Biol Invasions (2018) 20:2157–2171 https://doi.org/10.1007/s10530-018-1693-4 ORIGINAL PAPER Reconciling the biogeography of an invader through recent and historic genetic patterns: the case of topmouth gudgeon Pseudorasbora parva Emilie A. Hardouin . Demetra Andreou . Yahui Zhao . Pascale Chevret . David H. Fletcher . J. Robert Britton . Rodolphe E. Gozlan Received: 4 July 2017 / Accepted: 19 February 2018 / Published online: 28 February 2018 Ó The Author(s) 2018. This article is an open access publication Abstract The genetic variability and population China (100%), with a general split around the Qinling structure of introduced species in their native range Mountains. Dating of both haplogroups closely are potentially important determinants of their inva- matched past geological events. More recently, its sion success, yet data on native populations are often distribution has been influenced by fish movements in poorly represented in relevant studies. Consequently, aquaculture, resulting in gene flow between previously to determine the contribution of genetic structuring in separated populations in Northern and Southern the native range of topmouth gudgeon Pseudorasbora China. Their phylogeography in Europe indicate as parva to their high invasion success in Europe, we few as two introductions events and two dispersal used a dataset comprising of 19 native and 11 non- routes. Microsatellite data revealed native populations native populations. A total of 666 samples were had higher genetic diversity than those in the invasive analysed at 9 polymorphic microsatellite loci and range, a contrast to previous studies on P. parva.This sequenced for 597 bp of mitochondrial DNA. The study confirms the importance of extensive sampling analysis revealed three distinct lineages in the native in both the native and non-native range of invasive range, of which two haplogroups were prevalent in species in evaluating the influence of genetic variabil- ity on invasion success. Emilie A. Hardouin and Demetra Andreou have contributed Keywords Pseudorabora parva Á Invasive species Á equally. Non-native Á Invasion genetics Á Biological invasion Á Biogeography Electronic supplementary material The online version of this article (https://doi.org/10.1007/s10530-018-1693-4) con- tains supplementary material, which is available to authorized users. E. A. Hardouin (&) Á D. Andreou Á D. H. Fletcher Á P. Chevret ´ J. R. Britton Á R. E. Gozlan Laboratoire de Biometrie et Biologie Evolutive (UMR Department of Life and Environmental Sciences, Faculty CNRS 5558), Universite´ Claude Bernard Lyon, 1 Bat. of Sciences and Technology, Bournemouth University, Mendel, 43 bd du 11 Novembre 1918, Dorset BH12 5BB, UK 69622 Villeurbanne Cedex, France e-mail: [email protected] R. E. Gozlan Y. Zhao UMR BOREA IRD-MNHN-Universite´ Pierre et Marie Institute of Zoology, Chinese Academy of Sciences, Curie, Muse´um National d’Histoire Naturelle, 47 rue Chaoyang District, Beijing 100101, China Cuvier, 75231 Paris Cedex 5, France 123 2158 E. A. Hardouin et al. Introduction (Bermond et al. 2012; Biebach and Keller 2012; Chapple et al. 2013; Keller et al. 2014; Schulte et al. A central theme in evolutionary biology is to under- 2013). This can increase the level of heterozygosity in stand the processes of how species adapt to changing newly established populations and lead to increased environmental conditions (Bell and Gonzalez 2011; fitness through heterosis (Keller et al. 2014). Sampling Ghalambor et al. 2007). Although empirical studies biases, however, such as extensive sampling in the have confirmed some important theoretical predic- invasive range and under sampling in the native range, tions regarding how population size influences neutral often bias true estimates of genetic variability, genetic variation, it remains poorly understood how, phenotypic traits and behaviours, impeding accurate for example, initial small population sizes affect the comparisons across the two ranges (Diez-del-Molino long-term survival of populations (Hedge et al. 2014; et al. 2013; Sanz et al. 2013). Such issues are Hufbauer et al. 2013). Biological invasions are well particularly apparent in studies on freshwater fishes suited to addressing such fundamental questions since due to the inherent difficulties and expense of exten- they represent a natural translocation experiment over sive sampling programmes (Smith et al. 2014). Since multiple generations (Blanchet 2012; Vandepitte et al. each invaded river catchment potentially represents a 2014). Abiotic and biotic conditions often differ biogeographical island where populations may have between native and invaded environments, with the locally adapted following separation and isolation introduced species not sharing recent evolutionary through, for example, past geological events, it is history with species in the native community (Gallien important to have an extensive representation of et al. 2012). The colonisation of the new environment variability in the native range (DeFaveri et al. 2014; by the introduced species might be impeded by factors Wiens et al. 2014). including competition for food resources and the Small freshwater fishes are often accidentally unpredictable impacts of native parasites on new hosts introduced into new environments via contaminated (Kumschick et al. 2015), which can constrain its batches of other fishes used in angling or aquaculture ability to establish self-sustaining populations. Thus, if (Britton and Gozlan 2013; Davies et al. 2013) and so they are to be successful, invasive species must invasions of small-bodied freshwater fish are often respond quickly and efficiently to the selective regime strongly associated with aquaculture trade pathways imposed by the colonised ecosystem (Broennimann (Copp et al. 2010). The topmouth gudgeon Pseudo- and Guisan 2008). rasbora parva, a small cyprinid fish, is naturally Introductions of non-native species are often based distributed in eastern Asia. It was introduced into on the release of a low number of founding propagules Europe from China in the 1960s through a succession containing only a fraction of the genetic variation of of accidental introductions into the area around the the source populations (Hanfling 2007; Searle 2008). Black Sea when they contaminated batches of Chinese During this process, these populations often undergo a carp species being moved in aquaculture (Gozlan et al. succession of genetic bottlenecks, resulting in their 2010a; Gozlan 2011). It has now invaded at least 32 invasive populations having lower genetic diversity countries, including most of Europe, plus Turkey, Iran compared with populations in the native range (Bes- and North Africa, with their long-distance dispersal nard et al. 2014; Facon et al. 2011; Hardouin et al. also occurring via aquaculture trade routes (Gozlan 2010, 2015). Such reduced genetic diversity theoret- 2011). P. parva’s expansion is not, however, just ically limits a species’ ability to establish invasive limited to a non-Asian range, with their translocation populations, invoking a genetic paradox over how to numerous locations within China. The native range introduced species can successfully develop invasive of P. parva in China encompasses the Yangtzee River populations despite this low diversity (Hanfling 2007). around the Qinling Mountains. Human translocations This paradox of genetic diversity is often counter- have led to non-native P. parva populations in western acted by admixture among genetically divergent China, Tibet and Mongolia (Gozlan et al. 2010a, b). source populations upon their introduction (Roman The wide geographic range invaded by P. parva thus and Darling 2007; Rosenthal et al. 2008). For example, makes this a strong model species for understanding multiple introductions have resulted in high genetic invasion genetics. To date, the two studies that address diversity of invasive crustaceans, fish and lizards the genetic diversity of P. parva (Simon et al. 123 Biogeography of an invader through recent and historic genetic patterns 2159 2011, 2015) only included a very restricted sampling was identified as P. parva, measured and a tissue of their native range. In those studies, higher levels of biopsy (fin-clip) taken and stored in 95% ethanol. genetic variability in the introduced range were detected than in the native range, highlighting the Cytochrome b gene sequencing and analysis potential role of admixture in the invasive range in benefitting invasive vigour (Simon et al. 2011). DNA was extracted from the P. parva fin-clips using However, the samples from the native range used DNeasy extraction Kit (Qiagen). A total of 563 potentially biased these conclusions, constraining Cytochrome B gene sequences were amplified using understanding of their invasion history. Moreover, L15267 and H15891Ph primers (Briolay et al. 1998). placing greater emphasis on sampling in the native All reactions were carried out in a final volume of range, can reveal a more complete picture of the long- 10 lL. PCR cycling parameters were as follow: 95 °C term native biogeographic history of the species, for 15 min followed by 35 cycles of 95 °C for 30 s, including the role of geological events in shaping 60 °C for 1.30 min, 72 °C for 1 and 15 min at 70 °C genetic topology (i.e. lineages), which could have for the final elongation time. Exo-Sap purification influenced recent invasions (Diez-del-Molino et al. (USB Corp.) was performed with the following 2013). incubation: 37 °C for 30 min and 80 °C for 20 min. Given the