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Invasive cyprinid fish in Europe originate from the single introduction of an admixed source population followed by a complex pattern of spread.

Simon A, Britton R, Gozlan R, van Oosterhout C, Volckaert FA, Hänfling B - PLoS ONE (2011)

Bottom Line: A highly invasive freshwater fish, it is currently found in at least 32 countries outside its native range.Based on coalescent theory, all introduced and some native populations showed a relative excess of nucleotide diversity compared to haplotype diversity.Furthermore, it was preceded by, or associated with, the admixture of genetically diverse source populations that may have augmented its invasive-potential.

View Article: PubMed Central - PubMed

Affiliation: Evolutionary Biology Group, Department of Biological Sciences, University of Hull, Hull, United Kingdom. a.simon@2007.hull.ac.uk

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.

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Phylogenetic relationship of haplotypes based on NJ analysis.First value on branches indicate ML support value, second value indicate non-parametric bootstrapping of the NJ-tree. Values are only given for support values >70%.
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pone-0018560-g003: Phylogenetic relationship of haplotypes based on NJ analysis.First value on branches indicate ML support value, second value indicate non-parametric bootstrapping of the NJ-tree. Values are only given for support values >70%.

Mentions: A total of 30 haplotypes were identified using 310 sequences from 8 native and 14 introduced populations (Table 1). The phylogenetic relationship among haplotypes is shown in Figure 3. Both NJ and ML methods yielded the same topology, hence only the NJ tree is displayed but ML support values were added to tree nodes. The two Japanese haplotypes, H23 and H24 were closely related to each other and the phylogenetic analysis (Figure 3) showed that they formed a highly divergent sister group to the remaining P. parva haplotypes (sequences divergence ∼5–6%). One highly divergent haplotype found in the invasive Polish populations clustered closely to a sequence of G. gobio. This haplotype and the Japanese haplotypes were therefore not included in the network analysis. Thirteen haplotypes were found in the invasive populations, five of which were found in more than one invasive population and will be subsequently referred to as common haplotypes. Three of the common haplotypes and two of the rare haplotypes were also found in at least one native population. Three main lineages of P. parva haplotypes can be recognised outside of Japan (Figures 3 and 4); a highly diverse central lineage (lineage 2) and two peripheral lineages (lineages 1 and 3) that are separated from the central lineage by 6 and 7 mutations, respectively. Lineage 3 consists of a single haplotype which is fixed in one of the native Taiwanese populations. One native population (TI) sampled in this study and the yellow river sample from Liu et al (2010) [39] are restricted to lineage 2 but do not share haplotypes with invasive populations. Three native populations (CG, CK, CY) sampled in this study and the Minjiang sample from Liu et al (2010) are restricted to lineage 1 and these populations also share a common haplotype with most introduced populations. Furthermore the Pearl River samples from Liu et al (2010) [39] fall into lineage 1 but do not share haplotypes with native populations. Two native populations (CRH, CH, Figure 1), however, contained haplotypes from both lineage 1 and 2 but share few haplotypes with the invasive populations. These two populations are from the Hai He River basin at the northern margin of the species distribution. The invasive populations are widely scattered across the network and most populations contain highly divergent haplotypes from both lineage 1 and 2. Among the native populations, the Taiwanese and Japanese (TI, TT, JB) populations do not share haplotypes with any native or invasive populations.


Invasive cyprinid fish in Europe originate from the single introduction of an admixed source population followed by a complex pattern of spread.

Simon A, Britton R, Gozlan R, van Oosterhout C, Volckaert FA, Hänfling B - PLoS ONE (2011)

Phylogenetic relationship of haplotypes based on NJ analysis.First value on branches indicate ML support value, second value indicate non-parametric bootstrapping of the NJ-tree. Values are only given for support values >70%.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3108587&req=5

pone-0018560-g003: Phylogenetic relationship of haplotypes based on NJ analysis.First value on branches indicate ML support value, second value indicate non-parametric bootstrapping of the NJ-tree. Values are only given for support values >70%.
Mentions: A total of 30 haplotypes were identified using 310 sequences from 8 native and 14 introduced populations (Table 1). The phylogenetic relationship among haplotypes is shown in Figure 3. Both NJ and ML methods yielded the same topology, hence only the NJ tree is displayed but ML support values were added to tree nodes. The two Japanese haplotypes, H23 and H24 were closely related to each other and the phylogenetic analysis (Figure 3) showed that they formed a highly divergent sister group to the remaining P. parva haplotypes (sequences divergence ∼5–6%). One highly divergent haplotype found in the invasive Polish populations clustered closely to a sequence of G. gobio. This haplotype and the Japanese haplotypes were therefore not included in the network analysis. Thirteen haplotypes were found in the invasive populations, five of which were found in more than one invasive population and will be subsequently referred to as common haplotypes. Three of the common haplotypes and two of the rare haplotypes were also found in at least one native population. Three main lineages of P. parva haplotypes can be recognised outside of Japan (Figures 3 and 4); a highly diverse central lineage (lineage 2) and two peripheral lineages (lineages 1 and 3) that are separated from the central lineage by 6 and 7 mutations, respectively. Lineage 3 consists of a single haplotype which is fixed in one of the native Taiwanese populations. One native population (TI) sampled in this study and the yellow river sample from Liu et al (2010) [39] are restricted to lineage 2 but do not share haplotypes with invasive populations. Three native populations (CG, CK, CY) sampled in this study and the Minjiang sample from Liu et al (2010) are restricted to lineage 1 and these populations also share a common haplotype with most introduced populations. Furthermore the Pearl River samples from Liu et al (2010) [39] fall into lineage 1 but do not share haplotypes with native populations. Two native populations (CRH, CH, Figure 1), however, contained haplotypes from both lineage 1 and 2 but share few haplotypes with the invasive populations. These two populations are from the Hai He River basin at the northern margin of the species distribution. The invasive populations are widely scattered across the network and most populations contain highly divergent haplotypes from both lineage 1 and 2. Among the native populations, the Taiwanese and Japanese (TI, TT, JB) populations do not share haplotypes with any native or invasive populations.

Bottom Line: A highly invasive freshwater fish, it is currently found in at least 32 countries outside its native range.Based on coalescent theory, all introduced and some native populations showed a relative excess of nucleotide diversity compared to haplotype diversity.Furthermore, it was preceded by, or associated with, the admixture of genetically diverse source populations that may have augmented its invasive-potential.

View Article: PubMed Central - PubMed

Affiliation: Evolutionary Biology Group, Department of Biological Sciences, University of Hull, Hull, United Kingdom. a.simon@2007.hull.ac.uk

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.

Show MeSH
Related in: MedlinePlus