To beg or not to beg - Evolutionary ecological perspectives on bird family life
30 June 2017
Campus Drie Eiken, R2 - Universiteitsplein 1 - 2610 Antwerpen-Wilrijk (route: UAntwerpen, Campus Drie Eiken
PhD defence Nolwenn Fresneau - Faculty of Science, Department of Biology
Some species invest a lot of energy in raising their young, in order to improve offspring condition and survival. This parental care requires optimal communication to guarantee the optimal transfer of resources. Elaborate offspring solicitation behaviour, also called begging, can be observed in several species of birds and insects. This signal can be acoustic, visual or postural and aims to trigger parental provisioning. Even though parental provisioning is essential for offspring development and survival, it comes at a cost to the parents. Due to a relatedness asymmetry, parents and offspring rate these costs differently, creating a number of conflicts of interest about the amount of resources to be invested.
Indeed, each offspring is more related to itself than to its parents, and is thus selected to demand more resources than their parents are selected to give. Begging may then serve as a mean to manipulate the parents and should thus come with a cost in order to ensure its honesty (according to the handicap principal). Quantifying costs of begging empirically has proven to be difficult. The evolutionary trajectory of begging and parental provisioning is not only influenced by a parent-offspring conflict; it is also an example of social selection, since begging and parental provisioning reciprocally influence each other. They are both targets and agents of selection, and thus have been hypothesized to coevolve and potentially become ultimately genetically correlated. Indeed if both behaviours covary and a certain form of parental provisioning and offspring performance leads to a higher fitness benefit, individuals carrying both traits should be selected.
Besides, in broods with more than one offspring, each offspring is in competition with its siblings. Each nestling is more related to itself than to its siblings, and evolution favours selfish behaviours that lead to a greater individual share of resources. However, an optimal begging strategy will also depend on the competitive abilities of the siblings as well as their need, and thus the likelihood of obtaining food. Taking their social environment (i.e. their siblings) into account is thus crucial for the offspring in order to optimise its begging behaviour. This may lead to cooperation or negotiation between siblings which both lower the cost of sibling conflict. Yet examples of such strategies are rather limited and it is not clear what kind of selective pressure would favour one strategy over another.
Since the parents are the resource holders, their response and feeding decisions will be the ultimate selection force. Parental feeding decisions are also complicated by a conflict of interest, i.e. a sexual conflict over the amount of parental investment. When two parents contribute to parental care, they are typically unrelated. Thus the benefits (offspring growth and survival) of care depend on the investments of both parents, while each individual only paying the cost of their own contribution. So it may be in each parent’s interest to have its mate investing more into care than itself. One consequence of this conflict is that both parents are more reluctant to provide care in order to avoid exploitation by its mate. Negotiation that facilitates coordinated parental behaviour may be the key to ease the cost of this conflict. Since success of begging is ultimately dependant of the willingness of the parent to provide care, the outcome of this conflict has consequences for the offspring.
Taken together, this thesis aims to improve our understanding of the evolutionary trajectory of begging, taking the complex social environment that is shaped by parents and siblings into account.
First, I applied a bidirectional artificial selection on begging using Fife fancy canaries (Serinus canaria) as a model species. After three generations of selection, offspring of the high begging and low begging line significantly differed in their begging behaviour. Interestingly, nestlings of the low begging line grew significantly faster than before the selection, and couples of the low begging line increased the number of fledglings they produced. Thus, there is a clear advantage to begging less. This result suggests that before selection, begging is an exaggerated offspring signal and parents seem to counterbalance the cost of a high demanding brood by using brood reduction. The total costs of care for the parents thus remain rather constant, given the interplay between the number of offspring and the offspring’s demands.
Yet, I did not find any evidence for genetic correlation between offspring begging and parental provisioning as parental provisioning was not different between the two lines, indicating that it was not coselected.
However, it has been shown previously that parental provisioning and offspring begging covary. Since I found no genetic correlation between these two behaviours, I focussed on behavioural plasticity as a potential mechanism underlying the covariation between offspring begging and parental provisioning, which had been observed repeatedly.
To this end, I measured parent-offspring interactions at two levels of nestling hunger, which allowed me to take a behavioural reaction norm and (co)variance partitioning approach. The latter enabled me to disentangle covariances at a between-nest level that are indicative for genetic or permanent maternal effects (i.e. fixed strategy), as well as the covariances at the within-nest level which describe the parts of the phenotypic covariation that are related to responsiveness/plasticity (i.e. conditional strategy). My experiment showed that the phenotypic covariance was mainly driven by behavioural responsiveness. This indicates that parental- and offspring behaviours covary at the phenotypic level, because of a plastic behavioural coadjustment in response to one another.
Since I showed that parents and offspring adjust their behaviour to each other, I then focussed on sibling competition in order to determine the influence of sibling hunger and condition on begging strategies. I performed two experiments: the first one was a satiation experiment with captive canaries, and the second a food deprivation experiment using the wild blue tits (Cyanistes caeruleus). In canary nestlings, I found that only female nestlings responded honestly, begging significantly less when satiated. Male nestlings, on the contrary, did not alter their begging according to their own level of satiation. Nestlings only weakly responded to the need of their siblings, even though that could lower the cost of sibling competition, and again only female nestlings did so by reducing their begging when their sibling was satiated. Thus, in canaries female nestlings appeared to be more sensitive to both intrinsic need as well as changes in their social environment.
Blue tit nestlings increased their begging duration in response to the elevated, experimentally-induced hunger levels. Again, I found a differential begging strategy, this time according to the position within the brood size hierarchy. While the lightest nestlings did not modulate their begging level as a function of sibling hunger, I found - opposite to what I expected - that heavier nestlings significantly increased their begging when lighter nestlings were food deprived. However, in both cases (lighter and heavier nestlings’ strategies) instead of adjusting their begging according to their nestling need (in order to reduce the sibling conflict), nestlings either did not adjust their begging or increased the competition. So in both experiments, I did not find evidence of a cooperative begging strategy to reduce the costs of sibling competition. Intriguingly, despite some potentially manipulative signals, parents fed accurately, with hungrier nestlings receiving more food in both cases.
Finally, I studied a recently suggested behavioural mechanism about how parents coordinate their investment in an attempt to resolve their sexual conflict. Such coordinated behaviour may well be hampered, given that parental care is often (1) multidimensional, (2) sex-specific, and (3) temporally variable. Canaries showed a clear division of tasks between males and females in (among others) provisioning, brooding, and foraging. These task specialisations faded with increasing nestling age. When parental tasks became more similar, the degree of alternated feeding visits, which represent a form of conditional cooperation, also increased. Such cooperation is thought to benefit offspring development, but this was not supported by our data. Thus, the interpretation of alternation as a mechanism of conditional cooperation critically depends on the division and specialisation of parental tasks, and the ultimate benefits have yet to be shown.
Thus, my PhD project improves our understanding of the evolutionary and ecological aspects of begging. First of all, it showed that behavioural plasticity and responsiveness are potentially the central components of parent-offspring coevolution. Furthermore, begging appeared to be a complex multidimensional trait that could be manipulative in certain contexts. This view is supported by the artificial selection experiment, suggesting that begging in its current form represents an exaggerated offspring signal. Besides, nestlings did not adjust their begging in an altruistic way, as they did not retreat from competition when their siblings were needier and even increased the sibling competition by increasing their begging. This increased signalling within competition might also be a cause for exaggeration of the offspring’s signal. Finally, different offspring begging strategies can be found not just within the same species but, interestingly, even within the same nest. This means that one strategy may be optimal in a certain context or for a certain condition but not in another. Evolution of begging behaviour is thus complicated by the coexistence of several optimal strategies.