Deciphering the Routes of invasion of Drosophila suzukii by Means of ABC Random Forest

Abstract Deciphering invasion routes from molecular data is crucial to understanding biological invasions, including identifying bottlenecks in population size and admixture among distinct populations. Here, we unravel the invasion routes of the invasive pest Drosophila suzukii using a multi-locus microsatellite dataset (25 loci on 23 worldwide sampling locations). To do this, we use approximate Bayesian computation (ABC), which has improved the reconstruction of invasion routes, but can be computationally expensive. We use our study to illustrate the use of a new, more efficient, ABC method, ABC random forest (ABC-RF) and compare it to a standard ABC method (ABC-LDA). We find that Japan emerges as the most probable source of the earliest recorded invasion into Hawaii. Southeast China and Hawaii together are the most probable sources of populations in western North America, which then in turn served as sources for those in eastern North America. European populations are genetically more homogeneous than North American populations, and their most probable source is northeast China, with evidence of limited gene flow from the eastern US as well. All introduced populations passed through bottlenecks, and analyses reveal five distinct admixture events. These findings can inform hypotheses concerning how this species evolved between different and independent source and invasive populations. Methodological comparisons indicate that ABC-RF and ABC-LDA show concordant results if ABC-LDA is based on a large number of simulated datasets but that ABC-RF out-performs ABC-LDA when using a comparable and more manageable number of simulated datasets, especially when analyzing complex introduction scenarios.

[1]  A. Estoup,et al.  Is There a Genetic Paradox of Biological Invasion , 2016 .

[2]  Simon C. Groen,et al.  Using Drosophila to study the evolution of herbivory and diet specialization. , 2016, Current opinion in insect science.

[3]  Jean-Marie Cornuet,et al.  ABC model choice via random forests , 2014, 1406.6288.

[4]  A. Loiseau,et al.  new set of microsatellite markers for the spotted-wing Drosophila suzukii (diptera: drosophilidae): a promising molecular tool for inferring the invasion history of this major insect pest , 2015 .

[5]  M. Gautier Genome-Wide Scan for Adaptive Divergence and Association with Population-Specific Covariates , 2015, Genetics.

[6]  R. Isaacs,et al.  Invasion biology of spotted wing Drosophila (Drosophila suzukii): a global perspective and future priorities , 2015, Journal of Pest Science.

[7]  M. Cristescu Genetic reconstructions of invasion history , 2015, Molecular ecology.

[8]  Dan G. Bock,et al.  What we still don't know about invasion genetics , 2015, Molecular ecology.

[9]  Samantha R Anderson,et al.  The devil is in the details: genetic variation in introduced populations and its contributions to invasion , 2015, Molecular ecology.

[10]  S. Hoban,et al.  Using ABC and microsatellite data to detect multiple introductions of invasive species from a single source , 2015, Heredity.

[11]  F. Zalom,et al.  Comparative Developmental Times and Laboratory Life Tables for Drosophlia suzukii and Drosophila melanogaster (Diptera: Drosophilidae) , 2014 .

[12]  Arnaud Estoup,et al.  Complementarity of statistical treatments to reconstruct worldwide routes of invasion: the case of the Asian ladybird Harmonia axyridis , 2014, Molecular ecology.

[13]  Laurent Excoffier,et al.  Expansion load: recessive mutations and the role of standing genetic variation , 2014, bioRxiv.

[14]  Timothy B Sackton,et al.  Drosophila suzukii: The Genetic Footprint of a Recent, Worldwide Invasion , 2014, Molecular biology and evolution.

[15]  A. Estoup,et al.  Invasion genetics of a human commensal rodent: the black rat Rattus rattus in Madagascar , 2014, Molecular ecology.

[16]  Maríndia Deprá,et al.  The first records of the invasive pest Drosophila suzukii in the South American continent , 2014, Journal of Pest Science.

[17]  A. Kopp,et al.  The making of a pest: the evolution of a fruit-penetrating ovipositor in Drosophila suzukii and related species , 2014, Proceedings of the Royal Society B: Biological Sciences.

[18]  Jean-Marie Cornuet,et al.  DIYABC v2.0: a software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data , 2014, Bioinform..

[19]  J. Darling,et al.  How important is intraspecific genetic admixture to the success of colonising populations? , 2014, Trends in ecology & evolution.

[20]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[21]  Gregory A. Wray,et al.  Genomics and the Evolution of Phenotypic Traits , 2013 .

[22]  Ernest K. Lee,et al.  Genome of Drosophila suzukii, the Spotted Wing Drosophila , 2013, G3: Genes, Genomes, Genetics.

[23]  P. Fontana,et al.  Linking Genomics and Ecology to Investigate the Complex Evolution of an Invasive Drosophila Pest , 2013, Genome biology and evolution.

[24]  S. Sisson,et al.  A comparative review of dimension reduction methods in approximate Bayesian computation , 2012, 1202.3819.

[25]  D. Simberloff Biological invasions: Much progress plus several controversies , 2013 .

[26]  P. Groot,et al.  Retracing the routes of introduction of invasive species: the case of the Sirex noctilio woodwasp , 2012, Molecular ecology.

[27]  Christian P Robert,et al.  Molecular Ecology Ressources – subject area: Methodological Advances 1 2 Estimation of demo-genetic model probabilities with Approximate Bayesian 3 Computation using linear discriminant analysis on summary statistics , 2012 .

[28]  M. Pascual,et al.  First records of the potential pest species Drosophila suzukii (Diptera: Drosophilidae) in Europe , 2012 .

[29]  A. Estoup,et al.  Anthropogenically induced adaptation to invade (AIAI): contemporary adaptation to human-altered habitats within the native range can promote invasions , 2011, Evolutionary applications.

[30]  T. Uller,et al.  Founder events predict changes in genetic diversity during human‐mediated range expansions , 2011 .

[31]  M. Hauser A historic account of the invasion of Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) in the continental United States, with remarks on their identification. , 2011, Pest management science.

[32]  Jana C. Lee,et al.  The susceptibility of small fruits and cherries to the spotted-wing drosophila, Drosophila suzukii. , 2011, Pest management science.

[33]  Christian P Robert,et al.  Lack of confidence in approximate Bayesian computation model choice , 2011, Proceedings of the National Academy of Sciences.

[34]  A. Estoup,et al.  Experimental evidence for the phenotypic impact of admixture between wild and biocontrol Asian ladybird (Harmonia axyridis) involved in the European invasion , 2011, Journal of evolutionary biology.

[35]  R. Plevin,et al.  Approximate Bayesian Computation in Evolution and Ecology , 2011 .

[36]  M. Beaumont Approximate Bayesian Computation in Evolution and Ecology , 2010 .

[37]  John K Kruschke,et al.  Bayesian data analysis. , 2010, Wiley interdisciplinary reviews. Cognitive science.

[38]  Arnaud Estoup,et al.  Reconstructing routes of invasion using genetic data: why, how and so what? , 2010, Molecular ecology.

[39]  D. R. Taylor,et al.  Genomic admixture increases fitness during a biological invasion , 2010, Journal of evolutionary biology.

[40]  Jean-Marie Cornuet,et al.  Inference on population history and model checking using DNA sequence and microsatellite data with the software DIYABC (v1.0) , 2010, BMC Bioinformatics.

[41]  G. Bertorelle,et al.  ABC as a flexible framework to estimate demography over space and time: some cons, many pros , 2010, Molecular ecology.

[42]  Jean-Marie Hombert,et al.  Origins and Genetic Diversity of Pygmy Hunter-Gatherers from Western Central Africa , 2009, Current Biology.

[43]  Jean-Marie Cornuet,et al.  Inferring population history with DIY ABC: a user-friendly approach to approximate Bayesian computation , 2008, Bioinform..

[44]  P. David,et al.  High Genetic Variance in Life-History Strategies within Invasive Populations by Way of Multiple Introductions , 2008, Current Biology.

[45]  Katrina M. Dlugosch,et al.  Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions , 2008, Molecular ecology.

[46]  R. Huey,et al.  Introduction history of Drosophila subobscura in the New World: a microsatellite‐based survey using ABC methods , 2007, Molecular ecology.

[47]  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.

[48]  Donald B. Rubin,et al.  Validation of Software for Bayesian Models Using Posterior Quantiles , 2006 .

[49]  K. Schierenbeck,et al.  Hybridization as a stimulus for the evolution of invasiveness in plants? , 2006, Euphytica.

[50]  P. David,et al.  A general eco-evolutionary framework for understanding bioinvasions. , 2006, Trends in ecology & evolution.

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

[52]  J. Cornuet,et al.  Estimating admixture proportions with microsatellites: comparison of methods based on simulated data , 2004, Molecular ecology.

[53]  R. Huey,et al.  A TIME SERIES OF EVOLUTION IN ACTION: A LATITUDINAL CLINE IN WING SIZE IN SOUTH AMERICAN DROSOPHILA SUBOBSCURA , 2004, Evolution; international journal of organic evolution.

[54]  Christopher A. Edmonds,et al.  Mutations arising in the wave front of an expanding population. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[55]  Leo Breiman,et al.  Random Forests , 2001, Machine Learning.

[56]  C. Hutter,et al.  Mutation and evolution of microsatellites in Drosophila melanogaster , 2004, Genetica.

[57]  R. Huey,et al.  Rapid evolution of wing size clines in Drosophila subobscura , 2004, Genetica.

[58]  D. Balding,et al.  Approximate Bayesian computation in population genetics. , 2002, Genetics.

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

[60]  Thomas Lenormand,et al.  Gene flow and the limits to natural selection , 2002 .

[61]  M. S. Hoddle,et al.  Population biology of invasive species. , 2001 .

[62]  R. C. Woodruff,et al.  Mutation and Evolution , 2012, Contemporary Issues in Genetics and Evolution.

[63]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[64]  Xiao-Li Meng,et al.  Posterior Predictive $p$-Values , 1994 .

[65]  B. Tabashnik,et al.  Gene flow accelerates local adaptation among finite populations: simulating the evolution of insecti , 1992 .

[66]  M. Nei,et al.  THE BOTTLENECK EFFECT AND GENETIC VARIABILITY IN POPULATIONS , 1975, Evolution; international journal of organic evolution.

[67]  S. Matsumura 6000 illustrated insects of Japan-Empire , 1931 .