Biologists have long been fascinated by coevolutionary interactions, such as those between pollinators and flowers, predators and prey or parasites and hosts. These interactions have caused great interest because they are important drivers of the evolution of traits in many taxa. For instance, in antagonistic coevolution exploiters select for the evolution of defences in their victims, which in turn select for counter-adaptations in the exploiters, giving rise to an evolutionary arms race. But what happens if the exploiter “wins” the arms race, or if defences are too costly for victims to evolve? Another possible outcome of antagonistic coevolution is the evolution of tolerance in victims; instead of evolving defences to reduce the number of successful enemy attacks, victims evolve ways to minimize the impact of attacks (Svensson and Råberg 2010). For instance, many plants invest in the production of a massive number of seeds instead of investing in the production of thorns or chemicals to deter herbivores. The evolution of tolerance in hosts of avian brood parasites is the focus of the new review by Avilés (2017). Brood parasitism is a classic example of coevolution between hosts and parasites. Brood parasites lay their eggs in the nests of their hosts and abandon their young entirely to the care of the host (Davies 2000). Parasitism often results in the death of the host’s young, and this high cost has selected for a suite of defences in hosts, including mobbing of adult brood parasites (Feeney et al. 2012), and rejection of parasite eggs and chicks (Langmore et al. 2003). However, a long-standing puzzle is why some hosts fail to evolve defences despite experiencing high costs of parasitism. A possible solution to this puzzle is that hosts have evolved tolerance towards parasites and thereby significantly reduced the costs of parasitism (Svensson and Råberg 2010; Medina and Langmore 2016). However, evidence of tolerance in hosts of brood parasites is scarce. Avilés (2017) argues that there are two main reasons for this. First, most of the literature has focused on the arms race between hosts and parasites, which is mainly driven by resistance, not tolerance, strategies. Second, the literature tends to focus on highly virulent parasites, which kill all the progeny of the host. In this case, there is very little space for tolerance to operate, because it is difficult to decrease the costs of such a negative interaction. However, Avilés (2017) proposes some mechanisms related to clutch size adjustment and breeding frequency that might have evolved as tolerance adaptations. These mechanisms have been suggested previously in the literature, but they have not been tested explicitly and recent evidence suggests that the logic behind some of these arguments may be flawed (Medina et al. 2017). A particularly novel contribution of Avilés (2017) review is to propose an experimental framework for detecting the effects of tolerance in future studies. Avilés proposes investigating the repertoire of phenotypic fitness responses of a host genotype along a gradient of intensity of brood parasitism, using a reaction norm approach. Such an approach has been applied to studies of nematode parasites in sheep (Hayward et al. 2014), but has not yet been adopted in studies of avian brood parasitism. He also suggests manipulating perceived risk of parasitism to test for phenotypically plastic tolerance responses. An interesting point raised in Avilés review is that our current observations might already be the result of tolerance to brood parasites in the past, and the current costs of parasitism are already lower than they were at the beginning of the interaction. This idea is of course very difficult to test, but could explain why demonstrating tolerance has proved difficult. To build on Avilés’ point, a potential interesting avenue for future work would be to measure the costs of parasitism in species that have been hosts for a long time, and compare this to the costs of recently parasitized hosts, which presumably have not had as much time to evolve tolerance. If some tolerance mechanisms are behavioral and plastic (e.g., feeding patterns, renesting, hatching synchrony) then they might evolve and spread very rapidly in a population, giving us little opportunity to detect such changes. Overall, Avilés’ review highlights an important and neglected area of brood parasite—host interactions and proposes a promising framework for future investigations. Very little is known about the evolution of tolerance in hosts of brood parasites, but the potential for taking this research in new directions is exciting. REFERENCES Avilés JM. 2017. Can hosts tolerate avian brood parasites? An appraisal of mechanisms. Behav. Ecol . doi:10.1093/beheco/arx150. Google Scholar CrossRef Search ADS Davies NB. 2000. Cuckoos, cowbirds and other cheats . T. & A.D. Poyser. Bloomsbury Publishing PLC. p. 310. Feeney WE, Welbergen JA, Langmore NE. 2012. The frontline of avian brood parasite–host coevolution. Animal Behav . 84: 3– 12. Google Scholar CrossRef Search ADS Hayward AD, Nussey DH, Wilson AJ, Berenos C, Pilkington JG, Watt KA, Pemberton JM, Graham AL. 2014. Natural selection on individual variation in tolerance of gastrointestinal nematode infection. PLoS Biol . 12: e1001917. Google Scholar CrossRef Search ADS PubMed Langmore NE, Hunt S, Kilner RM. 2003. Escalation of a coevolutionary arms race through host rejection of brood parasitic young. Nature . 422: 157– 160. Google Scholar CrossRef Search ADS PubMed Medina I, Langmore NE. 2016. The evolution of acceptance and tolerance in hosts of avian brood parasites. Biol Rev Camb Philos Soc . 91: 569– 577. Google Scholar CrossRef Search ADS PubMed Medina I, Langmore NE, Lanfear R, Kokko H. 2017. The evolution of clutch size in hosts of avian brood parasites. The American Naturalist . 190: E112– E123. Google Scholar CrossRef Search ADS PubMed Svensson EI, Råberg L. 2010. Resistance and tolerance in animal enemy-victim coevolution. Trends Ecol Evol . 25: 267– 274. Google Scholar CrossRef Search ADS PubMed © The Author(s) 2017. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: firstname.lastname@example.org This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)
Behavioral Ecology – Oxford University Press
Published: Dec 30, 2017
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