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Worldwide phylogeography of the invasive ctenophore Mnemiopsis leidyi (Ctenophora) based on nuclear and mitochondrial DNA data

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Abstract

The ctenophore Mnemiopsis leidyi is one of the most successful marine bioinvaders on record. Native to the Atlantic coast of the Americas, M. leidyi invaded the Black Sea, Caspian and Mediterranean Seas beginning the in late 1980s, followed by the North and Baltic Seas starting in 2006, with major concomitant alterations in pelagic ecology, including fishery collapses in some cases. Using extensive native range sampling (21 sites), along with 11 invasive sites in the Black, Caspian, Mediterranean, North and Baltic Seas, we examined M. leidyi worldwide phylogeographic patterns using data from mitochondrial cytochrome b (cytb) and six nuclear microsatellite loci. Cytb and microsatellite data sets showed different levels of genetic differentiation in the native range. Analyses of cytb data revealed considerable genetic differentiation, recovering three major clusters (northwestern Atlantic, Caribbean, and South America) and further divided northwestern Atlantic sampling sites into three groups, separated approximately at Cape Hatteras on the US Atlantic coast and at the Floridian peninsula, separating the Gulf of Mexico and Atlantic coasts. In contrast, microsatellite data only distinguished samples north and south of Cape Hatteras, and suggested considerable gene flow among native samples with clear evidence of isolation by distance. Both cytb and microsatellite data sets indicated that the northern invaders (North/Baltic Seas) originated from north of Cape Hatteras, with cytb data pointing to Delaware and north. Microsatellite data indicated a source for the southern invaders (Black, Caspian and Mediterranean Seas) to be south of Cape Hatteras, while cytb data narrowed the source location to the Gulf of Mexico region. Both cytb and microsatellite data sets suggested that the southern invasion was associated with genetic bottlenecks while evidence was equivocal for the northern invasion. By increasing the native range spatial sampling, our dataset was able to sufficiently characterize patterns and levels of genetic differentiation in the native range of M. leidyi and identify likely biogeographic boundaries, allowing for the most complete characterization of M. leidyi’s invasion histories and most realistic estimates of its source region(s) to date.

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Acknowledgments

The authors would like to thank the following people and Institutions for either providing tissue, helping in the collection of tissue or offering lab space or ship time, all of which was vital to the success of this manuscript: W.M. Graham, S.M. Chapotin, E. Christou, Dauphin Island Sea Lab, M. Faasse, V. Fuentes, S. Gunn, F. Hernandez, J. Javidpour, P. Kasapidis, A. Kideys, P. Kremer, H. Mianzan, A. Morandini, A. Moss, U. Niermann, K. Robinson, T. Shiganova, I. Sikou-Frangou, B. Sullivan, M. Telli, D. Thibault-Botha, R. Waggett, Smithsonian Environmental Research Center, and the crews of the R/V Bilim [Middle East Technical University], R/V Knorr [Woods Hole Oceanographic Institute]. PCR primers for cytb were designed based on preliminary sequences gratefully provided by M.Q. Martindale prior to sequencing of the complete mitochondrial genome of M. leidyi (Pett et al. 2011). A small part of the cytb dataset was collected in the lab of M.N. Dawson. K.M.B would like to acknowledge the assistance of A. Marsh during the early stages of this project. The study was supported by YIBS (Yale Institute for Biospheric Studies) funding and research grants from Sigma Xi and YSEA (Yale Science and Engineering Association) supporting the work of Yale undergraduates (Chang and Moseley) and a Sigma Xi Grant in Aid of Research (GIAR) to K. Bayha. The publication of this paper is supported by CONISMA, the Italian National Interuniversity Consortium for Marine Sciences, which received funding from the European Community’s Seventh Framework Programme (FP7/2007-2013) for the project VECTORS (http://www.marine-vectors.eu). This paper stems from the International workshop MOLTOOLS (Molecular Tools for Monitoring Marine Invasive Species), held in Lecce, Italy, in September 2012.

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10530_2014_770_MOESM7_ESM.tif

Comparison of cytb haplotype diversity values (θ) between invasive sampling sites and their likeliest source regions based on phylogeographic and population genetic data for two independent invasions of M. leidyi. (A) “Southern” Invasion: Native (Gulf of Mexico [TAM to PAT]) and Invasive (Southern Europe [Black/Caspian/Mediterranean Seas]) sites; (B) “Northern” invasion: Native (Atlantic sites north of Chesapeake Bay [WH to RBD] and invasive (Northern Europe [KBG and NTH]) sites. Mean haplotype diversity values were compared by Welch’s t-tests calculated using SYSTAT v.11 (SYSTAT Software Inc.) (TIFF 719 kb)

10530_2014_770_MOESM8_ESM.tif

Results of the Structure analyses within the native range using six microsatellite loci for different K values (A; K = 3, B: K = 4; C: K = 15) (TIFF 807 kb)

10530_2014_770_MOESM9_ESM.tif

Comparison of genetic diversity based on microsatellite data between native and invasive sites for two independent invasions by M. leidyi: (A) “Southern” invasion of the Black, Caspian and Mediterranean Seas and (B) “Northern” invasion of the North and Baltic Seas. For each invasion, the first graph shows comparisons of allelic diversity (An) and the second shows the same for observed heterozygosity (Ho). Native regions are defined based on population genetic analyses of microsatellite data. For the “Southern” invasion (A), the native range is assigned as all sites south of Cape Hatteras to the Caribbean (CHS to BEZ). South American sites were removed since they clustered apart from other native and invasive populations in Fig. 6. For the “Northern” invasion (B), the native range is assigned as all Atlantic coastal sites north of Cape Hatteras (WH to PAM). For both allelic richness (An) and observed heterozygosity (Ho), mean values were compared by Welch’s t-tests calculated using SYSTAT v.11 (SYSTAT Software Inc.) (TIFF 881 kb)

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Bayha, K.M., Chang, M.H., Mariani, C.L. et al. Worldwide phylogeography of the invasive ctenophore Mnemiopsis leidyi (Ctenophora) based on nuclear and mitochondrial DNA data. Biol Invasions 17, 827–850 (2015). https://doi.org/10.1007/s10530-014-0770-6

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