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Cited by 85Genetic diversity and population structureMarine Ecology and Invasive SpeciesMarine Biology and Ecology Research

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Contrasting global genetic patterns in two biologically similar, widespread and invasive Ciona species (Tunicata, Ascidiacea)

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Bouchemousse, Sarah, Bishop, John D. D., Viard, Frédérique·2016·Scientific Reports
DOI 10.1038/srep24875PMC PMC4853746
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Abstract

Human-mediated dispersal interplays with natural processes and complicates understanding of the biogeographical history of species. This is exemplified by two invasive tunicates, Ciona robusta (formerly Ciona intestinalis type A) and C. intestinalis (formerly Ciona intestinalis type B), globally distributed and sympatric in Europe. By gathering new mitochondrial sequences that were merged with published datasets, we analysed genetic patterns in different regions, with a focus on 1) their sympatric range and 2) allopatric populations in N and S America and southern Europe. In the sympatric range, the two species display contrasting genetic diversity patterns, with low polymorphism in C. robusta supporting the prevalent view of its recent introduction. In the E Pacific, several genetic traits support the non-native status of C. robusta. However, in the NE Pacific, this appraisal requires a complex scenario of introduction and should be further examined supported by extensive sampling efforts in the NW Pacific (putative native range). For C. intestinalis, Bayesian analysis suggested a natural amphi-North Atlantic distribution, casting doubt on its non-native status in the NW Atlantic. This study shows that both natural and human-mediated dispersal have influenced genetic patterns at broad scales; this interaction lessens our ability to confidently ascertain native vs. non-native status of populations, particularly of those species that are globally distributed.

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Figure 1 Worldwide distribution of Ciona robusta (A) and C. intestinalis (B) based on literature records. Areas where the species have been regarded as native or as non-native or cryptogenic (i.e. of undefined status) are in blue and red respectively. For each allopatric geographical region, the approximate time is given of the first report in the literature of Ciona intestinalis sensu lato (i.e. including both C. intestinalis and C. robusta before the distinction was appreciated); for the EC (sympatric region), the time shown for C. robusta is of its first documented presence as distinct from C. intestinalis; details in Supplementary Note. Map was obtained from http://www.pedagogie.ac-aix-marseille.fr/jcms/c_67064/fr/cartotheque under the permission of the creator (Daniel Dalet©Académie Aix-Marseille).
Figure 1 Worldwide distribution of Ciona robusta (A) and C. intestinalis (B) based on literature records. Areas where the species have been regarded as native or as non-native or cryptogenic (i.e. of undefined status) are in blue and red respectively. For each allopatric geographical region, the approximate time is given of the first report in the literature of Ciona intestinalis sensu lato (i.e. including both C. intestinalis and C. robusta before the distinction was appreciated); for the EC (sympatric region), the time shown for C. robusta is of its first documented presence as distinct from C. intestinalis; details in Supplementary Note. Map was obtained from http://www.pedagogie.ac-aix-marseille.fr/jcms/c_67064/fr/cartotheque under the permission of the creator (Daniel Dalet©Académie Aix-Marseille).CC BY · PubMed Central
Figure 2 Location of the study populations and haplotype frequencies (COX3-ND1) at the population level for C. robusta (A) and C. intestinalis (B). Sites of Ciona robusta (A) and of Ciona intestinalis (B) sampled for this study are indicated in black and bold (for population codes and sampling, see Table S1). The localities studied by Zhan and co-authors25 that are included in the present study are in grey and underlined. Each color in pie charts refers to a given haplotype (see haplotype name in the box) as defined in the network in Fig. 3ab for C. robusta and C. intestinalis, respectively. The haplotypes with a name followed by an asterisk are shared between at least two regions. For sake of clarity, only the haplotypes shared between regions or with frequency higher than 0.1 at population level are shown wth a specific color for C. intestinalis. Maps were obtained from http://www.pedagogie.ac-aix-marseille.fr/jcms/c_67064/fr/cartotheque under the permission of the creator (Daniel Dalet©Académie Aix-Marseille).
Figure 2 Location of the study populations and haplotype frequencies (COX3-ND1) at the population level for C. robusta (A) and C. intestinalis (B). Sites of Ciona robusta (A) and of Ciona intestinalis (B) sampled for this study are indicated in black and bold (for population codes and sampling, see Table S1). The localities studied by Zhan and co-authors25 that are included in the present study are in grey and underlined. Each color in pie charts refers to a given haplotype (see haplotype name in the box) as defined in the network in Fig. 3ab for C. robusta and C. intestinalis, respectively. The haplotypes with a name followed by an asterisk are shared between at least two regions. For sake of clarity, only the haplotypes shared between regions or with frequency higher than 0.1 at population level are shown wth a specific color for C. intestinalis. Maps were obtained from http://www.pedagogie.ac-aix-marseille.fr/jcms/c_67064/fr/cartotheque under the permission of the creator (Daniel Dalet©Académie Aix-Marseille).CC BY · PubMed Central
Figure 3 Median-joining haplotype networks of Ciona robusta (A) and C. intestinalis (B) based on COX3-ND1 sequences. Data from this study and from Zhan et al.25. Haplotype circles are proportional to haplotype frequency in the whole dataset. Branch lengths are proportional to number of mutational steps between two haplotypes. Missing haplotypes are indicated by small black circles. Colors represent the regions where the individuals possessing the haplotypes were found (regional codes are provided in Table 1).
Figure 3 Median-joining haplotype networks of Ciona robusta (A) and C. intestinalis (B) based on COX3-ND1 sequences. Data from this study and from Zhan et al.25. Haplotype circles are proportional to haplotype frequency in the whole dataset. Branch lengths are proportional to number of mutational steps between two haplotypes. Missing haplotypes are indicated by small black circles. Colors represent the regions where the individuals possessing the haplotypes were found (regional codes are provided in Table 1).CC BY · PubMed Central
Figure 4 Non-metric multidimensional scaling plots constructed using pairwise FST estimates among (A) all populations of C. robusta and (B) all populations of C. intestinalis. The same colour code as in Fig. 3 was used to represent regions.
Figure 4 Non-metric multidimensional scaling plots constructed using pairwise FST estimates among (A) all populations of C. robusta and (B) all populations of C. intestinalis. The same colour code as in Fig. 3 was used to represent regions.CC BY · PubMed Central
Figure 5 Demographic and divergence parameters estimated under isolation with migration model for Ciona intestinalis. (A) Diagram of the population splitting events (see Table 1 for codes of geographical areas). Time axis is not to scale. (B) Estimates of times of divergence and demographic parameters for the two studied regions using COX3-ND1 sequences. Nanc, NNEA, NNWA: effective population size; M1 and M2: number of migrants per generation; tdiv: time since divergence. Median value and the 95% highest posterior density (95 HPD) of each parameter are given. (C) Tests for the migration model; Log(p’(Θ|X): log of the highest posterior density of each model; −2Λ: likelihood ratio; d.f.: degrees of freedom; and P-value.
Figure 5 Demographic and divergence parameters estimated under isolation with migration model for Ciona intestinalis. (A) Diagram of the population splitting events (see Table 1 for codes of geographical areas). Time axis is not to scale. (B) Estimates of times of divergence and demographic parameters for the two studied regions using COX3-ND1 sequences. Nanc, NNEA, NNWA: effective population size; M1 and M2: number of migrants per generation; tdiv: time since divergence. Median value and the 95% highest posterior density (95 HPD) of each parameter are given. (C) Tests for the migration model; Log(p’(Θ|X): log of the highest posterior density of each model; −2Λ: likelihood ratio; d.f.: degrees of freedom; and P-value.CC BY · PubMed Central

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Citations

Cites

Research works printed but not linked: 5

  1. Millar, R. H. In L.M.B.C. Memoirs of typical British marine palnts and animals, XXXV (ed J. S. Colman ) 123 (Liverpool University Press, 1953).
  2. Carver, C. E., Mallet, A. L. & Vercaemer, B. Biological synopsis of the solitary tunicate Ciona intestinalis . Can. Man. Rep. Fish. Aquat. Sci. 2746, v+ 55p. (2006).
  3. Bouchemousse, S., Haag-Liautard, C., Bierne, N. & Viard, F. Past and contemporary introgression between two strongly differentiated Ciona species as revealed by a post-genomic SNPs panel. BioRxiv, doi: 10.1101/030346 (2015). · DOI
  4. Guillemin, M.-L. et al. In Seaweed Phylogeography (eds Zi-Min Hu & Ceridwen Fraser ) Ch. 10, 251–277 (Springer Netherlands, 2016).
  5. Brante, A., Fernandez, M. & Viard, F. Phylogeography and biogeography concordance in the marine gastropod Crepipatella dilatata (Calyptraidae) along the South Eastern Pacific coast J. Heredity 103, 630–637, doi: 10.11093/jhered/ess030 (2012). · DOI

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Metadata

Authors
Bouchemousse, S., Bishop, J. D. D., & Viard, F.
Affiliations
  • Centre National de la Recherche Scientifique (FR)
  • Marine Biological Association of the United Kingdom (GB)
Corresponding author
  • Bouchemousse, Sarah
  • Viard, Frédérique
ORCID
Venue
Scientific Reports
Publisher
Springer Science and Business Media LLC
Published
2016-05-03
Volume
6
Issue
1
Pages
24875-24875
ISSN
2045-2322 (ISSN-L)
DOI
10.1038/srep24875
PMC
PMC4853746
OpenAlex
W2346624115
Cited by
85
References
82
Citations by year
2026: 4 · 2025: 6 · 2024: 5 · 2023: 3 · 2022: 10 · 2021: 6 · 2020: 12 · 2019: 11 · 2018: 12 · 2017: 12 · 2016: 4
FWCI
10.50
Type
journal article
Language
en
Open access
Licence
Locations
  • Scientific Reports (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Marine Biological Association (acceptedVersion)
  • HAL (submittedVersion, cc-by)
Funders
  • Agence Nationale de la Recherche (ANR-12-BSV7-0011, ANR-12)
  • Centre National de la Recherche Scientifique
  • Institut National de la Recherche Agronomique
  • Muséum National d'Histoire Naturelle
  • Interreg
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic diversity and population structure
  • Physical Sciences › Environmental Science › Global and Planetary Change › Marine Ecology and Invasive Species
  • Physical Sciences › Earth and Planetary Sciences › Oceanography › Marine Biology and Ecology Research
Keywords
Ciona robusta, Ciona intestinalis, invasive species, biogeography, genetic diversity, mitochondrial DNA, sympatric populations, allopatric populations, human-mediated dispersal, North Atlantic distribution, Pacific Ocean distribution
MeSH terms
Animals, Ciona intestinalis, DNA, Mitochondrial, Europe, North America, South America, Genetic Variation, Sequence Analysis, DNA, Phylogeography

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