Integrating mechanisms in the study of tolerance to brood parasites: a response to comments on Avilés

Integrating mechanisms in the study of tolerance to brood parasites: a response to comments on... The study of tolerance defenses against brood parasites has grown rapidly from a functional and evolutionary perspective, but with a poor understanding of mechanisms and weak empirical support. In my review (Avilés 2017), I highlight unstudied mechanisms for tolerance and provide an integrative framework for the empirical study of tolerance that hopefully will facilitate future work on host-parasite interactions. I am deeply grateful for the comments I received on my review and take here the opportunity to clarify some of the main points raised. While Medina and Langmore (2017) agree with the general premise of my review, that hypothesized mechanisms of tolerance have not yet been explicitly tested, they question whether mechanisms based on clutch size adjustments and breeding frequencies might be based on a flawed logic. They argue that reducing clutch size and multiple brooding may not be a good choice for a parasitized host if the new breeding attempt might still be parasitized. I agree with that argument provided the key assumption of stability of risk of parasitism was empirically verified. However, a clutch size reduction in response to parasitism could be a likely evolutionary outcome if it assumed a direct costs of parasitism to hosts, such as a model on conspecific brood parasitism (CBP) illustrates (Lyon et al. 2018). Soler (2018a) alludes to the “general vigor” problem as one that could affect the interpretation of experiments where parasitism intensity is manipulated to detect plastic responses in host traits. I agree that differences in individual quality may explain part of the variance in responses. This possibility can be qualified by considering correlates of individual quality and testing the interaction between quality and parasitism on host traits. But the best choice would be to perform these experiments on the same individuals (or genetically related individuals) to analyze reaction norms in response to manipulated brood parasitism. Soler (2018b) stresses that “it would be worthwhile to emphasize the important role that comparative studies exploring geographical covariation between tolerance by hosts and brood parasite prevalence”. I agree, although I would urge controlling for population differences in host qualities to discard a “general vigor” effect. Lyon et al. (2018) suggest that some of the premises of the tolerance mechanism that I developed based on inter-specific brood parasitism (IBP) can naturally be expanded to CBP. They argue that CBP is a particularly suitable system to study the degree to which tolerance strategies may reduce parasitism costs in the long term, linking mechanisms and life history evolution. I totally agree with these points and consider CBP a suitable system to broaden the study of tolerance. Given the relative lower costs of CBP parasitism compared to IBP, tolerance is likely more prevalent among species affected by CBP than among those affected by IBP. Welbergen (2018) and Abolins-Abols and Hauber (2017) argue that the dichotomy between resistance and tolerance in terms of their cost to parasites may be artificial, as some traits providing tolerance are also likely to negatively impact on parasites. This practical difficulty, however, is not exclusive to a brood parasitism context and has been noted previously in the field of immunopathology (e.g., Raberg et al. 2009), and can be handled by testing whether parasite fitness is decreased in response to changes in host traits (Aviles 2017). Moreover, knowing whether brood parasites are impacted or not by host defensive mechanisms in cases where the parasite offspring survive will provide a more realistic assessment of the costs of parasitism and defense for host and brood parasite and, in the end, result in a better understanding of the eco-evolutionary dynamics between hosts and brood parasites. REFERENCES Abolins-Abols M , Hauber ME . 2018 . Applying the framework and concepts of parasitology to avian brood parasitism: a comment on Avilés . Behav Ecol . Avilés JM . 2017 . Can hosts tolerate avian brood parasites? an apprasial of mechanisms . Behav Ecol . doi:10.1093/beheco/arx150. Lyon BE , Eadie JM , Shizuka D . 2018 . Conspecific brood parasitism can also help us to understand the evoluton of tolerance: a comment on Avilés . Behav Ecol . Medina I , Langmore NE . 2018 . Tolerance in hosts of brood parasites: a comment on Avilés . Behav Ecol . Raberg L , Graham AL , Read AF . 2009 . Decomposing health: tolerance and resistance to parasites in animals . Philos Trans R Soc Lond B Biol Sci . 364 : 37 – 49 Google Scholar CrossRef Search ADS PubMed Soler JJ . 2018a . Tolerance to brood parasitism: a comment on Avilés . Behav Ecol . Soler M . 2018b . The reliability of current evidence on tolerance by hosts of brood parasites and suggestions for studying it: a comment on Avilés . Behav Ecol . Welbergen JA . 2018 . When resistance is futile - tolerance in avian brood parasite hosts: a comment on Avilés . Behav Ecol . © The Author(s) 2018. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com 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) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Behavioral Ecology Oxford University Press

Integrating mechanisms in the study of tolerance to brood parasites: a response to comments on Avilés

Behavioral Ecology , Volume Advance Article (3) – Mar 13, 2018

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Publisher
Oxford University Press
Copyright
© The Author(s) 2018. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com
ISSN
1045-2249
eISSN
1465-7279
D.O.I.
10.1093/beheco/ary027
Publisher site
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Abstract

The study of tolerance defenses against brood parasites has grown rapidly from a functional and evolutionary perspective, but with a poor understanding of mechanisms and weak empirical support. In my review (Avilés 2017), I highlight unstudied mechanisms for tolerance and provide an integrative framework for the empirical study of tolerance that hopefully will facilitate future work on host-parasite interactions. I am deeply grateful for the comments I received on my review and take here the opportunity to clarify some of the main points raised. While Medina and Langmore (2017) agree with the general premise of my review, that hypothesized mechanisms of tolerance have not yet been explicitly tested, they question whether mechanisms based on clutch size adjustments and breeding frequencies might be based on a flawed logic. They argue that reducing clutch size and multiple brooding may not be a good choice for a parasitized host if the new breeding attempt might still be parasitized. I agree with that argument provided the key assumption of stability of risk of parasitism was empirically verified. However, a clutch size reduction in response to parasitism could be a likely evolutionary outcome if it assumed a direct costs of parasitism to hosts, such as a model on conspecific brood parasitism (CBP) illustrates (Lyon et al. 2018). Soler (2018a) alludes to the “general vigor” problem as one that could affect the interpretation of experiments where parasitism intensity is manipulated to detect plastic responses in host traits. I agree that differences in individual quality may explain part of the variance in responses. This possibility can be qualified by considering correlates of individual quality and testing the interaction between quality and parasitism on host traits. But the best choice would be to perform these experiments on the same individuals (or genetically related individuals) to analyze reaction norms in response to manipulated brood parasitism. Soler (2018b) stresses that “it would be worthwhile to emphasize the important role that comparative studies exploring geographical covariation between tolerance by hosts and brood parasite prevalence”. I agree, although I would urge controlling for population differences in host qualities to discard a “general vigor” effect. Lyon et al. (2018) suggest that some of the premises of the tolerance mechanism that I developed based on inter-specific brood parasitism (IBP) can naturally be expanded to CBP. They argue that CBP is a particularly suitable system to study the degree to which tolerance strategies may reduce parasitism costs in the long term, linking mechanisms and life history evolution. I totally agree with these points and consider CBP a suitable system to broaden the study of tolerance. Given the relative lower costs of CBP parasitism compared to IBP, tolerance is likely more prevalent among species affected by CBP than among those affected by IBP. Welbergen (2018) and Abolins-Abols and Hauber (2017) argue that the dichotomy between resistance and tolerance in terms of their cost to parasites may be artificial, as some traits providing tolerance are also likely to negatively impact on parasites. This practical difficulty, however, is not exclusive to a brood parasitism context and has been noted previously in the field of immunopathology (e.g., Raberg et al. 2009), and can be handled by testing whether parasite fitness is decreased in response to changes in host traits (Aviles 2017). Moreover, knowing whether brood parasites are impacted or not by host defensive mechanisms in cases where the parasite offspring survive will provide a more realistic assessment of the costs of parasitism and defense for host and brood parasite and, in the end, result in a better understanding of the eco-evolutionary dynamics between hosts and brood parasites. REFERENCES Abolins-Abols M , Hauber ME . 2018 . Applying the framework and concepts of parasitology to avian brood parasitism: a comment on Avilés . Behav Ecol . Avilés JM . 2017 . Can hosts tolerate avian brood parasites? an apprasial of mechanisms . Behav Ecol . doi:10.1093/beheco/arx150. Lyon BE , Eadie JM , Shizuka D . 2018 . Conspecific brood parasitism can also help us to understand the evoluton of tolerance: a comment on Avilés . Behav Ecol . Medina I , Langmore NE . 2018 . Tolerance in hosts of brood parasites: a comment on Avilés . Behav Ecol . Raberg L , Graham AL , Read AF . 2009 . Decomposing health: tolerance and resistance to parasites in animals . Philos Trans R Soc Lond B Biol Sci . 364 : 37 – 49 Google Scholar CrossRef Search ADS PubMed Soler JJ . 2018a . Tolerance to brood parasitism: a comment on Avilés . Behav Ecol . Soler M . 2018b . The reliability of current evidence on tolerance by hosts of brood parasites and suggestions for studying it: a comment on Avilés . Behav Ecol . Welbergen JA . 2018 . When resistance is futile - tolerance in avian brood parasite hosts: a comment on Avilés . Behav Ecol . © The Author(s) 2018. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com 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)

Journal

Behavioral EcologyOxford University Press

Published: Mar 13, 2018

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