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Successful worldwide invasion of the veined rapa whelk, Rapana venosa, despite a dramatic genetic bottleneck

Successful worldwide invasion of the veined rapa whelk, Rapana venosa, despite a dramatic genetic... Biological invasions represent an important component of global change, with potentially huge detrimental effects on native biological biodiversity and ecosystems. Knowledge about invasion history provides information about the invasion process and the origin and genetic composition of invading populations. To clarify the source and invasive routes of a successful world-wide invader, the veined rapa whelk, Rapana venosa, genetic variability of samples from five representative native populations from coasts of Japan and China and 13 worldwide invasive populations was analyzed using 11 nuclear microsatellite loci. A dramatic decrease of genetic variation was detected in the invasive populations compared with the native populations. The results demonstrated that R. venosa was capable of establishing itself in many areas despite a dramatic genetic bottleneck, suggesting that a remarkable reduction of genetic diversity is not a limiting factor for short-term success of this invasive species. Considering the lack of mitochondrial variation previously observed in the invasive populations, the dramatic genetic bottleneck and the allele distribution detected using microsatellites suggested that the original introduced Black Sea population could have been founded by very few individuals, perhaps only a single female and a single male. The initial invasive Black Sea population was likely an accidental introduction from Japan, and then invaded the Adriatic Sea by range expansion, which served as a source for subsequent invasive populations in Europe and America by various transport vectors. In addition, microsatellite alleles in the invasive populations showed a tendency to mutate with the addition or deletion of a single repeat, which is consistent with the stepwise mutation model. Our findings provide a good example of how an aquatic invader with a drastic genetic bottleneck and very low genetic diversity rapidly expands its geographical range. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Biological Invasions Springer Journals

Successful worldwide invasion of the veined rapa whelk, Rapana venosa, despite a dramatic genetic bottleneck

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Publisher
Springer Journals
Copyright
Copyright © 2018 by Springer International Publishing AG, part of Springer Nature
Subject
Life Sciences; Ecology; Freshwater & Marine Ecology; Plant Sciences; Developmental Biology
ISSN
1387-3547
eISSN
1573-1464
DOI
10.1007/s10530-018-1774-4
Publisher site
See Article on Publisher Site

Abstract

Biological invasions represent an important component of global change, with potentially huge detrimental effects on native biological biodiversity and ecosystems. Knowledge about invasion history provides information about the invasion process and the origin and genetic composition of invading populations. To clarify the source and invasive routes of a successful world-wide invader, the veined rapa whelk, Rapana venosa, genetic variability of samples from five representative native populations from coasts of Japan and China and 13 worldwide invasive populations was analyzed using 11 nuclear microsatellite loci. A dramatic decrease of genetic variation was detected in the invasive populations compared with the native populations. The results demonstrated that R. venosa was capable of establishing itself in many areas despite a dramatic genetic bottleneck, suggesting that a remarkable reduction of genetic diversity is not a limiting factor for short-term success of this invasive species. Considering the lack of mitochondrial variation previously observed in the invasive populations, the dramatic genetic bottleneck and the allele distribution detected using microsatellites suggested that the original introduced Black Sea population could have been founded by very few individuals, perhaps only a single female and a single male. The initial invasive Black Sea population was likely an accidental introduction from Japan, and then invaded the Adriatic Sea by range expansion, which served as a source for subsequent invasive populations in Europe and America by various transport vectors. In addition, microsatellite alleles in the invasive populations showed a tendency to mutate with the addition or deletion of a single repeat, which is consistent with the stepwise mutation model. Our findings provide a good example of how an aquatic invader with a drastic genetic bottleneck and very low genetic diversity rapidly expands its geographical range.

Journal

Biological Invasions – Springer Journals

Published: May 31, 2018

References

  • The estimation of population differentiation with microsatellite markers
    Balloux, F; Lugon-Moulin, N
  • Adaptation from standing genetic variation
    Barrett, RDH; Schluter, D
  • Approximate Bayesian computation in evolution and ecology
    Beaumont, MA
  • Approximate Bayesian computation in population genetics
    Beaumont, MA; Zhang, W; Balding, DJ
  • Comparison of Bayesian and maximum-likelihood inference of population genetic parameters
    Beerli, P
  • Genomic signatures of rapid adaptive evolution in the bluespotted cornetfish, a Mediterranean Lessepsian invader
    Bernardi, G; Azzurro, E; Golani, D; Miller, MR
  • The influence of numbers on invasion success
    Blackburn, TM; Lockwood, JL; Cassey, P
  • What we still don’t know about invasion genetics
    Bock, DG; Caseys, C; Cousens, RD
  • First report of predation by a small shark on the invasive rapa whelk Rapana venosa (Valenciennes, 1846) in Argentinean waters
    Bonelli, AG; Giachetti, CB; Jaureguizar, AJ; Milessi, AC
  • Population genetics of the invasive cryptogenic anemone, Anemonia alicemartinae, along the southeastern Pacific coast
    Canales-Aguirre, C; Quiñones, A; Hernández, C; Neill, P; Brante, A
  • Observations on the invading gastropod Rapana venosa in Punta del Este, Maldonado Bay, Uruguay
    Carranza, A; Mello, C; Ligrone, A; González, S; Píriz, P; Scarabino, F
  • Loggerhead turtles Caretta caretta (Linnaeus) preying on the invading gastropod Rapana venosa (Valenciennes) in the Río de la Plata Estuary
    Carranza, A; Scarabino, F; Estrades, A
  • Shell morphotypes of the invasive gastropod Rapana venosa in the Northern Adriatic Sea
    Castellazzi, M; Savini, D; Ambrogi, AO
  • Genetically monomorphic invasive populations of the rapa whelk, Rapana venosa
    Chandler, E; Mcdowell, J; Graves, J
  • Sexual maturation, spawning, and deposition of the egg capsules of the female purple shell, Rapana venosa (Gastropoda: Muricidae)
    Chung, EY; Kim, SY; Park, K; Park, GM
  • Contemporary evolution during invasion: evidence for differentiation, natural selection, and local adaptation
    Colautti, RI; Lau, JA
  • Inferring population history with DIY ABC: a user-friendly approach to approximate Bayesian computation
    Cornuet, J-M; Santos, F; Beaumont, MA; Robert, CP; Marin, J-M; Balding, DJ; Guillemaud, T; Estoup, A
  • Genetic reconstructions of invasion history
    Cristescu, ME
  • Combining field epidemiological information and genetic data to comprehensively reconstruct the invasion history and the microevolution of the sudden oak death agent Phytophthora ramorum (Stramenopila: Oomycetes) in California
    Croucher, PJP; Mascheretti, S; Garbelotto, M
  • Genetic studies of aquatic biological invasions: closing the gap between research and management
    Darling, JA
  • The devil is in the details: genetic variation in introduced populations and its contributions to invasion
    Dlugosch, KM; Anderson, SR; Braasch, J; Cang, FA; Gillette, HD
  • Effect of Rapana bezoar Linne (Mollusca, Muricidae) on the Black Sea fauna
    Drapkin, E
  • Genome sequencing and population genomics in non-model organisms
    Ellegren, H
  • Reconstructing routes of invasion using genetic data: why, how and so what?
    Estoup, A; Guillemaud, T
  • Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study
    Evanno, G; Regnaut, S; Goudet, J
  • Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows
    Excoffier, L; Lischer, HEL
  • Invasion biology-resolving the genetic paradoxin invasive species
    Frankham, R
  • An increase in transmission-related traits and in phenotypic plasticity is documented during a fungal invasion
    Garbelotto, M; Rocca, GD; Osmundson, T; Lonardo, VD; Danti, R
  • Genetic bottlenecks and successful biological invasions: the case of a recent Lessepsian migrant
    Golani, D; Azzurro, E; Corsini-Foka, M
  • Global invasion history of the tropical fire ant: a stowaway on the first global trade routes
    Gotzek, D; Axen, HJ; Suarez, AV; Helms Cahan, S; Shoemaker, D
  • Predation by blue crabs, Callinectes sapidus, on rapa whelks, Rapana venosa: possible natural controls for an invasive species?
    Harding, JM
  • Growth and development of veined rapa whelk Rapana venosa veligers
    Harding, JM
  • Veined rapa whelk (Rapana venosa) range extensions in the Virginia waters of Chesapeake Bay, USA
    Harding, JM; Mann, R
  • The effects of female size on fecundity in a large marine gastropod Rapana venosa (Muricidae)
    Harding, JM; Mann, R; Kilduff, CW
  • Genetic evidence for multiple sources of the non-native fish Cichlasoma urophthalmus (Günther; Mayan Cichlids) in Southern Florida
    Harrison, E; Trexler, JC; Collins, TM
  • Genetic assessment of connectivity among marine populations
    Hellberg, ME; Burton, RS; Neigel, JE; Palumbi, SR
  • Genetic diversity and colony breeding structure in native and introduced ranges of the Formosan subterranean termite, Coptotermes formosanus
    Husseneder, C; Simms, DM; Delatte, JR
  • adegenet: a R package for the multivariate analysis of genetic markers
    Jombart, T
  • Discriminant analysis of principal components: a new method for the analysis of genetically structured populations
    Jombart, T; Devillard, S; Balloux, F
  • Relationship between phylogenetic distribution and genomic features in Neurospora crassa
    Kasuga, T; Mannhaupt, G; Glass, NL
  • Host-induced aneuploidy and phenotypic diversification in the Sudden Oak Death pathogen Phytophthora ramorum
    Kasuga, T; Mai, B; Bernhardt, E
  • Heterozygosity in an isolated population of a large mammal founded by four individuals is predicted by an individual-based genetic model
    Kekkonen, J; Wikström, M; Brommer, JE
  • Clumpak: a program for identifying clustering modes and packaging population structure inferences across K
    Kopelman, NM; Mayzel, J; Jakobsson, M; Rosenberg, NA; Mayrose, I
  • Comparative analysis of Rapana venosa (Valenciennes, 1846) from different biotopes of the Black Sea based on its morphological characteristics
    Kos’yan, A
  • Unintended backpackers: bio-fouling of the invasive gastropod Rapana venosa on the green turtle Chelonia mydas in the Río de la Plata Estuary, Uruguay
    Lezama, C; Carranza, A; Fallabrino, A; Estrades, A; Scarabino, F; López-Mendilaharsu, M
  • StructureSelector: a web based software to select and visualize the optimal number of clusters using multiple methods
    Li, Y-L; Liu, J-X
  • Low mutation rates of microsatellite loci in Drosophila melanogaster
    Malcolm, DS; Aquadro, F
  • Invasion of the North American Atlantic coast by a large predatory Asian mollusc
    Mann, R; Harding, JM
  • Salinity tolerance of larval Rapana venosa: implications for dispersal and establishment of an invading predatory gastropod on the North American Atlantic coast
    Mann, R; Harding, JM
  • Alien species alert: Rapana venosa (veined whelk)
    Mann, R; Occhipinti, A; Harding, JM
  • Genetic epidemiology of the sudden oak death pathogen Phytophthora ramorum in California
    Mascheretti, S; Croucher, PJP; Kozanitas, M; Baker, L; Garbelotto, M
  • Molecular evidence for an extreme genetic bottleneck during introduction of an invading grass to California
    Meimberg, H; Hammond, JI; Jorgensen, CM
  • Beyond Bonferroni: less conservative analyses for conservation genetics
    Narum, SR
  • Accuracy of estimated phylogenetic trees from molecular data
    Nei, M; Tajima, F; Tateno, Y
  • Rapana venosa (Gastropoda: Muricidae): a new invasive species in the North Sea
    Nieweg, D; Post, J; Vink, R
  • Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power
    Paetkau, D; Slade, R; Burden, M; Estoup, A
  • Rapana Venosa (Valenciennes, 1846) (Mollusca: Muricidae): a new gastropod in South Atlantic waters
    Pastorino, G; Penchaszadeh, PE; Schejter, L; Bremec, C
  • GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update
    Peakall, R; Smouse, PE
  • GENECLASS2: a software for genetic assignment and first-generation migrant detection
    Piry, S; Alapetite, A; Cornuet, J-M; Paetkau, D; Baudouin, L; Estoup, A
  • Adaptive evolution in invasive species
    Prentis, PJ; Wilson, JR; Dormontt, EE; Richardson, DM; Lowe, AJ
  • Documentation for structure software: version 2.3
    Pritchard, J; Wen, X; Falush, D
  • Genetic bottleneck in invasive species: the potato tuber moth adds to the list
    Puillandre, N; Dupas, S; Dangles, O
  • Evaluation of the introduction history and genetic diversity of a serially introduced fish population in New Zealand
    Purcell, K; Ling, N; Stockwell, C
  • Correlation between fitness and genetic diversity
    Reed, DH; Frankham, R
  • Paradox lost: genetic diversity and the success of aquatic invasions
    Roman, J; Darling, JA
  • GENEPOP ‘007: a complete re-implementation of the GENEPOP software for Windows and Linux
    Rousset, F
  • The population biology of invasive species
    Sakai, AK; Allendorf, FW; Holt, JS
  • Invasion success of the bumblebee, Bombus terrestris, despite a drastic genetic bottleneck
    Schmid-Hempel, P; Schmid-Hempel, R; Brunner, P; Seeman, O; Allen, G
  • Rapa whelk controls demersal community structure off Zmiinyi Island, Black Sea
    Snigirov, S; Medinets, V; Chichkin, V; Sylantyev, S
  • POPTREE2: software for constructing population trees from allele frequency data and computing other population statistics with Windows interface
    Takezaki, N; Nei, M; Tamura, K
  • Reduced genetic variation and the success of an invasive species
    Tsutsui, ND; Suarez, AV; Holway, DA; Case, TJ
  • Mitochondrial and microsatellite DNA markers reveal a Balkan origin for the highly invasive horse-chestnut leaf miner Cameraria ohridella (Lepidoptera, Gracillariidae)
    Valade, R; Kenis, M; Hernandez-Lopez, A
  • Reconstruction of microsatellite mutation history reveals a strong and consistent deletion bias in invasive clonal snails, Potamopyrgus antipodarum
    Weetman, D; Hauser, L; Carvalho, GR
  • Rapid evolution in introduced species, ‘invasive traits’ and recipient communities: challenges for predicting invasive potential
    Whitney, KD; Gabler, CA
  • Microsatellite evidence for high frequency of multiple paternity in the marine gastropod Rapana venosa
    Xue, D-X; Zhang, T; Liu, J-X
  • Influences of population density on polyandry and patterns of sperm usage in the marine gastropod Rapana venosa
    Xue, D-X; Zhang, T; Liu, J-X
  • Genetic diversity and population structure of the veined rapa whelk Rapana venosa along the coast of China based on microsatellites
    Xue, D-X; Zhang, T; Li, Y-L; Liu, J-X
  • Studies on species of Murididae off the China coasts* III. Rapana
    Zhang, FS
  • Genetic diversity in native and introduced populations of the amethyst gem clam Gemma gemma (Totten, 1834) from the US east and west coasts
    Zhang, H; Geller, JB; Vrijenhoek, RC
  • The Black Sea ecosystem changes related to the introduction of new mollusc species
    Zolotarev, V