The reliability of current evidence on tolerance by hosts of brood parasites and suggestions for studying it: a comment on Avilés

The reliability of current evidence on tolerance by hosts of brood parasites and suggestions for... The goal of stimulating interest in the study of tolerance as a defensive response against brood parasites is a challenging one and Avilés (2017) has been commendably thorough in searching the literature for evidence of host tolerance strategies. His paper is both timely and important, for 2 reasons. Firstly, it will help to stop the misuse of the term “tolerance” in the brood parasitism literature. For example, tolerance has been taken to mean acceptance of parasitic eggs (e.g. Petit 1991) and the term “nestmate tolerance” has often been used to mean non-evicting brood parasites, a situation better described as “nestmate acceptance” (Soler and de Neve 2013). Secondly, and more importantly, I agree with Avilés (2017) that since tolerance, together with resistance, is an important component of host defence, its consideration in brood parasitism studies would “achieve a better comprehension of avian brood parasite-host coevolution.” This latter conclusion is based on several reasons (not discussed by Avilés 2017). Since both resistance and tolerance are likely to be costly traits for the host, the evolution of tolerance should reduce selection for resistance, and vice versa (Svensson and Råberg 2010). Also, given that defensive resistance prevents parasitism or releases hosts from it, whereas defensive tolerance reduces the negative fitness effects of parasitism without affecting parasite fitness (Svensson and Råberg 2010), both types of host defence imply very different selective pressures on parasites, triggering different evolutionary outcomes in brood parasite–host coevolution (Medina and Langmore 2016; Soler and Soler 2017). For instance, host resistance, but not host tolerance, selects for counter-adaptation in parasites, so that only resistance will provoke antagonistic coevolution. Finally, the relative importance of host defensive tolerance and resistance will have a profound effect not only on host–parasite coevolution but also on the pace of evolutionary change of brood parasites (Soler and Soler 2017). Avilés (2017) has only found 10 studies, including those previously reported by Medina and Langmore (2016), which report effects presumably provoked by host tolerance. Hence it is worth emphasizing that, as underlined by Avilés (2017), “current evidence of tolerance is still inconclusive and very scarce” and there exists only one “explicit test of the adaptive value of tolerance in a brood parasitic system” (Soler et al. 2011). Moreover, evidence of tolerance is weaker than presented by Avilés (2017) in Table 1. The ‘evidence’ of tolerance reported in the cited studies is frequently misleading. To give just three examples: (i) not all “species suffering high parasitism have shorter nesting periods,” but only those of intermediate size (Remeš 2006). (ii) The result specified in Table 1 with respect to Petit’s (1991) study is a comment included in the Discussion section as a possibility, not a result. (iii) With respect to the study by Anderson et al. (2013), it is stated “populations suffering high parasitism have more nesting attempts,” which is incorrect; what is found is a geographical trend due to both prevalence of parasitism and number of nesting attempts being greater at higher latitudes. Furthermore, cases of tolerance based on instances of brood parasitism that result in reduced harm to hosts cannot be real tolerance because most host life-history adjustments taken as evidence of tolerance are likely to reduce the survival probability of the parasitic nestlings, implying resistance (as recognized by Avilés 2017). In addition, cases of potential tolerance may also be a consequence of the brood parasite reducing its virulence (Soler and Soler 2017). In all, convincing empirical evidence of tolerance is extremely rare and hard to obtain. I certainly agree with Avilés (2017) that there is an urgent need for studies investigating the role of tolerance in brood parasite – host systems. In general, I also agree with much of what he has suggested regarding the methodologies for studying tolerance, but have four comments to make. Firstly, I feel that the experimental method has been oversimplified and needs further consideration. Readers would need to be informed in detail about how a similar experimental approach to that used in studies of plasticity in resistance defences could be used to study tolerance. In addition, it is worth mentioning that in order to demonstrate experimentally that a life-history trait is an evolved defence based on tolerance of brood parasitism, it needs to be shown that hosts with such a trait are proportionally less affected by brood parasitism than those that lack it. Secondly, I think it is worthwhile to emphasize the important role that comparative studies exploring geographical covariation between tolerance by hosts and brood parasite prevalence in different host populations could play in the study of tolerance (see Soler et al. 2011). The predicted negative relationship between levels of tolerance and resistance could also be tested by estimating the level of host resistance. Thirdly, I suggest that studies of host tolerance should also examine how host defensive responses (tolerance/resistance) comparatively affect brood parasites, a broader approach that would enable general coevolutionary predictions to be tested. For instance, host tolerance would select for facultative virulence in brood parasites and facultative virulence of parasites would select for tolerance by their hosts (Soler and Soler 2017). Finally, tolerance is not expected to play a role of similar importance in all brood parasite—host systems as Avilés (2017; Figure 2) seems to assume. Specifically, tolerance will be more frequent and easily detected in brood parasites showing facultative virulence against their hosts than in brood parasites exhibiting fixed virulence (Soler and Soler 2017). Thus, considering the magnitude of effort involved in studying tolerance, it would be worthwhile to identify those brood parasites in which investigation of tolerance could be more fruitful. As a generalization, evictor brood parasites exhibit higher and fixed virulence while non-evictors, which share the nest with host nestlings, exhibit lower and facultative virulence. Therefore, tolerance defence can be predicted to be more frequent and easier to detect in non-evictor brood parasites. I hope these comments will help to put future research on tolerance by brood parasite hosts on a more practical foundation. REFERENCES Anderson MG, Gill BJ, Briskie JV, Brunton DH, Hauber ME. 2013. Latitudinal differences in the breeding phenology of Grey Warblers covary with the prevalence of parasitism by Shining Bronze-Cuckoos. Emu . 113: 187– 191. Google Scholar CrossRef Search ADS   Avilés JM. 2017. Can hosts tolerate avian brood parasites? An appraisal of mechanisms. Behav Ecol . doi:10.1093/beheco/arx150. Medina I, Langmore NE. 2016. The evolution of acceptance and tolerance in hosts of avian brood parasites. Biol Rev . 91: 569– 577. Google Scholar CrossRef Search ADS PubMed  Petit LJ. 1991. Adaptive tolerance of cowbird parasitism by prothonotary warblers - a consequence of nest-site limitation. Anim Behav  41: 425– 432. Google Scholar CrossRef Search ADS   Remeš, V. 2006. Growth strategies of passerine birds are related to brood parasitism by the brown-headed cowbird (Molothrus ater). Evolution 60: 1692– 1700. 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  Soler JJ, Soler M. 2017. Evolutionary change: facultative virulence by brood parasites and tolerance and plastic resistance by hosts. Anim Behav . 125: 101– 107. Google Scholar CrossRef Search ADS   Soler M, de Neve L. 2013. Brood mate eviction or brood mate acceptance by brood parasitic nestlings? An experimental study with the non-evictor great spotted cuckoo and its magpie host. Behav Ecol Sociobiol . 67: 601– 607. Google Scholar CrossRef Search ADS   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) 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

The reliability of current evidence on tolerance by hosts of brood parasites and suggestions for studying it: a comment on Avilés

Behavioral Ecology , Volume Advance Article (3) – Jan 30, 2018

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Abstract

The goal of stimulating interest in the study of tolerance as a defensive response against brood parasites is a challenging one and Avilés (2017) has been commendably thorough in searching the literature for evidence of host tolerance strategies. His paper is both timely and important, for 2 reasons. Firstly, it will help to stop the misuse of the term “tolerance” in the brood parasitism literature. For example, tolerance has been taken to mean acceptance of parasitic eggs (e.g. Petit 1991) and the term “nestmate tolerance” has often been used to mean non-evicting brood parasites, a situation better described as “nestmate acceptance” (Soler and de Neve 2013). Secondly, and more importantly, I agree with Avilés (2017) that since tolerance, together with resistance, is an important component of host defence, its consideration in brood parasitism studies would “achieve a better comprehension of avian brood parasite-host coevolution.” This latter conclusion is based on several reasons (not discussed by Avilés 2017). Since both resistance and tolerance are likely to be costly traits for the host, the evolution of tolerance should reduce selection for resistance, and vice versa (Svensson and Råberg 2010). Also, given that defensive resistance prevents parasitism or releases hosts from it, whereas defensive tolerance reduces the negative fitness effects of parasitism without affecting parasite fitness (Svensson and Råberg 2010), both types of host defence imply very different selective pressures on parasites, triggering different evolutionary outcomes in brood parasite–host coevolution (Medina and Langmore 2016; Soler and Soler 2017). For instance, host resistance, but not host tolerance, selects for counter-adaptation in parasites, so that only resistance will provoke antagonistic coevolution. Finally, the relative importance of host defensive tolerance and resistance will have a profound effect not only on host–parasite coevolution but also on the pace of evolutionary change of brood parasites (Soler and Soler 2017). Avilés (2017) has only found 10 studies, including those previously reported by Medina and Langmore (2016), which report effects presumably provoked by host tolerance. Hence it is worth emphasizing that, as underlined by Avilés (2017), “current evidence of tolerance is still inconclusive and very scarce” and there exists only one “explicit test of the adaptive value of tolerance in a brood parasitic system” (Soler et al. 2011). Moreover, evidence of tolerance is weaker than presented by Avilés (2017) in Table 1. The ‘evidence’ of tolerance reported in the cited studies is frequently misleading. To give just three examples: (i) not all “species suffering high parasitism have shorter nesting periods,” but only those of intermediate size (Remeš 2006). (ii) The result specified in Table 1 with respect to Petit’s (1991) study is a comment included in the Discussion section as a possibility, not a result. (iii) With respect to the study by Anderson et al. (2013), it is stated “populations suffering high parasitism have more nesting attempts,” which is incorrect; what is found is a geographical trend due to both prevalence of parasitism and number of nesting attempts being greater at higher latitudes. Furthermore, cases of tolerance based on instances of brood parasitism that result in reduced harm to hosts cannot be real tolerance because most host life-history adjustments taken as evidence of tolerance are likely to reduce the survival probability of the parasitic nestlings, implying resistance (as recognized by Avilés 2017). In addition, cases of potential tolerance may also be a consequence of the brood parasite reducing its virulence (Soler and Soler 2017). In all, convincing empirical evidence of tolerance is extremely rare and hard to obtain. I certainly agree with Avilés (2017) that there is an urgent need for studies investigating the role of tolerance in brood parasite – host systems. In general, I also agree with much of what he has suggested regarding the methodologies for studying tolerance, but have four comments to make. Firstly, I feel that the experimental method has been oversimplified and needs further consideration. Readers would need to be informed in detail about how a similar experimental approach to that used in studies of plasticity in resistance defences could be used to study tolerance. In addition, it is worth mentioning that in order to demonstrate experimentally that a life-history trait is an evolved defence based on tolerance of brood parasitism, it needs to be shown that hosts with such a trait are proportionally less affected by brood parasitism than those that lack it. Secondly, I think it is worthwhile to emphasize the important role that comparative studies exploring geographical covariation between tolerance by hosts and brood parasite prevalence in different host populations could play in the study of tolerance (see Soler et al. 2011). The predicted negative relationship between levels of tolerance and resistance could also be tested by estimating the level of host resistance. Thirdly, I suggest that studies of host tolerance should also examine how host defensive responses (tolerance/resistance) comparatively affect brood parasites, a broader approach that would enable general coevolutionary predictions to be tested. For instance, host tolerance would select for facultative virulence in brood parasites and facultative virulence of parasites would select for tolerance by their hosts (Soler and Soler 2017). Finally, tolerance is not expected to play a role of similar importance in all brood parasite—host systems as Avilés (2017; Figure 2) seems to assume. Specifically, tolerance will be more frequent and easily detected in brood parasites showing facultative virulence against their hosts than in brood parasites exhibiting fixed virulence (Soler and Soler 2017). Thus, considering the magnitude of effort involved in studying tolerance, it would be worthwhile to identify those brood parasites in which investigation of tolerance could be more fruitful. As a generalization, evictor brood parasites exhibit higher and fixed virulence while non-evictors, which share the nest with host nestlings, exhibit lower and facultative virulence. Therefore, tolerance defence can be predicted to be more frequent and easier to detect in non-evictor brood parasites. I hope these comments will help to put future research on tolerance by brood parasite hosts on a more practical foundation. REFERENCES Anderson MG, Gill BJ, Briskie JV, Brunton DH, Hauber ME. 2013. Latitudinal differences in the breeding phenology of Grey Warblers covary with the prevalence of parasitism by Shining Bronze-Cuckoos. Emu . 113: 187– 191. Google Scholar CrossRef Search ADS   Avilés JM. 2017. Can hosts tolerate avian brood parasites? An appraisal of mechanisms. Behav Ecol . doi:10.1093/beheco/arx150. Medina I, Langmore NE. 2016. The evolution of acceptance and tolerance in hosts of avian brood parasites. Biol Rev . 91: 569– 577. Google Scholar CrossRef Search ADS PubMed  Petit LJ. 1991. Adaptive tolerance of cowbird parasitism by prothonotary warblers - a consequence of nest-site limitation. Anim Behav  41: 425– 432. Google Scholar CrossRef Search ADS   Remeš, V. 2006. Growth strategies of passerine birds are related to brood parasitism by the brown-headed cowbird (Molothrus ater). Evolution 60: 1692– 1700. 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  Soler JJ, Soler M. 2017. Evolutionary change: facultative virulence by brood parasites and tolerance and plastic resistance by hosts. Anim Behav . 125: 101– 107. Google Scholar CrossRef Search ADS   Soler M, de Neve L. 2013. Brood mate eviction or brood mate acceptance by brood parasitic nestlings? An experimental study with the non-evictor great spotted cuckoo and its magpie host. Behav Ecol Sociobiol . 67: 601– 607. Google Scholar CrossRef Search ADS   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) 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: Jan 30, 2018

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