Defences against brood parasitism in the common blackbird (Turdus merula)Plasticity, physiology and evolution

Resumen

Antagonistic interactions between avian brood parasites and their hosts provide excellent examples of reciprocal evolution of host adaptations and parasite counter-adaptations. The high fitness costs imposed by brood parasitism select for the evolution of host defences, which set the stage for a co-evolutionary arms race, in which brood parasites evolve adaptive counter-defences that select for improved host defences, further parasitic adaptations, and so on. Although these adaptations can be found in all stages of the breeding cycle, the main host defence is the rejection of parasitic eggs. Previous studies have suggested that egg rejection is a complex process in which different stages can be differentiated: egg recognition, decision and the action of reject itself. Throughout this thesis, the study of egg rejection is approached according to this perspective, focusing on the factors that govern each of these stages. Most studies on brood parasitism have focused on the last stage of the egg-rejection process (action itself), which can be carried out by deserting the parasitized nests, ejecting the foreign egg, or even burying it in the nest. However, as potential costs associated with each of these egg-rejection mechanisms vary, the choice of the egg-rejection mechanism by hosts should consequently be modulated by a balance between the costs and benefits of the response. In Chapter 1, we investigated whether nest desertion can be considered an egg-rejection mechanism in medium or large-sized hosts. We found that nest desertion cannot be seen as an unequivocal response to brood parasitism in the common blackbird Turdus merula, a medium-sized potential host species. Thus, our findings suggest that future studies on egg rejection using similar species should cautiously consider nest desertion as a response to brood parasitism. Importantly, each stage of the egg rejection process is likely to be impacted by different factors that determine the host response. In this thesis, different traits of parasitic eggs (egg mass, colour and size) are proven to affect particular stages of the egg-rejection process, including the decision to eject, which may lead to the acceptance of previously recognized eggs. Chapter 2 shows that hosts are not willing to assume the potential costs associated to the ejection of a slightly heavier egg (low motivation), which turned out in acceptance decisions, therefore confirming that egg recognition is not necessarily followed by egg rejection. Chapter 3 goes one step further and studies how the different stages of the egg-rejection process can be independently impacted by different traits of the parasitic egg. In particular, this chapter describes how colour mimicry makes hampers the recognition of parasitic eggs (the first stage of the process), thus leading to egg acceptance. On the other hand, egg size does not seem to affect recognition, but it can impose mechanical restrictions on the action stage (the third stage) and delays the decision to eject (the second stage of the process). Importantly, the existence of acceptance decisions implies that the egg-rejection rate does not necessarily reflect the recognition abilities of hosts, so it is necessary to study other variables clearly attributable to egg recognition to fully understand the rejection process. In this thesis, the “egg-touching behaviour” exhibited by blackbirds is revealed as a reliable indicator of the egg-recognition abilities in this species, allowing a more detailed study of the relationships between recognition and rejection. Given its importance in regulating animal behaviour, endocrine pathways are excellent candidates to continue unravelling the proximate mechanisms underlying the egg-rejection process. However, the detailed knowledge of behavioural responses to parasitic eggs contrasts with the limited information available on the hormonal processes that govern these behaviours. Chapter 4 therefore investigates how hosts adjust their hormonal state to deal with parasitic eggs, as well as the potential effects of these adjustments on the physical state of hosts. Our results show that a parasitic egg is, from a hormonal perspective, a stressful factor for adult hosts since parasitized individuals showed higher baseline corticosterone levels, and lower body condition, than non-parasitized individuals. In addition, unaffected levels of prolactin suggest that blackbirds tend to maintain parental care even when parasitized, which may explain some behaviours found in this species, such as the absence of nest desertion in response to experimental parasitism. The important role of decision-making in the host response revealed by the previous chapters suggests that plastic responses in egg rejection could be common among host species. Consequently, Chapter 5 reviews the evidence of plastic defences against parasitic eggs, showing that phenotypic plasticity in egg rejection is less widespread than might be expected. This chapter discuss the factors that could favour the evolution of phenotypic plasticity and its importance in the co-evolutionary relationship between brood parasites and their hosts, where fixed responses seems to be more frequent than previously suspected, even in the absence of brood parasitism. Precisely, Chapter 6 provides experimental evidence on the evolutionary origin of the egg-rejection abilities exhibited by species not currently impacted by interspecific brood parasitism, as is the case of blackbirds. Although previous studies have suggested that egg rejection evolved in these species because of conspecific brood parasitism, our results indicate that the most probable origin of these abilities is a past exploitation by interspecific parasites. Likewise, current absence of interspecific brood parasitism in these species could be due to their well-developed defences, which are maintained even after speciation events, probably due to the lack of costs for their maintenance. Since it has been assumed that females play the leading role in the egg-rejection process, Chapter 7 tries to confirm such assumption and investigates whether there are sex differences in the host response to parasitic eggs. This question is particularly relevant in species, like blackbirds, in which the incubation depends exclusively on the female. Contrary to conventional theory, we found that blackbird males are able to recognize and eject parasitic eggs. Interestingly, recognition abilities of males are less developed than those of females, probably due to their looser association to the nest during the incubation stage. The evolution of egg recognition in non-incubating males is an intriguing fact that can have important implications in the evolution of anti-parasitic defences within host populations. The results of previous chapters provide a detailed insight into the egg-rejection process. These findings in addition to the recent new theoretical framework in the field of animal decision making highlights the need to update some terms frequently used in egg-rejection studies, as well as the inclusion of new concepts to future studies. This thesis therefore concludes with the proposal, in Chapter 8, of an updated terminology advocating for a consistent use of terms in future works on egg rejection, which could contribute to the advance of scientific knowledge in the field of brood parasitism. Summarizing, this thesis addresses the study of egg rejection as a complex and potentially plastic process in which host decision-making plays a key role. The environmental context, clutch characteristics and cognitive abilities of hosts will determine the outcome of egg rejection by modulating the different stages of this process, which is probably mediated by endocrine pathways. This approach is complemented by an evolutionary perspective on the origin of egg rejection abilities in non-exploited potential hosts, as well as the importance of considering the role of males in egg rejection. This thesis therefore provides significant advances in our understanding of the co-evolutionary interactions between parasites and hosts, particularly in relation to one of the main anti-parasitic defences, egg rejection.