When resistance is futile - tolerance in avian brood parasite hosts: a comment on Avilés

When resistance is futile - tolerance in avian brood parasite hosts: a comment on Avilés The reciprocal interactions between avian brood parasites and their hosts have become canonical examples of coevolution (Davies 2000). Historically, the focus has been on adaptations that allow hosts to “resist” parasitism (e.g., egg rejection). In his review, Avilés (2017) argues compellingly that adaptations that help hosts “tolerate” parasitism (e.g., enhanced chick competitiveness) have been neglected, and he does a great service by bringing this potentially pervasive set of defenses to the fore (see also Medina and Langmore 2016). In addition, the review helpfully lays out a framework for investigating tolerance, using a reaction norm approach. Perhaps this framework could be extended to incorporate plastic/learnt resistance traits (e.g., Welbergen and Davies 2012) and so bring about a more holistic understanding of defense plasticity in hosts? Where the review does seem to run into some trouble, however, is around what exactly constitutes resistance and tolerance. There is already conceptual inconsistency across fields as to how these terms are applied (Read et al. 2008) and we should guard against uncritical adoption of terminologies from differing epistemological traditions. Some of this inconsistency is perpetuated by the language in Avilés’ review. For example, “mechanisms minimizing the frequency of effective parasite attacks” (p509) entails a definition of resistance that sensu stricto excludes all defenses that are deployed after the parasitic egg is laid; although this is evidently not intended. Perhaps more fundamentally problematic is the notion that tolerance will not select for parasite counteradaptations. Tolerance, by original definitions (e.g., Svensson and Råberg 2010), does not impose a fitness cost on the parasite, so that it “will not” (Svensson and Råberg 2010, p267) or “rarely” (Avilés 2017, p509) result in antagonistic coevolution. However, host defenses evolve because of selection on hosts so that dichotomizing a suite of host defenses in terms of their fitness effects on parasites is functionally akin to putting the cart before the horse. Indeed, “tolerance” strategies may diminish parasite fitness as a non-selected by-product (see also: Svensson and Råberg 2010) or as an added selective benefit (e.g., below). Yet, in Avilés’ review, as soon as there is a negative fitness impact on the parasite, tolerance “switches” (p514) to resistance or is no longer “true” (p511). The current dichotomy may also obscure the eco-evolutionary significance of host defenses. For example, host chicks may be under selection to compete more intensely for food in the presence of nonevictor parasites [which may even result in mimicry of parasite mouth markings by host chicks (Hauber and Kilner 2007)]. Here, increased chick competitiveness would be considered a tolerance strategy as it enables host chicks to access resources that would otherwise be usurped by parasitic chicks; however, this likely affects parasite fitness as it withdraws resources from the parasite’s offspring and so shares defining characteristics of resistance too. As a converse example, nest desertion in response to parasitism would be a resistance strategy as it renders parasitism unsuccessful; however, it also reduces harm from parasitism by freeing up time and resources for a renesting attempt (Davies and Brooke 1988) and thus arguably shares defining characteristics of tolerance as well. While Avilés’ review recognizes the difficulty of assigning such dualistic cases to resistance or tolerance, it provides no solutions. I suggest a more inclusive resolution to this conceptual conundrum: hosts can reduce the negative fitness consequences from brood parasitism with i) strategies that prevent or terminate parasitic exploitation (“resistance”) and ii) strategies that decrease the proximate harm incurred during exploitation (“tolerance”). To borrow terminology from an even more distantly-related field (Williams et al. 2008), i) includes all strategies that reduce a host’s “exposure” to exploitation, whereas ii) includes all strategies that reduce a host’s “sensitivity” to that exploitation given a certain level of exposure; however, both i) and ii) ultimately reduce a host’s “vulnerability” to the potential negative fitness impacts from parasitism. Framed this way, it is perfectly reasonable for a defense to perform both functions simultaneously. Indeed, they can then be considered truly “non-mutually exclusive responses to parasitism” (Avilés 2017, p510) and can be expected to coevolve (Medina and Langmore 2016) as closely intertwined components of a host’s portfolio of antiparasitism adaptations (Welbergen and Davies 2009). Therefore, we should ask: does the defense enable a host to resist or tolerate parasitism, or both? REFERENCES Avilés JM. 2017. Can hosts tolerate avian brood parasites? An appraisal of mechanisms. Behav Ecol . doi: 10.1093/beheco/arx150 Davies NB. 2000. Cuckoos, cowbirds and other cheats . London: T. & A.D. Poyser. Davies NB, Brooke MdL. 1988. Cuckoos versus reed warblers: adaptations and counteradaptations. Anim Behav . 36: 262– 284. Google Scholar CrossRef Search ADS   Hauber ME, Kilner RM. 2007. Coevolution, communication, and host chick mimicry in parasitic finches: who mimics whom? Behav Ecol Sociobiol . 61: 497– 503. 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  Read AF, Graham AL, Råberg L. 2008. Animal defenses against infectious agents: is damage control more important than pathogen control. PLoS Biol . 6: e4. 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  Welbergen JA, Davies NB. 2009. Strategic variation in mobbing as a front line of defense against brood parasitism. Curr Biol . 19: 235– 240. Google Scholar CrossRef Search ADS PubMed  Welbergen JA, Davies NB. 2012. Direct and indirect assessment of parasitism risk by a cuckoo host. Behav Ecol . 23:783–789. Williams SE, Shoo LP, Isaac JL, Hoffmann AA, Langham G. 2008. Towards an integrated framework for assessing the vulnerability of species to climate change. PLoS Biol . 6: 2621– 2626. Google Scholar CrossRef Search ADS PubMed  © 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

When resistance is futile - tolerance in avian brood parasite hosts: a comment on Avilés

Behavioral Ecology , Volume Advance Article (3) – Mar 7, 2018

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Oxford University Press
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© 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
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1045-2249
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1465-7279
D.O.I.
10.1093/beheco/ary019
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Abstract

The reciprocal interactions between avian brood parasites and their hosts have become canonical examples of coevolution (Davies 2000). Historically, the focus has been on adaptations that allow hosts to “resist” parasitism (e.g., egg rejection). In his review, Avilés (2017) argues compellingly that adaptations that help hosts “tolerate” parasitism (e.g., enhanced chick competitiveness) have been neglected, and he does a great service by bringing this potentially pervasive set of defenses to the fore (see also Medina and Langmore 2016). In addition, the review helpfully lays out a framework for investigating tolerance, using a reaction norm approach. Perhaps this framework could be extended to incorporate plastic/learnt resistance traits (e.g., Welbergen and Davies 2012) and so bring about a more holistic understanding of defense plasticity in hosts? Where the review does seem to run into some trouble, however, is around what exactly constitutes resistance and tolerance. There is already conceptual inconsistency across fields as to how these terms are applied (Read et al. 2008) and we should guard against uncritical adoption of terminologies from differing epistemological traditions. Some of this inconsistency is perpetuated by the language in Avilés’ review. For example, “mechanisms minimizing the frequency of effective parasite attacks” (p509) entails a definition of resistance that sensu stricto excludes all defenses that are deployed after the parasitic egg is laid; although this is evidently not intended. Perhaps more fundamentally problematic is the notion that tolerance will not select for parasite counteradaptations. Tolerance, by original definitions (e.g., Svensson and Råberg 2010), does not impose a fitness cost on the parasite, so that it “will not” (Svensson and Råberg 2010, p267) or “rarely” (Avilés 2017, p509) result in antagonistic coevolution. However, host defenses evolve because of selection on hosts so that dichotomizing a suite of host defenses in terms of their fitness effects on parasites is functionally akin to putting the cart before the horse. Indeed, “tolerance” strategies may diminish parasite fitness as a non-selected by-product (see also: Svensson and Råberg 2010) or as an added selective benefit (e.g., below). Yet, in Avilés’ review, as soon as there is a negative fitness impact on the parasite, tolerance “switches” (p514) to resistance or is no longer “true” (p511). The current dichotomy may also obscure the eco-evolutionary significance of host defenses. For example, host chicks may be under selection to compete more intensely for food in the presence of nonevictor parasites [which may even result in mimicry of parasite mouth markings by host chicks (Hauber and Kilner 2007)]. Here, increased chick competitiveness would be considered a tolerance strategy as it enables host chicks to access resources that would otherwise be usurped by parasitic chicks; however, this likely affects parasite fitness as it withdraws resources from the parasite’s offspring and so shares defining characteristics of resistance too. As a converse example, nest desertion in response to parasitism would be a resistance strategy as it renders parasitism unsuccessful; however, it also reduces harm from parasitism by freeing up time and resources for a renesting attempt (Davies and Brooke 1988) and thus arguably shares defining characteristics of tolerance as well. While Avilés’ review recognizes the difficulty of assigning such dualistic cases to resistance or tolerance, it provides no solutions. I suggest a more inclusive resolution to this conceptual conundrum: hosts can reduce the negative fitness consequences from brood parasitism with i) strategies that prevent or terminate parasitic exploitation (“resistance”) and ii) strategies that decrease the proximate harm incurred during exploitation (“tolerance”). To borrow terminology from an even more distantly-related field (Williams et al. 2008), i) includes all strategies that reduce a host’s “exposure” to exploitation, whereas ii) includes all strategies that reduce a host’s “sensitivity” to that exploitation given a certain level of exposure; however, both i) and ii) ultimately reduce a host’s “vulnerability” to the potential negative fitness impacts from parasitism. Framed this way, it is perfectly reasonable for a defense to perform both functions simultaneously. Indeed, they can then be considered truly “non-mutually exclusive responses to parasitism” (Avilés 2017, p510) and can be expected to coevolve (Medina and Langmore 2016) as closely intertwined components of a host’s portfolio of antiparasitism adaptations (Welbergen and Davies 2009). Therefore, we should ask: does the defense enable a host to resist or tolerate parasitism, or both? REFERENCES Avilés JM. 2017. Can hosts tolerate avian brood parasites? An appraisal of mechanisms. Behav Ecol . doi: 10.1093/beheco/arx150 Davies NB. 2000. Cuckoos, cowbirds and other cheats . London: T. & A.D. Poyser. Davies NB, Brooke MdL. 1988. Cuckoos versus reed warblers: adaptations and counteradaptations. Anim Behav . 36: 262– 284. Google Scholar CrossRef Search ADS   Hauber ME, Kilner RM. 2007. Coevolution, communication, and host chick mimicry in parasitic finches: who mimics whom? Behav Ecol Sociobiol . 61: 497– 503. 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  Read AF, Graham AL, Råberg L. 2008. Animal defenses against infectious agents: is damage control more important than pathogen control. PLoS Biol . 6: e4. 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  Welbergen JA, Davies NB. 2009. Strategic variation in mobbing as a front line of defense against brood parasitism. Curr Biol . 19: 235– 240. Google Scholar CrossRef Search ADS PubMed  Welbergen JA, Davies NB. 2012. Direct and indirect assessment of parasitism risk by a cuckoo host. Behav Ecol . 23:783–789. Williams SE, Shoo LP, Isaac JL, Hoffmann AA, Langham G. 2008. Towards an integrated framework for assessing the vulnerability of species to climate change. PLoS Biol . 6: 2621– 2626. Google Scholar CrossRef Search ADS PubMed  © 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 7, 2018

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