Phylogenetic Diversity of the Red Swamp Crayfish Procambarus clarkii and Its Dispersal Pattern in Northern and Central Italy

Simple Summary The red swamp crayfish Procambarus clarkii is one of the most threatening freshwater species in the world. Since 2016, it has been included in the Invasive Alien Species list of the European Union, and it is still actively colonizing new territories at the expense of native crayfish. The present study aimed to provide a genetic characterization for a better understanding of the invasion routes of this alien species in the Italian Peninsula. The analysis of the mitochondrial DNA of 153 P. clarkii samples collected from five Italian lakes and one river showed the presence of unique maternal lines in four of these basins, thus confirming the hypothesis of multiple introductions and strengthening the idea that knowledge of dispersion routes can be very useful to predict the invasiveness of this species and create control strategies to preserve biodiversity. Abstract The red swamp crayfish Procambarus clarkii is one of the most threatening freshwater species in the world. The aim of this study is to provide a better understanding of the phylogeography and the invasion routes of P. clarkii populations in the Italian Peninsula through the analysis of mitochondrial phylogeny. Mitochondrial control region and cytochrome c oxidase subunit I (COI) sequences of 153 samples collected from six Italian basins were analyzed and compared to worldwide data. Except for the lakes Bolsena and Posta Fibreno, a high genetic variability was found in the other basins. The mitochondrial DNA pattern of P. clarkii from the lakes Candia and Massaciuccoli confirmed the hypothesis of double introduction events. Another entry point could be represented by Lake Trasimeno, which shows haplotypes originating from Louisiana and not shared with other Italian basins. Moreover, unique lineages were also found in the Stella River, thus enhancing the hypothesis that multiple introductions of P. clarkii occurred in northern and Central Italy and strengthening the idea that knowledge about the dispersion routes of this alien species can be useful to predict its invasiveness and elaborate control strategies to preserve biodiversity.

[1]  E. Goretti,et al.  Sex and seasonal differences in metal accumulation of selected tissues in red swamp crayfish from Lake Trasimeno (Umbria, Italy) , 2022, Environmental Science and Pollution Research.

[2]  R. Bouckaert An Efficient Coalescent Epoch Model for Bayesian Phylogenetic Inference , 2021, bioRxiv.

[3]  H. Lancioni,et al.  Population Ecology and Genetic Diversity of the Invasive Alien Species Procambarus clarkii in Lake Trasimeno (Italy) , 2021, Biology.

[4]  G. Nie,et al.  Species diversity of freshwater shrimp in Henan Province, China, based on morphological characters and COI mitochondrial gene , 2021, Ecology and evolution.

[5]  R. Galarini,et al.  BFRs (PBDEs and HBCDs) in freshwater species from Lake Trasimeno (Italy): The singular case of HBCDs in red swamp crayfish. , 2020, The Science of the total environment.

[6]  M. Clavero,et al.  Historical, human, and environmental drivers of genetic diversity in the red swamp crayfish ( Procambarus clarkii ) invading the Iberian Peninsula , 2020, Freshwater Biology.

[7]  E. Goretti,et al.  Salinity tolerance of the invasive red swamp crayfish Procambarus clarkii (Girard, 1852) , 2020, Hydrobiologia.

[8]  A. Green,et al.  Unravelling the global invasion routes of a worldwide invader, the red swamp crayfish (Procambarus clarkii) , 2019, Freshwater Biology.

[9]  G. Haszprunar,et al.  Comparison of three DNA marker regions for identification of food relevant crustaceans of the order Decapoda , 2018, European Food Research and Technology.

[10]  O. Bronstein,et al.  Mind the gap! The mitochondrial control region and its power as a phylogenetic marker in echinoids , 2018, BMC Evolutionary Biology.

[11]  M. Almerão,et al.  Genetic diversity of the invasive crayfish Procambarus clarkii in France , 2018 .

[12]  E. Goretti,et al.  Resistance to dehydration and positive hygrotaxis in the invasive red swamp crayfish Procambarus clarkii , 2018 .

[13]  E. Ladoukakis,et al.  Evolution and inheritance of animal mitochondrial DNA: rules and exceptions , 2017, Journal of Biological Research-Thessaloniki.

[14]  H. Jacquemyn,et al.  Transatlantic invasion routes and adaptive potential in North American populations of the invasive glossy buckthorn, Frangula alnus. , 2016, Annals of botany.

[15]  Senhao Jiang,et al.  Characterization of the complete mitochondrial genome of the red crayfish, Procambarus clarkii (Decapoda: Cambaridae) , 2016, Mitochondrial DNA. Part A, DNA mapping, sequencing, and analysis.

[16]  R. Butlin,et al.  Contrasting patterns of genetic diversity and spatial structure in an invasive symbiont-host association , 2016, Biological Invasions.

[17]  Shunping He,et al.  DNA barcoding for the identification of common economic aquatic products in Central China and its application for the supervision of the market trade , 2016 .

[18]  A. Radulovici,et al.  Looking back on a decade of barcoding crustaceans , 2015, ZooKeys.

[19]  Weimin Wang,et al.  Inferring Invasion History of Red Swamp Crayfish (Procambarus clarkii) in China from Mitochondrial Control Region and Nuclear Intron Sequences , 2015, International journal of molecular sciences.

[20]  P. Anastácio,et al.  Red swamp crayfish: biology, ecology and invasion - an overview , 2015 .

[21]  R. Wayne,et al.  Origins of the invasive red swamp crayfish (Procambarus clarkii) in the Santa Monica Mountains. , 2014 .

[22]  Wolfgang Nentwig,et al.  A Unified Classification of Alien Species Based on the Magnitude of their Environmental Impacts , 2014, PLoS biology.

[23]  M. Valvo,et al.  A new record of the Red swamp crayfish, Procambarus clarkii (Girard, 1852) (Crustacea Cambaridae), in Sicily, Italy , 2014 .

[24]  Andrew P. Martin,et al.  Discerning invasion history in an ephemerally connected system: landscape genetics of Procambarus clarkii in Ash Meadows, Nevada , 2014, Biological Invasions.

[25]  Gang Liu,et al.  Population Genetic Structure of the Invasive Red Swamp Crayfish in China Revealed by ITS1 Variation , 2013, Biochemical Genetics.

[26]  W. Luo,et al.  Population Genetic Structure and Post-Establishment Dispersal Patterns of the Red Swamp Crayfish Procambarus Clarkii in China , 2012, PloS one.

[27]  Sanghee Kim,et al.  The mitochondrial genomes of Cambaroides similis and Procambarus clarkii (Decapoda: Astacidea: Cambaridae): the phylogenetic implications for Reptantia , 2012 .

[28]  M. D’Amen,et al.  A model of co-occurrence: segregation and aggregation patterns in the mycoflora of the crayfish Procambarus clarkii in Lake Trasimeno (central Italy) , 2012 .

[29]  F. Alvarez,et al.  Genetic variation in native and introduced populations of the red swamp crayfish Procambarus clarkii (Girard, 1852) (Crustacea, Decapoda, Cambaridae) in Mexico and Costa Rica. , 2012 .

[30]  M. Scalici,et al.  Phoma glomerata, a potential new threat to Italian inland waters , 2011 .

[31]  F. Gherardi,et al.  Invasive alien Crustacea: dispersal, establishment, impact and control , 2011, BioControl.

[32]  L. Filipová,et al.  Identification of exotic North American crayfish in Europe by DNA barcoding , 2011 .

[33]  M. Vilà,et al.  How well do we understand the impacts of alien species on ecosystem services? A pan-European, cross-taxa assessment , 2010 .

[34]  F. Gherardi,et al.  Structure and dynamics of an invasive population of the red swamp crayfish (Procambarus clarkii) in a Mediterranean wetland , 2007, Hydrobiologia.

[35]  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.

[36]  F. Gherardi,et al.  Genetics and invasion biology in fresh waters: a pilot study of Procambarus clarkii in Europe , 2007 .

[37]  G. Scholtz,et al.  The phylogenetic position of the East Asian freshwater crayfish Cambaroides within the Northern Hemisphere Astacoidea (Crustacea, Decapoda, Astacida) based on molecular data , 2006 .

[38]  R. Fani,et al.  Genetic Variability in European Populations of an Invasive American Crayfish: Preliminary Results , 2003, Biological Invasions.

[39]  H. Ackefors The positive effects of established crayfish introductions in Europe , 1999 .

[40]  R. Vrijenhoek,et al.  DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. , 1994, Molecular marine biology and biotechnology.

[41]  D. Holdich,et al.  Freshwater crayfish :: biology, management and exploitation , 1988 .

[42]  W. H. Clark,et al.  First Record of the Crayfish, Procambarus Clarkii, From Idaho, U.S.a. (Decapoda, Cambaridae) , 1978 .