Hybrid vigor between native and introduced salamanders raises new challenges for conservation. Proc Natl Acad Sci USA

Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN 37996, USA.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 11/2007; 104(40):15793-8. DOI: 10.1073/pnas.0704791104
Source: PubMed


Hybridization between differentiated lineages can have many different consequences depending on fitness variation among hybrid offspring. When introduced organisms hybridize with natives, the ensuing evolutionary dynamics may substantially complicate conservation decisions. Understanding the fitness consequences of hybridization is an important first step in predicting its evolutionary outcome and conservation impact. Here, we measured natural selection caused by differential viability of hybrid larvae in wild populations where native California Tiger Salamanders (Ambystoma californiense) and introduced Barred Tiger Salamanders (Ambystoma tigrinum mavortium) have been hybridizing for 50-60 years. We found strong evidence of hybrid vigor; mixed-ancestry genotypes had higher survival rates than genotypes containing mostly native or mostly introduced alleles. Hybrid vigor may be caused by heterozygote advantage (overdominance) or recombinant hybrid vigor (due to epistasis or complementation). These genetic mechanisms are not mutually exclusive, and we find statistical support for both overdominant and recombinant contributions to hybrid vigor in larval tiger salamanders. Because recombinant homozygous genotypes can breed true, a single highly fit genotype with a mosaic of native and introduced alleles may eventually replace the historically pure California Tiger Salamander (listed as Threatened under the U.S. Endangered Species Act). The management implications of this outcome are complex: Genetically pure populations may not persist into the future, but average fitness and population viability of admixed California Tiger Salamanders may be enhanced. The ecological consequences for other native species are unknown.

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    • "Hybridization with the invasive BTS is among the greatest threats facing CTS. Hybrid animals are more robust and have increased survival rates compared to pure native CTS, leading to concerns that hybrids will be strongly favoured by natural selection and replace pure CTS (Fitzpatrick & Shaffer 2007b; Ryan et al. 2012). Additionally, the presence of CTS/BTS hybrids has been found to negatively impact other amphibians breeding in the same ponds (Ryan et al. 2009; Searcy et al. 2015). "
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    ABSTRACT: Molecular ecology has become one of the key tools in the modern conservationist's kit. Here we review three areas where molecular ecology has been applied to amphibian conservation: genes on landscapes, within-population processes, and genes that matter. We summarize relevant analytical methods, recent important papers from the amphibian literature, and conservation implications for each section. Finally, we include five in-depth examples of how molecular ecology has been successfully applied to specific amphibian systems. This article is protected by copyright. All rights reserved.
    Molecular Ecology 10/2015; 24(20). DOI:10.1111/mec.13391 · 6.49 Impact Factor
    • "Hybrids might increase ecosystem resilience to environmental stressors if they can colonize extreme or novel habitats (Gross & Rieseberg 2005; Parmesan 2006). Further , despite the potential risks hybrids pose to the survival of rare species, they may act as source populations for genetic restoration (Allendorf et al. 2004; Fitzpatrick & Shaffer 2007; Ellstrand et al. 2010). "
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    ABSTRACT: Species hybrids have long been undervalued in conservation and are often perceived as a threat to pure species. Recently, the conservation value of hybrids, especially those of natural origin, has gained recognition; however, hybrid conservation remains controversial. We reviewed hybrid management policies, including laws, regulations, and management protocols, from a variety of organizations, primarily in Canada and the United States. We found that many policies are based on limited ethical and ecological considerations and provide little opportunity for hybrid conservation. In most policies, hybrids are either unrepresented or considered a threat to conservation goals. This is problematic because our review of the hybrid conservation literature identified many ethical and ecological considerations relevant to determining the conservation value of a hybrid, all of which are management-context specific. We also noted a lack of discussion of the ethical considerations regarding hybrid conservation. Based on these findings, we created a policy framework outlining situations in which hybrids could be eligible for conservation in Canada and the United States. The framework comprises a decision tree that helps users determine whether a hybrid should be eligible for conservation based on multiple ecological and ethical considerations. The framework may be applied to any hybrid and is flexible in that it accommodates context-specific management by allowing different options if a hybrid is a threat to or could benefit conservation goals. The framework can inform policy makers and conservationists in decision-making processes regarding hybrid conservation by providing a systematic set of decision criteria and guidance on additional criteria to be considered in cases of uncertainty, and it fills a policy gap that limits current hybrid management. © 2015 Society for Conservation Biology.
    Conservation Biology 05/2015; Early View Online. DOI:10.1111/cobi.12526 · 4.17 Impact Factor
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    • "Follow-up studies are needed to test the stability of the hybrid zone. Nevertheless, even a stable hybrid zone would provide a window for genetic pollution via introgressive hybridization (Fitzpatrick and Shaffer, 2007). "
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    ABSTRACT: Genetic pollution of a native species through hybridization with an invasive species poses an insidious conservation threat. To expose genetic pollution, molecular methods employing multilocus data are required. We present a case study of genetic pollution via hybridization of a native crested newt species, Triturus cristatus, by the invasive Triturus carnifex on the Veluwe in the Netherlands. We sequenced 50 nuclear markers by next generation sequencing and one mitochondrial marker by Sanger sequencing for four populations from the native range of both parent species and eleven ponds on the Veluwe. We use three population genetic approaches (HIest, BAPS and Structure) to determine the genetic composition of the Veluwe newts based on all nuclear markers, a subset of 18 diagnostic markers and the complementary 32 non-diagnostic markers, with and without parental populations. BAPS underestimates genetic pollution, whereas Structure is comparatively accurate compared to HIest, although Structure’s relative advantage decreases with the diagnosticity of the markers. Data simulation confirms these findings. Genetic composition of the Veluwe ponds ranges from completely native, via different degrees of genetic admixture, to completely invasive. The observed hybrid zone appears to be bimodal, suggesting negative selection against hybrids. A genetic footprint of the native species is present in invasive populations, evidencing that the invasive locally replaced the native species. Genetic pollution is currently confined to a small area, but the possibility of further expansion cannot be excluded. Removal of genetic pollution will not be easy. We emphasize the need for legal guidance to manage genetic pollution.
    Biological Conservation 04/2015; 184:145-153. · 3.76 Impact Factor
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