Invasive Cyprinid Fish in Europe Originate from the Single Introduction of an Admixed Source Population Followed by a Complex Pattern of Spread

Andrea Simon,Filip A M Volckaert,Bernd Hänfling,Rodolphe Gozlan,Robert Britton,Cock Van Oosterhout,Dirk Steinke

doi:10.1371/journal.pone.0018560

Andrea Simon, Filip A M Volckaert + Show 5 more

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https://doi.org/10.1371/journal.pone.0018560

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Abstract

The Asian cyprinid fish, the topmouth gudgeon (Pseudorasbora parva), was introduced into Europe in the 1960s. A highly invasive freshwater fish, it is currently found in at least 32 countries outside its native range. Here we analyse a 700 base pair fragment of the mitochondrial cytochrome b gene to examine different models of colonisation and spread within the invasive range, and to investigate the factors that may have contributed to their invasion success. Haplotype and nucleotide diversity of the introduced populations from continental Europe was higher than that of the native populations, although two recently introduced populations from the British Isles showed low levels of variability. Based on coalescent theory, all introduced and some native populations showed a relative excess of nucleotide diversity compared to haplotype diversity. This suggests that these populations are not in mutation-drift equilibrium, but rather that the relative inflated level of nucleotide diversity is consistent with recent admixture. This study elucidates the colonisation patterns of P. parva in Europe and provides an evolutionary framework of their invasion. It supports the hypothesis that their European colonisation was initiated by their introduction to a single location or small geographic area with subsequent complex pattern of spread including both long distance and stepping-stone dispersal. Furthermore, it was preceded by, or associated with, the admixture of genetically diverse source populations that may have augmented its invasive-potential.

Highlights

Population genetic studies of invasive species have become an instrumental component in the study of biological invasions [1], [2], [3]
The aim was to test three non-mutually exclusive models that were proposed to explain the spread of P. parva in Europe: i) ‘multiple source-sink’ model where several independent introduction events from genetically differentiated native source populations to separate European locations would have occurred without involving admixture; ii) ‘stepping-stone’ model [19] where introduction into a single geographical area would have been followed by gradual expansion from the original introduction; and iii) ‘long-distance’ model [22] where introduction into a geographical area would have been followed by long-distance translocation within Europe
Full table of posterior distributions are given in the Appendix, Table S3. The outputs of these analyses revealed that i) there are three evolutionary lineages of the topmouth gudgeon (P. parva) in the native range, two of which contributed to the colonisation of Europe; ii) most invasive populations have a higher genetic diversity than their native counterparts and a higher genetic diversity than expected under equilibrium conditions; iii) most native populations have a low genetic diversity typical for riverine fishes, an exception being samples from the Hai He river system which showed very high levels of genetic diversity, which under equilibrium conditions predict extremely high effective population sizes; and iv) the differentiation among invasive populations is much lower than among native populations

Summary

Introduction

Population genetic studies of invasive species have become an instrumental component in the study of biological invasions [1], [2], [3]. Introductions of non-native species are often based on the release of a low number of founding propagules containing only a fraction of the genetic variation of the source populations [7]. Multiple introductions have resulted in high genetic diversity of invasive crustaceans [14], fish [3], [15], [16], lizards [17] and plants [18] It is currently unknown whether such admixture is merely a side-effect of the invasion process or is facilitating the establishment process. Additional population genetic case studies, in combination with studies on ecologically significant traits and genome wide associations are crucial in providing answers to this question

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