Applying the framework and concepts of parasitology to avian brood parasitism: a comment on Avilés

Applying the framework and concepts of parasitology to avian brood parasitism: a comment on Avilés Most research in avian brood parasite and host systems to date has focused on 1) the ways by which hosts reject parasitism and 2) the parasites’ counter-adaptations that evolve to circumvent host defenses (Davies 2000). In his perspective piece, Avilés (2017) suggests that historical practices have distracted the scientific community from the opportunity to discuss avian brood parasitism in the context of broader eco-evolutionary principles of general host–parasite interactions. To overcome this constraint, he recommends that avian brood parasitism should be studied in the context of 2 terms re/introduced from the area of host-parasite interactions: resistance and tolerance (Medina and Langmore 2016), and that the field should adapt a reaction-norm perspective. We address briefly here what we see as one concern and one benefit of the approach advocated by Avilés. First, we consider that the definitions of resistance and tolerance that Avilés adopts from the literature do not accurately represent the cognitive and evolutionary context of avian brood parasitism. Avilés suggests that “resistance [is the collection of hosts’] mechanisms minimizing the frequency of effective parasite attacks”. In turn, “tolerance [is the collection of hosts’] mechanisms minimizing the impact of parasites after a successful attack”. According to a strict interpretation of these definitions, nest defense by hosts prior to egg laying qualifies as resistance whereas egg or chick rejection following parasitism qualifies as tolerance. However, this is not how Avilés eventually classifies host responses: instead, host responses resulting in the cessation of successful parasitism (parasitic offspring do not survive) should be considered resistance, while cases where the parasitic egg(s) and offspring continue to survive should be considered tolerance. This classification seems to be driven by the other aspect of the classical tolerance definition, namely that “tolerance diminishes the impact of parasite (upon the host) without causing direct negative effects in the parasite.” Therefore, we consider that only certain aspects of the classical definitions of resistance and tolerance are applicable to avian brood parasitism, which also begs a question of their general utility across the field of parasitology. Furthermore, we suggest that the dichotomy between resistance and tolerance in terms of their costs to parasite, while conceptually useful, may be biologically artificial, because, as Avilés suggests, it is likely that some traits increasing tolerance of the hosts will also have negative effects on the parasite. Despite these problems, we agree with Avilés that studies of appropriately defined tolerance in avian brood parasitism has indeed been studied very seldom (but see Soler et al. 2010; Takasu and Moskát 2011). In turn, we regard that the most opportune contribution of Avilés’ article to the field is his proposal of a framework that generates predictions about how hosts or host populations are expected to alter their (and their nestling) behavior, life-histories, and physiology to minimize the negative fitness effect of raising a parasitic nestling. Avilés suggests that these predictions are best tested using the reaction norm approach, where individuals or populations are tested across various levels of parasitism (e.g., none/single/multiple) to establish the slope of the reaction norm (the level of tolerance, Svensson and Råberg 2010). One utility of this approach, as Avilés suggests, is that reaction norms can reveal the contribution of genetic versus environmental factors to variation in tolerance. We applaud this suggestion, because heritability of hosts’ defenses against avian brood parasites has been broadly understudied. A further benefit of the reaction norm approach is that it transcends the artificial dichotomy between resistance and tolerance because it does not make assumptions about parasite fitness, and allows to conceive resistance (mean parasitism) and tolerance (slope) simultaneously. We also suggest that whether differences in tolerance are evident at the population-level, or across individually plastic responses, depends on the cost of producing the suboptimal phenotype, and the frequency of producing that phenotype (DeWitt et al. 1998). If the combined costs of a trait’s impact are higher in a population with a static phenotype, plasticity is expected to evolve, and vice versa. Such approach could incorporate the methods and concepts from already strong experimental tradition of studying the role of costs of own egg and nestling rejection due to perceptual mistakes in the evolution of resistance behavior in brood parasite hosts. In summary, Avilés provides a compelling case for expanding the terminological, conceptual, and practical scopes of avian host–parasite studies to include studies of tolerance. However, we advise that the traditional notion that traits fall into either resistance or tolerance categories may itself constrain the progress, and that they should be treated as endpoints of a continuum. We consider that the reaction norm framework is promising and may hold the potential suggested by the author but also note that strong inference from reaction norm approaches is achievable only in a few systems that experience multiple parasitism naturally and when sample sizes are large (Martin et al. 2011). REFERENCES Avilés JM. 2017. Can hosts tolerate avian brood parasites? An appraisal of mechanisms. Behav Ecol . 29: 509– 519. Google Scholar CrossRef Search ADS   Davies NB. 2000. Cuckoos, cowbirds, and other cheats . London: Poyser. Dewitt TJ, Sih A, Wilson DS. 1998. Costs and limits of phenotypic plasticity. Trends Ecol Evol . 13: 77– 81. Google Scholar CrossRef Search ADS PubMed  Martin JG a, Nussey DH, Wilson AJ, Réale D. 2011. Measuring individual differences in reaction norms in field and experimental studies: a power analysis of random regression models. Methods Ecol Evol . 2: 362– 374. Google Scholar CrossRef Search ADS   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  Soler JJ, Martín-Gálvez D, Martínez JG, Soler M, Canestrari D, Abad-Gómez JM, Møller AP. 2011. Evolution of tolerance by magpies to brood parasitism by great spotted cuckoos. Proc Biol Sci . 278: 2047– 2052. 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  Takasu F, Moskát C. 2011. Modeling the consequence of increased host tolerance toward avian brood parasitism. Popul Ecol . 53: 187– 193. Google Scholar CrossRef Search ADS   © 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: 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

Applying the framework and concepts of parasitology to avian brood parasitism: a comment on Avilés

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Oxford University Press
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© 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: journals.permissions@oup.com
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1045-2249
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1465-7279
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10.1093/beheco/arx178
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Abstract

Most research in avian brood parasite and host systems to date has focused on 1) the ways by which hosts reject parasitism and 2) the parasites’ counter-adaptations that evolve to circumvent host defenses (Davies 2000). In his perspective piece, Avilés (2017) suggests that historical practices have distracted the scientific community from the opportunity to discuss avian brood parasitism in the context of broader eco-evolutionary principles of general host–parasite interactions. To overcome this constraint, he recommends that avian brood parasitism should be studied in the context of 2 terms re/introduced from the area of host-parasite interactions: resistance and tolerance (Medina and Langmore 2016), and that the field should adapt a reaction-norm perspective. We address briefly here what we see as one concern and one benefit of the approach advocated by Avilés. First, we consider that the definitions of resistance and tolerance that Avilés adopts from the literature do not accurately represent the cognitive and evolutionary context of avian brood parasitism. Avilés suggests that “resistance [is the collection of hosts’] mechanisms minimizing the frequency of effective parasite attacks”. In turn, “tolerance [is the collection of hosts’] mechanisms minimizing the impact of parasites after a successful attack”. According to a strict interpretation of these definitions, nest defense by hosts prior to egg laying qualifies as resistance whereas egg or chick rejection following parasitism qualifies as tolerance. However, this is not how Avilés eventually classifies host responses: instead, host responses resulting in the cessation of successful parasitism (parasitic offspring do not survive) should be considered resistance, while cases where the parasitic egg(s) and offspring continue to survive should be considered tolerance. This classification seems to be driven by the other aspect of the classical tolerance definition, namely that “tolerance diminishes the impact of parasite (upon the host) without causing direct negative effects in the parasite.” Therefore, we consider that only certain aspects of the classical definitions of resistance and tolerance are applicable to avian brood parasitism, which also begs a question of their general utility across the field of parasitology. Furthermore, we suggest that the dichotomy between resistance and tolerance in terms of their costs to parasite, while conceptually useful, may be biologically artificial, because, as Avilés suggests, it is likely that some traits increasing tolerance of the hosts will also have negative effects on the parasite. Despite these problems, we agree with Avilés that studies of appropriately defined tolerance in avian brood parasitism has indeed been studied very seldom (but see Soler et al. 2010; Takasu and Moskát 2011). In turn, we regard that the most opportune contribution of Avilés’ article to the field is his proposal of a framework that generates predictions about how hosts or host populations are expected to alter their (and their nestling) behavior, life-histories, and physiology to minimize the negative fitness effect of raising a parasitic nestling. Avilés suggests that these predictions are best tested using the reaction norm approach, where individuals or populations are tested across various levels of parasitism (e.g., none/single/multiple) to establish the slope of the reaction norm (the level of tolerance, Svensson and Råberg 2010). One utility of this approach, as Avilés suggests, is that reaction norms can reveal the contribution of genetic versus environmental factors to variation in tolerance. We applaud this suggestion, because heritability of hosts’ defenses against avian brood parasites has been broadly understudied. A further benefit of the reaction norm approach is that it transcends the artificial dichotomy between resistance and tolerance because it does not make assumptions about parasite fitness, and allows to conceive resistance (mean parasitism) and tolerance (slope) simultaneously. We also suggest that whether differences in tolerance are evident at the population-level, or across individually plastic responses, depends on the cost of producing the suboptimal phenotype, and the frequency of producing that phenotype (DeWitt et al. 1998). If the combined costs of a trait’s impact are higher in a population with a static phenotype, plasticity is expected to evolve, and vice versa. Such approach could incorporate the methods and concepts from already strong experimental tradition of studying the role of costs of own egg and nestling rejection due to perceptual mistakes in the evolution of resistance behavior in brood parasite hosts. In summary, Avilés provides a compelling case for expanding the terminological, conceptual, and practical scopes of avian host–parasite studies to include studies of tolerance. However, we advise that the traditional notion that traits fall into either resistance or tolerance categories may itself constrain the progress, and that they should be treated as endpoints of a continuum. We consider that the reaction norm framework is promising and may hold the potential suggested by the author but also note that strong inference from reaction norm approaches is achievable only in a few systems that experience multiple parasitism naturally and when sample sizes are large (Martin et al. 2011). REFERENCES Avilés JM. 2017. Can hosts tolerate avian brood parasites? An appraisal of mechanisms. Behav Ecol . 29: 509– 519. Google Scholar CrossRef Search ADS   Davies NB. 2000. Cuckoos, cowbirds, and other cheats . London: Poyser. Dewitt TJ, Sih A, Wilson DS. 1998. Costs and limits of phenotypic plasticity. Trends Ecol Evol . 13: 77– 81. Google Scholar CrossRef Search ADS PubMed  Martin JG a, Nussey DH, Wilson AJ, Réale D. 2011. Measuring individual differences in reaction norms in field and experimental studies: a power analysis of random regression models. Methods Ecol Evol . 2: 362– 374. Google Scholar CrossRef Search ADS   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  Soler JJ, Martín-Gálvez D, Martínez JG, Soler M, Canestrari D, Abad-Gómez JM, Møller AP. 2011. Evolution of tolerance by magpies to brood parasitism by great spotted cuckoos. Proc Biol Sci . 278: 2047– 2052. 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  Takasu F, Moskát C. 2011. Modeling the consequence of increased host tolerance toward avian brood parasitism. Popul Ecol . 53: 187– 193. Google Scholar CrossRef Search ADS   © 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: 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: Dec 22, 2017

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