Population genetics reveals origin and number of founders in a biological invasion

Propagule pressure is considered the main determinant of success of biological invasions: when a large number of individuals are introduced into an area, the species is more likely to establish and become invasive. Nevertheless, precise data on propagule pressure exist only for a small sample of invasive species, usually voluntarily introduced. We studied the invasion of the American bullfrog, Rana catesbeiana, into Europe, a species that is considered a major cause of decline for native amphibians. For this major invader with scarce historical data, we used population genetics data (a partial sequence of the mitochondrial cytochrome b gene) to infer the invasion history and to estimate the number of founders of non‐native populations. Based on differences between populations, at least six independent introductions from the native range occurred in Europe, followed by secondary translocations. Genetic diversity was strongly reduced in non‐native populations, indicating a very strong bottleneck during colonization. We used simulations to estimate the precise number of founders and found that most non‐native populations derive from less than six females. This capability of invasion from a very small number of propagules challenges usual management strategies; species with such ability should be identified at an early stage of introduction.

[1]  G. Ficetola,et al.  Pattern of distribution of the American bullfrog Rana catesbeiana in Europe , 2007, Biological Invasions.

[2]  Wilfried Thuiller,et al.  Prediction and validation of the potential global distribution of a problematic alien invasive species — the American bullfrog , 2007 .

[3]  G. Ficetola,et al.  Genetic diversity, but not hatching success, is jointly affected by postglacial colonization and isolation in the threatened frog, Rana latastei , 2007, Molecular ecology.

[4]  J. Molofsky,et al.  Increased genetic variation and evolutionary potential drive the success of an invasive grass , 2007, Proceedings of the National Academy of Sciences.

[5]  M. Milinkovitch,et al.  Estimating population parameters using the structured serial coalescent with Bayesian MCMC inference when some demes are hidden. , 2007 .

[6]  D. Richardson,et al.  Residence time and potential range: crucial considerations in modelling plant invasions , 2007 .

[7]  S. Chown,et al.  A Global Indicator for Biological Invasion , 2006, Conservation biology : the journal of the Society for Conservation Biology.

[8]  M. Pace,et al.  Understanding the long-term effects of species invasions. , 2006, Trends in ecology & evolution.

[9]  D. Simberloff,et al.  Genetic divergence in the small Indian mongoose (Herpestes auropunctatus), a widely distributed invasive species , 2006, Molecular ecology.

[10]  P. Hulme Beyond control : wider implications for the management of biological invasions , 2006 .

[11]  M. Fisher,et al.  The emerging amphibian pathogen Batrachochytrium dendrobatidis globally infects introduced populations of the North American bullfrog, Rana catesbeiana , 2006, Biology Letters.

[12]  D. Strayer,et al.  Determinants of vertebrate invasion success in Europe and North America , 2006 .

[13]  V. E. Panov,et al.  Molecular ecology of zebra mussel invasions , 2006, Molecular ecology.

[14]  S. Wilson,et al.  Is management of an invasive grass Agropyron cristatum contingent on environmental variation , 2006 .

[15]  H. MacIsaac,et al.  Propagule pressure: a null model for biological invasions , 2006, Biological Invasions.

[16]  D. Simberloff,et al.  ECOLOGICAL RESISTANCE TO BIOLOGICAL INVASION OVERWHELMED BY PROPAGULE PRESSURE , 2005 .

[17]  R. Altwegg,et al.  MATRIX MODEL INVESTIGATION OF INVASIVE SPECIES CONTROL: BULLFROGS ON VANCOUVER ISLAND , 2005 .

[18]  P. S. Ward,et al.  The role of opportunity in the unintentional introduction of nonnative ants. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[19]  D. Post,et al.  Studying invasion: have we missed the boat? , 2005 .

[20]  T. Blackburn,et al.  The role of propagule pressure in explaining species invasions. , 2005, Trends in ecology & evolution.

[21]  Boris Worm,et al.  Ecosystem recovery after climatic extremes enhanced by genotypic diversity. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[22]  S. Schneider,et al.  Arlequin (version 3.0): An integrated software package for population genetics data analysis , 2005, Evolutionary bioinformatics online.

[23]  D. Sol,et al.  Global patterns of introduction effort and establishment success in birds , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[24]  J. Losos,et al.  Genetic variation increases during biological invasion by a Cuban lizard , 2004, Nature.

[25]  P. Boag,et al.  Discordant temporal and geographic patterns in maternal lineages of eastern North American frogs, Rana catesbeiana (Ranidae) and Pseudacris crucifer (Hylidae). , 2004, Molecular phylogenetics and evolution.

[26]  J. Briskie,et al.  Hatching failure increases with severity of population bottlenecks in birds. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[27]  T. Schmitt,et al.  The genetic pattern of population threat and loss: a case study of butterflies , 2004, Molecular ecology.

[28]  L. Kats,et al.  Alien predators and amphibian declines: review of two decades of science and the transition to conservation , 2003 .

[29]  D. H. Reed,et al.  Correlation between Fitness and Genetic Diversity , 2003 .

[30]  J. Vonesh,et al.  Complex life cycles and density dependence: assessing the contribution of egg mortality to amphibian declines , 2002, Oecologia.

[31]  Allan E. Strand,et al.  metasim 1.0: an individual-based environment for simulating population genetics of complex population dynamics , 2002 .

[32]  C. Lee Evolutionary genetics of invasive species , 2002 .

[33]  J. Kiesecker,et al.  Complexity in conservation: lessons from the global decline of amphibian populations , 2002 .

[34]  J. Cornuet,et al.  Inferring population history from microsatellite and enzyme data in serially introduced cane toads, Bufo marinus. , 2001, Genetics.

[35]  P. Hedrick,et al.  Purging of inbreeding depression and fitness decline in bottlenecked populations of Drosophila melanogaster , 2001 .

[36]  D. Forsyth,et al.  Propagule Size and the Relative Success of Exotic Ungulate and Bird Introductions to New Zealand , 2001, The American Naturalist.

[37]  C. Kolar,et al.  Progress in invasion biology: predicting invaders. , 2001, Trends in ecology & evolution.

[38]  K. Crandall,et al.  TCS: a computer program to estimate gene genealogies , 2000, Molecular ecology.

[39]  J. Wang Effects of population structures and selection strategies on the purging of inbreeding depression due to deleterious mutations. , 2000, Genetical research.

[40]  M. Soulé,et al.  Lag times in population explosions of invasive species: causes and implications , 1999 .

[41]  B. Grant,et al.  How large was the founding population of Darwin's finches? , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[42]  S. O’Brien,et al.  Elephant seal genetic variation and the use of simulation models to investigate historical population bottlenecks. , 1993, The Journal of heredity.

[43]  L. Excoffier,et al.  Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. , 1992, Genetics.

[44]  J. Stewart Introductions as Factors in Diseases of Fish and Aquatic Invertebrates , 1991 .

[45]  G. Caughley,et al.  Analysis of vertebrate populations , 1977 .

[46]  T. S. Baskett,et al.  Age Estimation, Growth Rates, and Population Structure in Missouri Bullfrogs , 1968 .

[47]  Mathieu Detaint,et al.  La Grenouille taureau Rana catesbeiana dans le sud-ouest de la France. Premiers résultats du programme de lutte , 2006 .

[48]  J. Memmott,et al.  The effect of propagule size on the invasion of an alien insect , 2005 .

[49]  Harold A. Mooney,et al.  Ecology of invasive plants: state of the art. , 2005 .

[50]  S. Lowe,et al.  100 of the world's worst invasive alien species. A selection from the global invasive species database , 2004 .

[51]  Åsa Berggren,et al.  COLONIZATION SUCCESS IN ROESEL'S BUSH-CRICKET METRIOPTERA ROESELI : THE EFFECTS OF PROPAGULE SIZE , 2001 .

[52]  Issg 100 of the World’s Worst Invasive Alien Species: A Selection From The Global Invasive Species Database , 2000 .

[53]  L. Durham AGE, GROWTH, AND HOMING IN THE BULLFROG' , 1963 .