Grantee Research Project Results
Final Report: Hybridization Between an Invasive Exotic and a Declining Native Amphibian: Molecular Characterization, Ecological Dynamics, and Genetic Remediation
EPA Grant Number: R828896Title: Hybridization Between an Invasive Exotic and a Declining Native Amphibian: Molecular Characterization, Ecological Dynamics, and Genetic Remediation
Investigators: Shaffer, Howard B. , Koenig, Walter D. , Voss, S. Randal , Fitzpatrick, Benjamin
Institution: University of California - Davis , University of Kentucky , University of California - Berkeley
Current Institution: University of California - Davis , University of California - Berkeley , University of Kentucky
EPA Project Officer: Packard, Benjamin H
Project Period: August 20, 2001 through August 19, 2004 (Extended to August 31, 2005)
Project Amount: $433,708
RFA: Exploratory Research to Anticipate Future Environmental Issues (2000) RFA Text | Recipients Lists
Research Category: Ecological Indicators/Assessment/Restoration , Water , Aquatic Ecosystems
Objective:
In this project, we conducted a detailed set of analyses of a unique problem in genetic biopollution—the invasion of a native species by genes of a nonnative hybridizing species. In this case, the native species is the California tiger salamander, Ambystoma californiense, whereas the nonnative invasive is the barred tiger salamander, A. tigrinum mavortium. These two species are superficially similar, but they vary in terms of color pattern, life history, morphology, and DNA sequences. Because the California tiger salamander is listed under the U.S. Endangered Species Act, understanding the invasion biology of nonnative genes has proved to be an important aspect of managing this threat to a highly endangered, fragile species.
The objectives of this research project were to: (1) quantify the extent of genetic invasion by this exotic species, (2) develop a full set of informative molecular markers that would allow us to identify and track the spread of nonnative genes, and (3) conduct detailed genetic and demographic analyses to identify the extent of genetic biopollution and reduce introduced exotic genes. This work provides the first complete assessment of the genetic biopollution risk involved for this species. Our reasoning has been, and continues to be, that by better understanding the ecological context in which successful invasions occur, we will be better able to control this important biological invasion.
Our approach has been to: (1) develop a panel of 10-20 mapped nuclear markers to quantify the extent of hybrid invasion at any point in time, (2) use these markers to determine the geographic extent of hybrid introgression and the concordance of introgression across genes, (3) collect key demographic information in the field and laboratory to quantify differences among pure and hybrid salamanders, and (4) test multiple ponds and genes to investigate the correlation of hybrid success with ecological pond characteristics. Our ultimate goal was to then conduct experiments to investigate how our results may be used to reduce or eliminate introduced exotic genotypes from this system.
Overall, we believe that we have accomplished all of the original goals of our work. Some of our results are now published, and we are working on writing up the rest. Below, we briefly summarize the high points of our work.
Summary/Accomplishments (Outputs/Outcomes):
Developing Genetic Tools
We developed 10 fully functional molecular markers that allow us to determine whether an individual is homozygous native, heterozygous, or homozygous nonnative at a particular marker. We implemented a strict quality assurance protocol requiring genotyping of 30 pure A. californiense and pure A. tigrinum systematically sampled from throughout their native ranges prior to declaring a molecular marker diagnostic. Because we have so many markers, we now are able to examine how specific gene regions perform with respect to natural selection and fitness in the field. That is, we can go beyond assessing the performance of individuals that are hybrid and instead ask how their native or nonnative genes at a variety of locations in their genome affect fitness. We have used these markers to ask two fundamental questions during this project: what is the geographical extent of hybrid invasion on the California landscape, and what is the performance of hybrid, compared to nonhybrid, individuals in the field.
Geographic Distribution of Hybrids
Our analysis of geography has just been accepted for publication in Ecological Applications, one of the premier journals in our field. In this study we used the eight 100 percent diagnostic ancestry-informative markers (AIMs) to evaluate the movement of genes on landscapes and the concordance of introgression across regions of genome. One very important result was that the AIMs were highly concordant geographically, indicating that we could use fewer markers to reliably estimate introduced allele frequencies across a larger number of sampling sites. Although a very low level of introgression could be detected as far as 60 km north of the Salinas Valley, the distribution of introduced alleles was restricted almost entirely to the Salinas Valley, within 12 km of known introduction sites. Further, the transition from highly invaded ponds to nearly pure native ponds was quite abrupt, dropping from about 70 percent to less than 1 percent over a distance less than 3 km. These observations lead us to conclude that the worst of the bioinvasion of nonnative genes is restricted to the Salinas Valley (Monterey County), and that populations outside of the Salinas Valley should remain fully protected under the Endangered Species Act.
Hybrid Performance
This can be measured in a number of ways, and we have employed a series of field and laboratory studies to examine this in some detail. From a demographic perspective, we have shown that A. californiense and A. tigrinum differ in how many eggs they lay (nonnative A. tigrinum lay many more) and in egg size (A. californiense lay fewer, bigger eggs). Hybrids are similar to A. tigrinum, and they are producing nearly twice as many eggs as native individuals. Nonnative salamanders also reach sexual maturity much faster (1-2 years) than do native California tiger salamanders (4-5 years in the field), with hybrids showing intermediate values. Earlier reproduction and production of a larger number of relatively small eggs are life history characteristics commonly associated with invasive species and the colonization of disturbed habitats followed by rapid population growth. These observations suggest that introduced A. tigrinum and hybrids sharing their life history characteristics might be favored by human land use practices that involve frequent construction of new ponds and destruction of old ones in addition to disturbance of the upland habitat.
Habitat Dependence of the Tiger Salamander Invasion
This work was published in 2004. We studied 12 ponds, including four natural vernal pools, four seasonal man-made cattle ponds, and four perennial man-made ponds. The first two pond types fill with water during the winter rainy season and dry up early each summer. In contrast, perennial ponds usually hold water throughout the year. Our most exciting and important result was that perennial ponds had significantly higher frequencies of introduced alleles than seasonal ponds, suggesting that nonnative genes thrive in human-modified ponds. Although we do not know what drives this result, we have expanded it to include some 85 ponds and still find that it holds up under close statistical scrutiny. Our current hypotheses, which we are testing with additional studies, are that a combination of life history differences and locomotor performance may explain the improved survivorship of nonnative genes in modified habitats. Even without a strong explanation for this trend, however, it suggests that trying to manage ponds to have ecological conditions similar to those in natural vernal pools may be an effective way to reduce the frequency of nonnative genes on the California landscape.
Hybrid Vigor
Finally, we used population sampling and genetic analysis to ask whether native, nonnative, or hybrid salamanders differentially survive during a single season. We estimated survival in the wild by comparing genotype frequencies in samples of hatchlings versus surviving larvae (~ 1-2 months after hatching) in five ponds. Surprisingly, larvae with intermediate ancestry had higher survival in every pond. This result suggests that it may be very difficult to completely eliminate nonnative genes, even in very naturalistic ponds. Some genes, or gene combinations, simply seem to do best when there are mixtures of native and nonnative genes, and natural selection may continue to favor those combinations. With funding from the National Science Foundation, we are continuing to explore exactly why some gene combinations seem to do so well and strategies to eliminate them in the future.
The Future
As we continue to refine our understanding of this system, we also are working with the U.S. Fish and Wildlife Service, the California Department of Fish and Game, Caltrans, and other agencies to help determine how to best protect California tiger salamanders and reduce the threat to their integrity caused by nonnative genes. We are heartened by our observations that nonnative genes still are geographically restricted to the Salinas Valley, and we look forward to continue collecting demographic and ecological data that will allow us to hold back, and potentially reverse, this important biological invasion.
Journal Articles on this Report : 2 Displayed | Download in RIS Format
Other project views: | All 13 publications | 5 publications in selected types | All 5 journal articles |
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Type | Citation | ||
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Fitzpatrick B, JOhnson J, Kump D, Shaffer H, Smith J, Voss S. Rapid fixation of non-native alleles revealed by genome-wide SNP analysis of hybrid tiger salamanders. BMC EVOLUTIONARY BIOLOGY 2009;9(176) |
R828896 (Final) |
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Fitzpatrick B, Johnson J, Kump D, Shaffer H. Rapid spread of invasive genes into a threatened native species. BIOLOGICAL SCIENCES 2010;107(8):3606-3610 |
R828896 (Final) |
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Supplemental Keywords:
ecological effects, sensitive populations, genetic polymorphisms, aquatic ecosystems, restoration, conservation, ecology, genetics, surveys, exploratory research environmental biology, genetic susceptibility, California, CA, amphibian, animal models, biodiversity, biopollution, conservation, demographic analyses, ecological dynamics, ecological effects, endangered species, environmental hazard exposures, exotic genotypes, exotic species, extinction risk, futures research, genetic predisposition, genetic remediation, hybridization, interbreeding, invasive species,, RFA, Scientific Discipline, Health, Geographic Area, Ecosystem Protection/Environmental Exposure & Risk, Genetics, Ecosystem/Assessment/Indicators, exploratory research environmental biology, State, Environmental Microbiology, Ecological Effects - Environmental Exposure & Risk, Susceptibility/Sensitive Population/Genetic Susceptibility, Monitoring/Modeling, Ecological Risk Assessment, genetic susceptability, Biology, Futures, Exp. Research/future, Ecological Indicators, extinction risk, ecological effects, biodiversity, endangered species, biopollution, molecular characterization, genetic predisposition, conservation, amphibian, animal models, exotic genotypes, genetic remediation, invasive species, ecological dynamics, demographic analyses, California (CA), hybridization, futures research, interbreeding, exotic speciesProgress and Final Reports:
Original AbstractThe perspectives, information and conclusions conveyed in research project abstracts, progress reports, final reports, journal abstracts and journal publications convey the viewpoints of the principal investigator and may not represent the views and policies of ORD and EPA. Conclusions drawn by the principal investigators have not been reviewed by the Agency.