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Selecting for Tolerance Against Pathogens and Herbivores to Enhance Success of Reintroduction and Translocation

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Selecting for Tolerance Against Pathogens and Herbivores to Enhance Success of Reintroduction and Translocation Essay Selecting for Tolerance against Pathogens and Herbivores to Enhance Success of Reintroduction and Translocation MATTHEW D. VENESKY,∗† JOSEPH R. MENDELSON III,‡§ BRITTANY F. SEARS,∗ PETER STILING,∗ AND JASON R. ROHR∗ ∗Department of Integrative Biology, The University of South Florida, 4202 East Fowler Avenue, SCA 110, Tampa, FL 33620, U.S.A. ‡Zoo Atlanta, 800 Cherokee Avenue SE, Atlanta, GA 30315, U.S.A. §Georgia Institute of Technology, School of Biology, 301 Ferst Drive, Atlanta, GA 30332, U.S.A. Abstract: Some species have insufficient defenses against climate change, emerging infectious diseases, and non-native species because they have not been exposed to these factors over their evolutionary history, and this can decrease their likelihood of persistence. Captive breeding programs are sometimes used to reintroduce individuals back into the wild; however, successful captive breeding and reintroduction can be difficult because species or populations often cannot coexist with non-native pathogens and herbivores without artificial selection. In captive breeding programs, breeders can select for host defenses that prevent or reduce pathogen or herbivore burden (i.e., resistance) or traits that limit the effects of parasitism or herbivory on host fitness (i.e., tolerance). We propose that selection for host tolerance may enhance the success of reintroduction or translocation because tolerant hosts generally have neutral effects on introduced pathogens and herbivores. The release of resistant hosts would have detrimental effects on their natural enemies, promoting rapid evolution to circumvent the host resistance that may reduce the long-term probability of persistence of the reintroduced or translocated species. We examined 2 case studies, one on the pathogenic amphibian chytrid fungus ( Batrachochytrium dendrobatidis [Bd]) and the other on the herbivorous cactus moth ( Cactoblastis cactorum) in the United States, where it is not native. In each case study, we provide recommendations for how captive breeders and managers could go about selecting for host tolerance. Selecting for tolerance may offer a promising tool to rescue hosts species from invasive natural enemies as well as new natural enemies associated with climate change-induced range shifts. Keywords: artificial selection, Batrachochytrium dendrobatidis, Cactoblastis cactorum, cactus moth, captive breeding, chytridiomycosis, non-native species, tolerance Seleccion´ de Tolerancia a Patogenos´ y Herb´ıvoros para Incrementar el Exito´ de la Reintroduccion´ y la Translocacion´ Resumen: Algunas especies no tienen suficientes defensas contra el cambio climatico,´ enfermedades in- fecciosas emergentes y especies no nativas porque no han sido expuestas a estos factores a lo largo de su historia evolutiva, y esto puede disminuir su probabilidad de persistencia. El ´exito de la reproduccion´ en cautiverio y de la reintroduccion´ puede ser dif´ıcil porque las especies o poblaciones a menudo no pueden coexistir con patogenos´ y herb´ıvoros no nativos sin seleccion´ artificial. En programas de reproduccion´ en cau- tiverio, los criadores pueden seleccionar defensas que prevengan infecciones o herbivor´ıa o que reducen la carga de patogenos´ o herb´ıvoros atacando directamente al patogeno´ o herb´ıvoro (i.e., resistencia) o atributos que limitan los efectos del parasitismo o la herbivor´ıa sobre la adaptabilidad del hu´esped (i.e., tolerancia). †email [email protected] Paper submitted August 16, 2011; revised manuscript accepted January 13, 2012. 586 Conservation Biology, Volume 26, No. 4, 586–592 C 2012 Society for Conservation Biology DOI: 10.1111/j.1523-1739.2012.01854.x Venesky et al. 587 Proponemos que la seleccion´ de tolerancia del hu´esped puede incrementar el ´exito de los programas de reintro- duccion´ o translocacion.´ Nuestra hipotesis´ es que los hu´espedes tolerantes generalmente tienen efectos neutros sobre patogenos´ y herb´ıvoros introducidos. En contraste, planteamos la hipotesis´ que los hu´espedes resistentes tienen efectos perjudiciales sobre los patogenos´ y herb´ıvoros porque promueven la evolucion´ rapida´ para sortear la resistencia del hu´esped, lo cual puede reducir la probabilidad de persistencia a largo plazo de la especie reintroducida o translocada. Examinamos dos casos de estudio, uno en el hongo quitridio patogeno´ de anfibios ( Batrachochytrium dendrobatidis [Bd]) y el otro en la polilla herb´ıvora ( Cactoblastis cactorum) en los Estados Unidos, donde es no nativa. Con anfibios, la tolerancia a Bd puede provenir de respuestas inmunologicas´ o de atributos fisiologicos´ que mantienen la funcion´ osmorguladora. En cactos, la tolerancia alaherbivor´ıa puede ser mediada por incremento en la produccion´ de brotes o por redistribucion´ de energ´ıa de las ra´ıces a la reproduccion.´ El conocimiento de la importancia relativa de la tolerancia de hu´espedes versus la resistencia podr´ıa tener implicaciones para taxa de plantas y animales amenazados. Palabras Clave: Batrachochytrium dendrobatidis, Cactoblastis cactorum, especie no nativa, polilla del cacto, quitridiomicosis, reproduccion´ en cautiverio, seleccion´ artificial, tolerancia Introduction a constant exposure to the pathogen or herbivore. Tol- erance reduces the fitness consequences of a particular Some species have insufficient defenses against intro- pathogen load or level of herbivory and thus, unlike re- duced pathogens and predators because they have not sistance, it is hypothesized to have either a neutral or been exposed to these organisms over evolutionary time. positive effect on the pathogen or herbivore (Miller et As species continue to shift their distributions naturally in al. 2006). Tolerance is typically measured as the slope response to climate change or as their distributions are of the relation between host fitness (or a proxy measure changed artificially through translocation, they will be of fitness) and pathogen or herbivore abundance (Fig. 1) more likely to be exposed to non-native pathogens and (Raberg et al. 2007; Raberg et al. 2009). Hence, reintro- predators to which they lack evolved defenses (Hoegh- duction and translocation programs can artificially select Guldberg et al. 2008). for individuals that are resistant or tolerant to a pathogen When species are unable to survive in their natural or herbivore or reintroduce or translocate the species habitat because of an introduced pathogen or herbivore, without selection. conservation efforts, such as captive breeding, are of- Given that resistance has a direct adverse effect on ten used to reduce the threat of extinction (Ebenhard pathogens and herbivores, but tolerance does not, re- 1995). The eventual introduction of captive-bred individ- sistance and tolerance can impose different selection uals to their natural habitat (Griffiths & Pavajeau 2008) pressures on pathogens and herbivores (Roy & Kirchner or their translocation to another area thought to be suffi- cient habitat (Hoegh-Guldberg et al. 2008) is an inherent element of captive breeding programs. Artificial selection in captive breeding programs is often an important tool because natural selection may not occur fast enough to protect hosts from rapid exposure to novel pathogens or herbivores. An unresolved question, however, is how to imple- ment a successful reintroduction or translocation pro- gram for species that cannot presently coexist with introduced pathogens or herbivores. In the disease and plant biology literature, strategies for coexisting with pathogens (here, pathogens include micro- and macroparasites) and herbivores are dichotomized into resistance and tolerance (e.g., Strauss & Agrawal 1999; Nunez-Farfan et al. 2007; Raberg et al. 2007). Resistance refers to defenses that reduce pathogen or herbivore bur- Figure 1. Comparison of the tolerance responses of den by either preventing infection or herbivory or di- individuals of 2 species or genotypes when exposed to rectly attacking the pathogen or herbivore (e.g., immune a pathogen or herbivore (slope of lines is tolerance). responses to pathogens, herbivore-deterring toxins); con- Fitness and pathogen or herbivore intensity increase sequently, resistance has a direct adverse effect on the on each axis from the origin. Individuals of the pathogen or herbivore. Resistance is typically measured species represented by the closed circles are less as the inverse of pathogen abundance or herbivory given tolerant than those represented by the open circles. Conservation Biology Volume 26, No. 4, 2012 588 Tolerance against Pathogens and Herbivores 2000) that may affect the success of reintroductions and cosis, so conservation strategies focus on management of translocations. For instance, to breed resistant individu- host populations. Captive breeding was explicitly rec- als, one selects for traits that provide countermeasures ommended in the International Union for Conservation (i.e., an action to oppose, neutralize, or retaliate against of Nature (IUCN) global amphibian action plan as a prior- some other action) to pathogens or herbivores. Given ity conservation initiative in response to the spatial and that pathogens and most herbivores (e.g., insects) have temporal spread of Bd epidemics (Gascon et al. 2007). shorter generation times than their hosts, host evolu- As a result of efforts by the IUCN Amphibian Ark tion would likely lag behind the countermeasures of the network and other conservation initiatives, hundreds of pathogens or herbivores. This evolutionary lag could re- threatened amphibian
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