Abstract
The analysis of temporal genetic variability is an essential yet largely neglected tool to unveil and predict the dynamics of introduced species. We here describe the temporal genetic structure and diversity over time of an introduced population of the ascidian Styela plicata (Lesueur, 1823) in Wilmington (North Carolina, USA, 34°08′24″N, 77°51′44″W). This population suffers important salinity and temperature changes, and in June every year we observed massive die-offs, leaving free substratum that was recolonized within a month. We sampled 12–14 individuals of S. plicata every 2 months from 2007 to 2009 (N = 196) and analyzed a mitochondrial marker (the gene cytochrome oxidase subunit I, COI) and seven nuclear microsatellites. Population genetic analyses showed similar results for both types of markers and revealed that most of the genetic variation was found within time periods. However, analyses conducted with microsatellite loci also showed weak but significant differences among time periods. Specifically, in the samplings after die-off episodes (August–November 2007 and 2008) the genetic diversity increased, the inbreeding coefficient showed prominent drops, and there was a net gain of alleles in the microsatellite loci. Taken together, our results suggest that recruits arriving from neighboring populations quickly occupied the newly available space, bringing new alleles with them. However, other shifts in genetic diversity and allele loss and gain episodes were observed in December–January and February–March 2008, respectively, and were apparently independent of die-off events. Overall, our results indicate that the investigated population is stable over time and relies on a periodic arrival of larvae from other populations, maintaining high genetic diversity and a complex interplay of allele gains and losses.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Airoldi L, Turon X, Perkol-Finkel S, Rius M (2015) Corridors for aliens but not for natives: effects of marine urban sprawl at a regional scale. Divers Distrib. doi:10.1111/ddi.12301
Altman S, Whitlatch RB (2007) Effects of small-scale disturbance on invasion success in marine communities. J Exp Mar Bio Ecol 342:15–29. doi:10.1016/j.jembe.2006.10.011
Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48
Barros RC, da Rocha RM, Pie MR (2009) Human-mediated global dispersion of Styela plicata (Tunicata, Ascidiacea). Aquat Invasions 4:45–57. doi:10.3391/ai.2009.4.1.4
Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (1996–2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier (France)
Blackburn TM, Pyšek P, Bacher S, Carlton JT, Duncan RP, Jarošík V, Wilson JRU, Richardson DM (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26:333–339. doi:10.1016/j.tree.2011.03.023
Bock DG, MacIsaac HJ, Cristescu ME (2012) Multilocus genetic analyses differentiate between widespread and spatially restricted cryptic species in a model ascidian. P Roy Soc B Biol Sci 279:2377–2385. doi:10.1098/rspb.2011.2610
Brunetti R, Menin F (1977) Ascidians of the Laguna Veneta II, Distribution and ecological observations. Boll Zool 44:337–352
Bunje PME, Barluenga M, Meyer A (2007) Sampling genetic diversity in the sympatrically and allopatrically speciating Midas cichlid species complex over a 16 year time series. BMC Evol Biol 7:25. doi:10.1186/1471-2148-7-25
Calderón I, Ortega N, Duran S, Becerro MA, Pascual M, Turon X (2007) Finding the relevant scale: clonality and genetic structure in a marine invertebrate (Crambe crambe, Porifera). Mol Ecol 16:1799–1810. doi:10.1111/j.1365-294X.2007.03276.x
Calderón I, Palacín C, Turon X (2009) Microsatellite markers reveal shallow genetic differentiation between cohorts of the common sea urchin Paracentrotus lividus (Lamarck) in northwest Mediterranen. Mol Ecol 18:3036–3049. doi:10.1111/j.1365-294X.2009.04239.x
Carlton J (1996) Marine bioinvasions: the alteration of marine ecosystems by nonindigenous species. Oceanography 9:36–43. doi:10.5670/oceanog.1996.25
Colautti RI, MacIsaac HJ (2004) A neutral terminology to define “invasive” species. Divers Distrib 10:135–141. doi:10.1111/j.1366-9516.2004.00061.x
Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014
Crooks JA, Chang AL, Ruiz GM (2011) Aquatic pollution increases the relative success of invasive species. Biol Invasions 13:165–176. doi:10.1007/s10530-010-9799-3
deRivera CE, Hitchcock NG, Teck SJ, Steves BP, Hines AH, Ruiz GM (2007) Larval development rate predicts range expansion of an introduced crab. Mar Biol 150:1275–1288. doi:10.1007/s00227-006-0451-9
Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449. doi:10.1111/j.1365-294X.2007.03538.x
Dupont L, Viard F, David P, Bishop JDD (2007) Combined effects of bottlenecks and selfing in populations of Corella eumyota, a recently introduced sea squirt in the English Channel. Divers Distrib 13:808–817. doi:10.1111/j.1472-4642.2007.00405.x
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620. doi:10.1111/j.1365-294X.2005.02553.x
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. doi:10.1111/j.1755-0998.2010.02847.x
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299
Forrest BM, Gardner JPA, Taylor MD (2009) Internal borders for managing invasive marine species. J Appl Ecol 46:46–54. doi:10.1111/j.1365-2664.2008.01544.x
Galil B (2000) A sea under siege–alien species in the Mediterranean. Biol Invasions 2:177–186. doi:10.1023/A:1010057010476
Galletly B, Blows M, Marshall D (2007) Genetic mechanisms of pollution resistance in a marine invertebrate. Ecol Appl 17:2290–2297. doi:10.1890/06-2079.1
Geller JB, Darling JA, Carlton JT (2010) Genetic perspectives on marine biological invasions. Ann Rev Mar Sci 2:367–393. doi:10.1146/annurev.marine.010908.163745
Gerlach G, Jueterbock A, Kraemer P, Deppermann J, Harmand P (2010) Calculations of population differentiation based on GST and D: forget GST but not all of statistics! Mol Ecol 19:3845–3852. doi:10.1111/j.1365-294X.2010.04784.x
Gienapp P, Teplitsky C, Alho JS, Mills JA, Merilä J (2008) Climate change and evolution: disentangling environmental and genetic responses. Mol Ecol 17:167–178. doi:10.1111/j.1365-294X.2007.03413.x
Goldstien SJ, Inglis GJ, Schiel DR, Gemmell NJ (2013) Using temporal sampling to improve attribution of source populations for invasive species. PLoS One 8:e65656. doi:10.1371/journal.pone.0065656
Gomaa NH, Montesinos-Navarro A, Alonso-Blanco C, Picó FX (2011) Temporal variation in genetic diversity and effective population size of Mediterranean and subalpine Arabidopsis thaliana populations. Mol Ecol 20:3540–3554. doi:10.1111/j.1365-294X.2011.05193.x
Grosberg R (1987) Limited dispersal and proximity-dependent mating success in the colonial ascidian Botryllus schlosseri. Evolution 41:372–384. doi:10.2307/2409145
Grosberg R, Cunningham CW (2001) Genetic structure in the sea. From populations to communities. In: Bertness MD, Gaines SDHM (eds) Marine community ecology. Sinauer Associates Inc, Sunderland, p 24
Grosholz E (2002) Ecological and evolutionary consequences of coastal invasions. Trends Ecol Evol 17:22–27. doi:10.1016/S0169-5347(01)02358-8
Habel JC, Husemann M, Finger A, Danley PD, Frank E (2013) The relevance of time series in molecular ecology and conservation biology. Biol Rev 89:484–492. doi:10.1111/brv.12068
Hedgecock D (1994) Population genetics of marine organisms. US Globec News 6:1–16. doi:10.1006/rwos.2001.0298
Hobbs RJ, Huenneke LF (1992) Disturbance, diversity, and invasion: implications for conservation. Conserv Biol 6:324–337. doi:10.1046/j.1523-1739.1992.06030324.x
Holland B (2000) Genetics of marine bioinvasions. Hydrobiologia 420:63–71. doi:10.1007/978-94-017-2184-4_7
Holland BS (2001) Invasion without a bottleneck : microsatellite variation in natural and invasive populations of the brown mussel Perna perna (L). Mar Biotechnol. doi:10.1007/s1012601-0060-Z
Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332. doi:10.1111/j.1755-0998.2009.02591.x
Jiang D, Smith WC (2005) Self- and cross-fertilization in the solitary ascidian Ciona savignyi. Biol Bull-US 209:107–112. doi:10.2307/3593128
Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. doi:10.1093/bioinformatics/btn129
Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94. doi:10.1186/1471-2156-11-94
Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026. doi:10.1111/j.1365-294X.2008.03887.x
Jost L (2009) D vs Gst: response to Heller and Siegismund (2009) and Ryman and Leimar (2009). Mol Ecol 18:20889–22091. doi:10.1111/j.1365-294X.2009.04186.x
Kalinowski ST (2005) Do polymorphic loci require large sample sizes to estimate genetic distances? Heredity 94:33–36. doi:10.1038/sj.hdy.6800548
Kano S, Chiba S, Satoh N (2001) Genetic relatedness and variability in inbred and wild populations of the solitary ascidian Ciona intestinalis revealed by arbitrarily primed polymerase chain reaction. Mar Biotechnol 3:58–67. doi:10.1007/s101260000048
Keller SR, Taylor DR (2008) History, chance and adaptation during biological invasion: separating stochastic phenotypic evolution from response to selection. Ecol Lett 11:852–866. doi:10.1111/j.1461-0248.2008.01188.x
Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204. doi:10.1016/S0169-5347(01)02101-2
Lambert G (2007) Invasive sea squirts: a growing global problem. J Exp Mar Bio Ecol 342:3–4. doi:10.1016/j.jembe.2006.10.009
Lee HJ, Boulding EG (2009) Spatial and temporal population genetic structure of four northeastern Pacific littorinid gastropods: the effect of mode of larval development on variation at one mitochondrial and two nuclear DNA markers. Mol Ecol 18:2165–2184. doi:10.1111/j.1365-294X.2009.04169.x
Lee CE, Gelembiuk GW (2008) Evolutionary origins of invasive populations. Evol Appl 1:427–448. doi:10.1111/j.1752-4571.2008.00039.x
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. doi:10.1093/bioinformatics/btp187
Locke A, Hanson JM (2011) Trends in invasive ascidian research: a view from the 3rd International Invasive Sea Squirt Conference. Aquat Invasions 6:367–370. doi:10.3391/ai.2011.6.4.01
Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228. doi:10.1016/j.tree.2005.02.004
Mallin MA, Esham EC, Williams KE, Nearhoof JE (1999) Tidal stage variability of fecal coliform and chlorophyll a concentrations in coastal creeks. Mar Pollut Bull 38:414–422. doi:10.1016/S0025-326X(99)00024-7
Mallin MA, Burkholder JM, Cahoon LB, Posey MH (2000) North and South Carolina coasts. Mar Pollut Bull 41:56–75. doi:10.1016/S0025-326X(00)00102-8
Manríquez P, Castilla J (2005) Self-fertilization as an alternative mode of reproduction in the solitary tunicate Pyura chilensis. Mar Ecol Prog Ser 305:113–125. doi:10.3354/meps305113
Marchetti M, Moyle P, Levine R (2004) Alien fishes in California watersheds: characteristics of successful and failed invaders. Ecol Appl 14:587–596. doi:10.1890/02-5301
Marin MG, Bressan M, Beghi L, Brunetti R (1987) Thermo-haline tolerance of Ciona intestinalis at different developmental stages. Cah Biol Mar 28:47–57
Meyers LA, Bull JJ (2002) Fighting change with change: adaptive variation in an uncertain world. Trends Ecol Evol 17:551–557. doi:10.1016/S0169-5347(02)02633-2
Narum SR (2006) Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv Genet 7:783–787. doi:10.1007/s10592-005-9056-y
Paz G, Douek J, Mo C, Goren M, Rinkevich B (2003) Genetic structure of Botryllus schlosseri (Tunicata) populations from the Mediterranean coast of Israel. Mar Ecol Prog Ser 250:153–162. doi:10.3354/meps250153
Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539. doi:10.1093/bioinformatics/bts460
Pérez-Portela R, Bishop JDD, Davis AR, Turon X (2009) Phylogeny of the families Pyuridae and Styelidae (Stolidobranchiata, Ascidiacea) inferred from mitochondrial and nuclear DNA sequences. Mol Phylogenet Evol 50:560–570. doi:10.1016/j.ympev.2008.11.014
Pérez-Portela R, Turon X, Bishop JDD (2012) Bottlenecks and loss of genetic diversity: spatio-temporal patterns of genetic structure in an ascidian recently introduced in Europe. Mar Ecol Prog Ser 451:93–105. doi:10.3354/meps09560
Pineda MC, López-Legentil S, Turon X (2011) The whereabouts of an ancient wanderer: global phylogeography of the solitary ascidian Styela plicata. PLoS One 6:e25495. doi:10.1371/journal.pone.0025495
Pineda MC, McQuaid CD, Turon X, López-Legentil S, Ordóñez V, Rius M (2012a) Tough adults, frail babies: an analysis of stress sensitivity across early life-history stages of widely introduced marine invertebrates. PLoS One 7:e46672. doi:10.1371/journal.pone.0046672
Pineda MC, Turon X, López-Legentil S (2012b) Stress levels over time in the introduced ascidian Styela plicata: the effects of temperature and salinity variations on hsp70 gene expression. Cell Stress Chaperones 17:435–444. doi:10.1007/s12192-012-0321-y
Pineda MC, López-Legentil S, Turon X (2013) Year-round reproduction in a seasonal sea: biological cycle of the introduced ascidian Styela plicata in the Western Mediterranean. Mar Biol 160:221–230. doi:10.1007/s00227-012-2082-7
Reem E, Douek J, Katzir G, Rinkevich B (2013) Long-term population genetic structure of an invasive urochordate: the ascidian Botryllus schlosseri. Biol Invasions 15:225–241. doi:10.1007/s10530-012-0281-2
Reusch TBH, Wood TE (2007) Molecular ecology of global change. Mol Ecol 16:3973–3992. doi:10.1111/j.1365-294X.2007.03454.x
Rius M, Darling J (2014) How important is intraspecific genetic admixture to the success of colonising populations? Trends Ecol Evol 29:233–242. doi:10.1016/j.tree.2014.02.003
Rius M, Turon X, Ordóñez V, Pascual M (2012) Tracking invasion histories in the sea: facing complex scenarios using multilocus data. PLoS One 7(4):e35815. doi:10.1371/journal.pone.0035815
Rius M, Turon X, Bernardi G, Volckaert FAM, Viard F (2015) Marine invasion genetics: from spatio-temporal patterns to evolutionary outcomes. Biol Inv 17:869–885. doi:10.1007/s10530-014-0792-0
Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454–464. doi:10.1016/j.tree.2007.07.002
Ruiz G, Carlton J, Grosholz E, Hines AH (1997) Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. Am Zool 37:621–632. doi:10.1093/icb/37.6.621
Sakai A, Allendorf F, Holt J (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332. doi:10.1146/annurev.ecolsys.32.081501.114037
Schneider SM, Guverich J (2001) Design and analysis of ecological experiments. Oxford University Press, New York
Selkoe K, Toonen RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol Lett 9:615–629. doi:10.1111/j.1461-0248.2006.00889.x
Stapley J, Reger J, Feulner PGD, Smadja C, Galindo J, Ekblom R, Bennison C, Ball AD, Beckerman AP, Slate J (2010) Adaptation genomics: the next generation. Trends Ecol Evol 25:705–712. doi:10.1111/j.1461-0248.2006.00889.x
Strayer DL, Eviner VT, Jeschke JM, Pace ML (2006) Understanding the long-term effects of species invasions. Trends Ecol Evol 21:645–651. doi:10.1016/j.tree.2006.07.007
Suarez AV, Tsutsui ND (2008) The evolutionary consequences of biological invasions. Mol Ecol 17:351–360. doi:10.1111/j.1365-294X.2007.03456.x
Sutherland JP (1974) Multiple stable points in natural communities. Am Nat 108:859–873. doi:10.1086/282961
Svane I, Young C (1989) The ecology and behaviour of ascidian larvae. Oceanogr Mar Biol Annu Rev 27:45–90
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molec Biol Evol 28:2731–2739. doi:10.1093/molbev/msr121
Torkkola J, Riginos C, Liggins L (2013) Regional patterns of mtDNA diversity in Styela plicata, an invasive ascidian, from Australian and New Zealand marinas. Mar Freshw Res 64:139–145. doi:10.1071/MF12289
Valero-Jiménez CA, Pérez-Portela R, López-Legentil S (2012) Characterization of novel microsatellite markers from the worldwide invasive ascidian Styela plicata. Conserv Genet Resour 4:559–561. doi:10.1007/s12686-011-9591-4
Vaselli S, Bulleri F, Benedetti-Cecchi L (2008) Hard coastal-defence structures as habitats for native and exotic rocky-bottom species. Mar Env Res 66:395–403. doi:10.1016/j.marenvres.2008.06.002
Verity R, Nichols RA (2014) What is genetic differentiation, and how should we measure it—GST, D, neither or both? Mol Ecol 23:4216–4225. doi:10.1111/mec.12856
Waples RS (1989) Temporal variation in allele frequencies: testing the right hypothesis. Evolution 43:1236–1251. doi:10.2307/2409359
Williamson M, Fitter A (1996) The varying success of invaders. Ecology 77:1661–1666. doi:10.2307/2265769
Yamaguchi M (1975) Growth and reproductive cycles of the marine fouling ascidians Ciona intestinalis, Styela plicata, Botrylloides violaceus, and Leptoclinum mitsukurii at Aburatsubo-Moroiso Inlet (central Japan). Mar Biol 29:253–259. doi:10.1007/BF00391851
Zenetos A, Gofas S, Verlaque M, Cinar ME, Garci JE, Bianchi CN, Morri C, Azzurro E, Bilecenoglu M, Froglia C, Siokou I, Violanti D, Sfriso A, Giangrande A, Mastrototaro F, An TK, Ballesteros E, Zingone A, Gambi MC, Streftaris N (2010) Alien species in the Mediterranean Sea by 2010. A contribution to the application of European Union’s Marine Strategy Framework Directive (MSFD). Part I. Spatial distribution. Mediterr Mar Sci 11:381–493
Acknowledgments
Special thanks are to C. Valero-Jimenez, who designed and optimized the microsatellite primers and collaborated with the genotyping of some samples. This research was supported by a grant from the United States–Israel Binational Science Foundation (BSF), Jerusalem, Israel (number 2014025), the Spanish Government project CTM2013—48163—and the Catalan Government Grant 2014SGR-336 for Consolidated Research Groups.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The present study does not raise any ethical issues. While this study involves research on animals, ascidians are not under the regulation of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES). Moreover, the number of collected animals was as low as possible and the manipulation was fast and painless.
Additional information
Responsible Editor: O. Puebla.
Reviewed by undisclosed experts.
This article is part of the Topical Collection on Invasive Species.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Pineda, M.C., Turon, X., Pérez-Portela, R. et al. Stable populations in unstable habitats: temporal genetic structure of the introduced ascidian Styela plicata in North Carolina. Mar Biol 163, 59 (2016). https://doi.org/10.1007/s00227-016-2829-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-016-2829-7