rates in response to the behaviour of their partner and their brood. We found that males and females behaved similarly, both responding more to each others behaviour than to chick calling. We also found that the degree to which adults negotiated their provisioning rates with each other varied between years. A review of the literature suggests that the extent of negotiation over provisioning is likely to vary not only between species of diverse taxa, but also between and within (this study) populations of the same species. We suggest that provisioning behaviour lies on a ‘negotiation continuum’, which describes the extent to which parents respond to the actions of other family members. We argue that an individuals location on the ‘negotiation continuum’ is determined partly by the extent to which it can physically respond to the behaviour shown by other members of the family and partly by the quality of information on offer.

Parent-Offspring Conflict and Coadaptation

Speak to Me, Mama Maternal effects are effects of the mother (for example, hormones) on her offspring that are independent of genetic inheritance, but related to the mothers phenotype and her environment. Despite their universal occurrence, little is known about the evolutionary influence of maternal effects. Hinde et al. (p. 1373; see the cover) modeled maternal effects in birds and showed that nestling begging, as well as provoking feeding, also provides parents with information about offspring vigor. Conversely, maternal effects provide information to the unborn offspring about parental quality. Experimental studies with canaries provided support for the theoretical predictions, and together these studies show that parent-offspring conflict (that is, the conflict between the offspring for its immediate needs and the need of the parent to conserve resources for any future offspring) is resolved by the reciprocal exchange of information before and after birth. Hormonal signaling ensures a match between parental capacity for resource provisioning and offspring behavior and development after hatching that meet the mothers capacity to provide resources. Prenatal hormonal signaling can match a mother bird’s capacity to provide food with her offsprings’ expectations. The evolution of family life has traditionally been studied in parallel by behavioral ecologists and quantitative geneticists. The former focus on parent-offspring conflict and whether parents or offspring control provisioning, whereas the latter concentrate on the coadaptation of parental supply and offspring demand. Here we show how prenatal effects on offspring begging can link the two different approaches. Using theoretical and experimental analyses, we show that when offspring control provisioning, prenatal effects primarily serve the parent’s interests: Selection on parents drives coadaptation of parent and offspring traits. In contrast, when parents control provisioning, prenatal effects primarily serve the offspring’s interests: Selection on the offspring drives coadaptation of parent and offspring traits. Parent-offspring conflict may thus be responsible for the selective forces that generate parent-offspring coadaptation.

Prenatal environmental effects match offspring begging to parental provisioning

The solicitation behaviours performed by dependent young are under selection from the environment created by their parents, as well as wider ecological conditions. Here we show how mechanisms acting before hatching enable canary offspring to adapt their begging behaviour to a variable post-hatching world. Cross-fostering experiments revealed that canary nestling begging intensity is positively correlated with the provisioning level of their own parents (to foster chicks). When we experimentally increased food quality before and during egg laying, mothers showed higher faecal androgen levels and so did their nestlings, even when they were cross-fostered before hatching to be reared by foster mothers that had been exposed to a standard regime of food quality. Higher parental androgen levels were correlated with greater levels of post-hatching parental provisioning and (we have previously shown) increased faecal androgens in chicks were associated with greater begging intensity. We conclude that androgens mediate environmentally induced plasticity in the expression of both parental and offspring traits, which remain correlated as a result of prenatal effects, probably acting within the egg. Offspring can thus adapt their begging intensity to variable family and ecological environments.

Chapter 6 Information Warfare and Parent–Offspring Conflict

Publisher Summary Information warfare occurs when factions use and manage information to gain an advantage over their rivals. It is common in diverse contexts ranging from identity fraud to industrial espionage, from biotech war to military campaigns. The information warfare plays an important role in influencing the outcome of the parent–offspring conflict, the evolutionary conflict of interest between parents and their young over the provision of parental investment. In principle, the asymmetry in knowledge can counterbalance any asymmetry in physical prowess between rivals, and the more knowledgeable party might gain the upperhand. For this reason, information warfare is aptly applied to the context of parent–offspring conflict, because young animals in conflict with their parents are often placed at a disadvantage by their relatively small size and weaker physical power. Two outcomes to parent–offspring conflict are possible. The first is an evolutionarily stable resolution and the alternative outcome to parent–offspring conflict is an unstable arms race through evolutionary time.

Parental food provisioning is related to nestling stress response in wild great tit nestlings: implications for the development of personality

BackgroundVariation in early nutrition is known to play an important role in shaping the behavioural development of individuals. Parental prey selection may have long-lasting behavioural influences. In birds foraging on arthropods, for instance, the specific prey types, e.g. spiders and caterpillars, matter as they have different levels of taurine which may have an effect on personality development. Here we investigated how naturally occurring variation in the amounts of spiders and caterpillars, provisioned to nestlings at day 4 and 8 after hatching, is related to the response to handling stress in a wild passerine, the great tit (Parus major). Broods were cross-fostered in a split-brood design allowing us to separate maternal and genetic effects from early rearing effects. Adult provisioning behaviour was monitored on day four and day eight after hatching using video recordings. Individual nestlings were subjected to a handling stress test at an age of 14 days, which is a validated proxy for exploratory behaviour as an adult.ResultsVariation in handling stress was mainly determined by the rearing environment. We show that, contrary to our predictions, not the amount of spider biomass, but the amount of caterpillar biomass delivered per nestling significantly affected individual performance in the stress test. Chicks provisioned with lower amounts of caterpillars exhibited a stronger stress response, reflecting faster exploratory behaviour later on in life, than individuals who received larger amounts of caterpillars.ConclusionsThese results suggest that natural variation in parental behaviour in wild birds modulates the developmental trajectories of their offsprings personality via food provisioning. Since parental provisioning behaviour might also reflect the local environmental conditions, provisioning behaviour may influence how nestlings respond to these local environmental conditions.

Evolutionary signals of selection on cognition from the great tit genome and methylome

For over 50 years, the great tit (Parus major) has been a model species for research in evolutionary, ecological and behavioural research; in particular, learning and cognition have been intensively studied. Here, to provide further insight into the molecular mechanisms behind these important traits, we de novo assemble a great tit reference genome and whole-genome re-sequence another 29 individuals from across Europe. We show an overrepresentation of genes related to neuronal functions, learning and cognition in regions under positive selection, as well as increased CpG methylation in these regions. In addition, great tit neuronal non-CpG methylation patterns are very similar to those observed in mammals, suggesting a universal role in neuronal epigenetic regulation which can affect learning-, memory- and experience-induced plasticity. The high-quality great tit genome assembly will play an instrumental role in furthering the integration of ecological, evolutionary, behavioural and genomic approaches in this model species.

Consistent individual differences in the social phenotypes of wild great tits, Parus major

Despite growing interest in animal social networks, surprisingly little is known about whether individuals are consistent in their social network characteristics. Networks are rarely repeatedly sampled; yet an assumption of individual consistency in social behaviour is often made when drawing conclusions about the consequences of social processes and structure. A characterization of such social phenotypes is therefore vital to understanding the significance of social network structure for individual fitness outcomes, and for understanding the evolution and ecology of individual variation in social behaviour more broadly. Here, we measured foraging associations over three winters in a large PIT-tagged population of great tits, and used a range of social network metrics to quantify individual variation in social behaviour. We then examined repeatability in social behaviour over both short (week to week) and long (year to year) timescales, and investigated variation in repeatability across age and sex classes. Social behaviours were significantly repeatable across all timescales, with the highest repeatability observed in group size choice and unweighted degree, a measure of gregariousness. By conducting randomizations to control for the spatial and temporal distribution of individuals, we further show that differences in social phenotypes were not solely explained by within-population variation in local densities, but also reflected fine-scale variation in social decision making. Our results provide rare evidence of stable social phenotypes in a wild population of animals. Such stable social phenotypes can be targets of selection and may have important fitness consequences, both for individuals and for their social-foraging associates.

Inferring social structure from temporal data

Social network analysis has become a popular tool for characterising the social structure of populations. Animal social networks can be built either by observing individuals and defining links based on the occurrence of specific types of social interactions, or by linking individuals based on observations of physical proximity or group membership, given a certain behavioural activity. The latter approaches of discovering network structure require splitting the temporal observation stream into discrete events given an appropriate time resolution parameter. This process poses several non-trivial problems which have not received adequate attention so far. Here, using data from a study of passive integrated transponder (PIT)-tagged great tits Parus major, we discuss these problems, demonstrate how the choice of the extraction method and the temporal resolution parameter influence the appearance and properties of the retrieved network and suggest a modus operandi that minimises observer bias due to arbitrary parameter choice. Our results have important implications for all studies of social networks where associations are based on spatio-temporal proximity, and more generally for all studies where we seek to uncover the relationships amongst a population of individuals that are observed through a temporal data stream of appearance records.

The role of social and ecological processes in structuring animal populations: a case study from automated tracking of wild birds

Both social and ecological factors influence population process and structure, with resultant consequences for phenotypic selection on individuals. Understanding the scale and relative contribution of these two factors is thus a central aim in evolutionary ecology. In this study, we develop a framework using null models to identify the social and spatial patterns that contribute to phenotypic structure in a wild population of songbirds. We used automated technologies to track 1053 individuals that formed 73 737 groups from which we inferred a social network. Our framework identified that both social and spatial drivers contributed to assortment in the network. In particular, groups had a more even sex ratio than expected and exhibited a consistent age structure that suggested local association preferences, such as preferential attachment or avoidance. By contrast, recent immigrants were spatially partitioned from locally born individuals, suggesting differential dispersal strategies by phenotype. Our results highlight how different scales of social decision-making, ranging from post-natal dispersal settlement to fission–fusion dynamics, can interact to drive phenotypic structure in animal populations.

Unpredictable environments lead to the evolution of parental neglect in birds.

A nest of begging chicks invites an intuitive explanation: needy chicks want to be fed and parents want to feed them. Surprisingly, however, in a quarter of species studied, parents ignore begging chicks. Furthermore, parents in some species even neglect smaller chicks that beg more, and preferentially feed the biggest chicks that beg less. This extreme variation across species, which contradicts predictions from theory, represents a major outstanding problem for the study of animal signalling. We analyse parent–offspring communication across 143 bird species, and show that this variation correlates with ecological differences. In predictable and good environments, chicks in worse condition beg more, and parents preferentially feed those chicks. In unpredictable and poor environments, parents pay less attention to begging, and instead rely on size cues or structural signals of quality. Overall, these results show how ecological variation can lead to different signalling systems being evolutionarily stable in different species.