Final Report Summary - FAMILY AFFAIRS (Parental care: shaped by parent–offspring conflict and co-adaptation)
Family life: harmonious or rife with conflict?
Although family life may often seem harmonious, interactions within families are also influenced by fundamental conflicts of interests between the different family members – such as between parents and their offspring – that can only be understood from an evolutionary perspective. The evolution of family life is governed by complex interactions between parents and their offspring that revolve around the allocation of parental care. Parents can increase the fitness (survival and future reproduction) of their offspring by providing care, such as food. Extensive parental care occurs in a wide range of taxa, including mammals, birds, fish and insects. Offspring often show elaborate solicitation behaviours that elicit care by their parents, for example crying by human infants and begging by nestlings of birds.
Parent offspring-co-adaptation within families
Recent theory predicts offspring demand for and parental supply of care to be co-adapted within families. Two main predictions of this theory are that (1) the behavioural responses of parents provisioning food and offspring begging for food are correlated, and that (2) cross-fostering of offspring creates mismatches between parental and offspring behaviours, leading to fitness costs (=reduced survival and/or reproduction) to parents and/or offspring. A high-profile lab study on domesticated canaries has provided support for these two predictions (Hinde et al. 2010, Science, 327: 1373-1376). These findings have potentially important implications for quantitative genetic studies that commonly use (experimental) cross-fostering as a method to be able to assess the relative influence of genetics and the environment on, for example, the development and behaviour of individuals. If cross-fostering per se generally impacts on offspring fitness, this would make it an invalid research method for distinguishing genetic and environmental influences.
Studying parent-offspring interactions in a wild bird
It is still unclear, however, how general the phenomenon of parent-offspring co-adaptation within families is, because rigorous tests under natural circumstances in outbred and free-living animals are lacking. Therefore, we carried out a large-scale experiment in a free-living population of a common songbird, the blue tit (Cyanistes caeruleus), testing for parent-offspring co-adaptation (investigating a total of n = 184 broods during two consecutive breeding seasons). Blue tits are an ideal model to investigate the phenomenon of within-family parent-offspring co-adaptation in a free-living animal. Blue tits have extensive bi-parental care, with both parents provisioning food (mostly caterpillars) to the offspring. Furthermore, they readily accept nestboxes for breeding, which makes it relatively easy to study parental provisioning and offspring begging behaviour in a natural setting (Figures 1 and 2).
In this study, we estimated the behavioural responses of parents by measuring provisioning rates as a function of short-term brood size manipulations, which created experimental variation in offspring demand. We estimated behavioural responses of offspring by measuring begging intensity as a function of experimental variation in food deprivation. It is essential to specifically measure these behavioural responses, rather than mean levels of provisioning and begging, because the parent-offspring behavioural interactions are highly dynamic. Parents and offspring continuously respond to each other’s behaviour: when the offspring get hungry, they will increase their begging, to which the parents will respond by increasing their provisioning rate; this in turn will lead to a lower hunger level in the offspring, which will decrease their level of begging, and so on. Furthermore, as an ultimate test of the parent-offspring mismatch hypothesis, we cross-fostered 2/3 of the broods we studied (n = 128), while 1/3 of broods (n = 56) were kept as controls. Such a non-cross-fostered control group is crucial for testing the effect of cross-fostering per se, but surprisingly such a control group is only rarely included in cross-fostering studies. A key prediction following from the parent-offspring co-adaptation hypothesis is that blue tit parents and/or offspring of cross-fostered broods will suffer fitness costs (for example reduced growth or survival), compared to parents and offspring of control (non-cross fostered) broods.
No fitness effects of cross-fostering: female compensation for reduction of male care?
Remarkably, we found no evidence for the predicted negative fitness effects due to the cross-fostering in either parents or offspring. Survival of parents and offspring was not lower for cross-fostered broods compared to control (non-cross-fostered) broods, and also the growth of the nestlings of cross-fostered and control broods was similar. The apparent absence of fitness effects appears good news for quantitative genetics studies using cross-fostering as a standard approach, because it confirms it to be a valid method for assessing the relative importance of genetic and environmental influences. Further analyses, however, revealed that in one of the two study years experimental males reduced their provisioning effort when caring for a cross-fostered brood, compared to control males caring for their own brood. The female partners of the experimental males increased their provisioning rates, thereby compensating for the reduction of male care. The female compensation for loss of male care could explain the absence of fitness effects in the offspring due to the cross-fostering. This result indicates that parent-offspring co-adaptation may in fact occur, influencing the behaviour (but apparently not fitness) of parents. This finding warrants further study of the occurrence of within-family parent-offspring co-adaptation, including the potential implications of this for cross-fostering studies. Important questions still remain: Why did we find a reduction in male care for cross-fostered broods in only one of the two study years? Does the quality of the environment play a role here, with the years perhaps differing in food availability? And what is the mechanism that caused the change in male provisioning behaviour? This is, how did the males detect that the offspring in their nest were not their own? (this is still a puzzle, because clutches were already cross-fostered before hatching of the eggs).
Follow-up research
We will follow up on these questions in our future research. We will for example test if odour cues could play a role in the recognition of related versus unrelated individuals (a phenomenon also referred to as kin recognition). This is well-known to occur in mammals, but has hardly been studied in birds. There is growing evidence, however, that also birds have a well-developed sense of smell, which may also be important in kin recognition, as well as in mate choice and inbreeding avoidance. Furthermore, a PhD student, Reinaldo Marfull (2012-2016), is currently investigating the behavioural interactions between the blue tit parents and their offspring, as well as the competitive interactions between the offspring, in much more detail. In further analyses we will also investigate how the behavioural responses of parents and offspring are correlated.
Project dissemination
The outcomes of the project were presented at international scientific conferences (Conference of the International Society for Behavioral Ecology, New York, USA, 2014; Congress of Zoology, Liege, Belgium, 2014) and will be published in peer-reviewed scientific papers. The ongoing research on the blue tit study population was also presented to a broader audience through several outreach activities, including a brief feature on television, a popular science lecture, and the permanent placement of a high-quality information panel in the study area explaining the research to the public.
Project’s contribution to the fellow’s scientific career
The Marie Curie Career Integration Grant (CIG) of the EU supporting this project has allowed the research fellow, Peter Korsten, to further strengthen his independent research lines on the behaviour, ecology and genetics of free-living animals. For most of his research, the fellow uses detailed field data from individual-based long-term population studies on free-living birds and mammals. The large datasets provided by such long-running field studies provide a unique resource for ecological studies and have for example been instrumental in the study of the impacts of environmental change (climate change, habitat fragmentation) on natural populations. The project has provided the fellow with valuable experience in the mentoring of MSc and PhD students. It also strongly contributed to extending and strengthening the fellow’s network of international research collaborators (for example leading to a joint publication on parent-offspring co-adaptation with his collaborators, Prof. W. Müller and C. Lucass, at the University of Antwerp, Belgium). Finally, the project has been of vital importance to the fellow in obtaining a research and teaching position (lecturer; since January 2015) at Bielefeld University, Germany, where he will have the opportunity to further develop his research lines and build his own research group.
Although family life may often seem harmonious, interactions within families are also influenced by fundamental conflicts of interests between the different family members – such as between parents and their offspring – that can only be understood from an evolutionary perspective. The evolution of family life is governed by complex interactions between parents and their offspring that revolve around the allocation of parental care. Parents can increase the fitness (survival and future reproduction) of their offspring by providing care, such as food. Extensive parental care occurs in a wide range of taxa, including mammals, birds, fish and insects. Offspring often show elaborate solicitation behaviours that elicit care by their parents, for example crying by human infants and begging by nestlings of birds.
Parent offspring-co-adaptation within families
Recent theory predicts offspring demand for and parental supply of care to be co-adapted within families. Two main predictions of this theory are that (1) the behavioural responses of parents provisioning food and offspring begging for food are correlated, and that (2) cross-fostering of offspring creates mismatches between parental and offspring behaviours, leading to fitness costs (=reduced survival and/or reproduction) to parents and/or offspring. A high-profile lab study on domesticated canaries has provided support for these two predictions (Hinde et al. 2010, Science, 327: 1373-1376). These findings have potentially important implications for quantitative genetic studies that commonly use (experimental) cross-fostering as a method to be able to assess the relative influence of genetics and the environment on, for example, the development and behaviour of individuals. If cross-fostering per se generally impacts on offspring fitness, this would make it an invalid research method for distinguishing genetic and environmental influences.
Studying parent-offspring interactions in a wild bird
It is still unclear, however, how general the phenomenon of parent-offspring co-adaptation within families is, because rigorous tests under natural circumstances in outbred and free-living animals are lacking. Therefore, we carried out a large-scale experiment in a free-living population of a common songbird, the blue tit (Cyanistes caeruleus), testing for parent-offspring co-adaptation (investigating a total of n = 184 broods during two consecutive breeding seasons). Blue tits are an ideal model to investigate the phenomenon of within-family parent-offspring co-adaptation in a free-living animal. Blue tits have extensive bi-parental care, with both parents provisioning food (mostly caterpillars) to the offspring. Furthermore, they readily accept nestboxes for breeding, which makes it relatively easy to study parental provisioning and offspring begging behaviour in a natural setting (Figures 1 and 2).
In this study, we estimated the behavioural responses of parents by measuring provisioning rates as a function of short-term brood size manipulations, which created experimental variation in offspring demand. We estimated behavioural responses of offspring by measuring begging intensity as a function of experimental variation in food deprivation. It is essential to specifically measure these behavioural responses, rather than mean levels of provisioning and begging, because the parent-offspring behavioural interactions are highly dynamic. Parents and offspring continuously respond to each other’s behaviour: when the offspring get hungry, they will increase their begging, to which the parents will respond by increasing their provisioning rate; this in turn will lead to a lower hunger level in the offspring, which will decrease their level of begging, and so on. Furthermore, as an ultimate test of the parent-offspring mismatch hypothesis, we cross-fostered 2/3 of the broods we studied (n = 128), while 1/3 of broods (n = 56) were kept as controls. Such a non-cross-fostered control group is crucial for testing the effect of cross-fostering per se, but surprisingly such a control group is only rarely included in cross-fostering studies. A key prediction following from the parent-offspring co-adaptation hypothesis is that blue tit parents and/or offspring of cross-fostered broods will suffer fitness costs (for example reduced growth or survival), compared to parents and offspring of control (non-cross fostered) broods.
No fitness effects of cross-fostering: female compensation for reduction of male care?
Remarkably, we found no evidence for the predicted negative fitness effects due to the cross-fostering in either parents or offspring. Survival of parents and offspring was not lower for cross-fostered broods compared to control (non-cross-fostered) broods, and also the growth of the nestlings of cross-fostered and control broods was similar. The apparent absence of fitness effects appears good news for quantitative genetics studies using cross-fostering as a standard approach, because it confirms it to be a valid method for assessing the relative importance of genetic and environmental influences. Further analyses, however, revealed that in one of the two study years experimental males reduced their provisioning effort when caring for a cross-fostered brood, compared to control males caring for their own brood. The female partners of the experimental males increased their provisioning rates, thereby compensating for the reduction of male care. The female compensation for loss of male care could explain the absence of fitness effects in the offspring due to the cross-fostering. This result indicates that parent-offspring co-adaptation may in fact occur, influencing the behaviour (but apparently not fitness) of parents. This finding warrants further study of the occurrence of within-family parent-offspring co-adaptation, including the potential implications of this for cross-fostering studies. Important questions still remain: Why did we find a reduction in male care for cross-fostered broods in only one of the two study years? Does the quality of the environment play a role here, with the years perhaps differing in food availability? And what is the mechanism that caused the change in male provisioning behaviour? This is, how did the males detect that the offspring in their nest were not their own? (this is still a puzzle, because clutches were already cross-fostered before hatching of the eggs).
Follow-up research
We will follow up on these questions in our future research. We will for example test if odour cues could play a role in the recognition of related versus unrelated individuals (a phenomenon also referred to as kin recognition). This is well-known to occur in mammals, but has hardly been studied in birds. There is growing evidence, however, that also birds have a well-developed sense of smell, which may also be important in kin recognition, as well as in mate choice and inbreeding avoidance. Furthermore, a PhD student, Reinaldo Marfull (2012-2016), is currently investigating the behavioural interactions between the blue tit parents and their offspring, as well as the competitive interactions between the offspring, in much more detail. In further analyses we will also investigate how the behavioural responses of parents and offspring are correlated.
Project dissemination
The outcomes of the project were presented at international scientific conferences (Conference of the International Society for Behavioral Ecology, New York, USA, 2014; Congress of Zoology, Liege, Belgium, 2014) and will be published in peer-reviewed scientific papers. The ongoing research on the blue tit study population was also presented to a broader audience through several outreach activities, including a brief feature on television, a popular science lecture, and the permanent placement of a high-quality information panel in the study area explaining the research to the public.
Project’s contribution to the fellow’s scientific career
The Marie Curie Career Integration Grant (CIG) of the EU supporting this project has allowed the research fellow, Peter Korsten, to further strengthen his independent research lines on the behaviour, ecology and genetics of free-living animals. For most of his research, the fellow uses detailed field data from individual-based long-term population studies on free-living birds and mammals. The large datasets provided by such long-running field studies provide a unique resource for ecological studies and have for example been instrumental in the study of the impacts of environmental change (climate change, habitat fragmentation) on natural populations. The project has provided the fellow with valuable experience in the mentoring of MSc and PhD students. It also strongly contributed to extending and strengthening the fellow’s network of international research collaborators (for example leading to a joint publication on parent-offspring co-adaptation with his collaborators, Prof. W. Müller and C. Lucass, at the University of Antwerp, Belgium). Finally, the project has been of vital importance to the fellow in obtaining a research and teaching position (lecturer; since January 2015) at Bielefeld University, Germany, where he will have the opportunity to further develop his research lines and build his own research group.
