Abstract
Indo-Pacific lionfish (Pterois volitans and P. miles) recently invaded Western Atlantic waters, rapidly spreading through the Caribbean and Gulf of Mexico (GoM). Previous genetic analyses using the mitochondrial d-loop determined that populations in the Western North Atlantic (NA) region have up to nine haplotypes, whereas Caribbean populations contain four of the North Atlantic haplotypes. The genetic composition of GoM populations, reported here for the first time, could lend insight into the pathway of dispersal into the GoM and better understanding of the biogeography of this recent invader. Here, we determined the genetic composition of lionfish throughout the GoM and compared haplotype composition to Caribbean and North Atlantic regions. We found that GoM samples contained only three d-loop haplotypes that are common in the Caribbean and North Atlantic. The genetic structure differed significantly among the three regions (AMOVA:Φ CT = 0.062; p = 0.001), but we found no differences between locations within regions (AMOVA:Φ SC = 0.005; p = 0.092). The composition of GoM samples most closely matches the composition of Caribbean samples indicating that Caribbean populations are the likely source of the GoM populations. As each region was successively invaded, a drop in haplotype diversity and changes in haplotype frequencies occurred indicating dispersal limitation across basin boundaries and founder effects within each basin. The lack of differentiation within regions indicates rapid population growth and unfettered dispersal within basins after initial colonization. We find no evidence of secondary invasions within samples. With well-established populations, the probability of detecting a secondary invasion is minuscule.
Similar content being viewed by others
References
Akins JL, Morris JA, Green SJ (2014) In situ tagging technique for fishes provides insight into growth and movement of invasive lionfish. Ecol Evol 4:3768–3777. doi:10.1002/ece3.1171
Beerli P, Palczewski M (2010) Unified framework to evaluate panmixia and migration direction among multiple sampling locations. Genetics 185:313–326. doi:10.1534/genetics.109.112532
Betancur RR, Hines A, Acero PA, Ortí G, Wilbur AE, Freshwater DW (2011) Reconstructing the lionfish invasion: insights into Greater Caribbean biogeography. J Biogeogr 38:1281–1293. doi:10.1111/j.1365-2699.2011.02496.x
Broughton RE, Stewart LB, Gold JR (2002) Microsatellite variation suggests substantial gene flow between king mackerel (Scomberomorus cavalla) in the western Atlantic Ocean and Gulf of Mexico. Fish Res 54:305–316. doi:10.1016/s0165-7836(01)00275-2
Butterfield JSS et al (2015) Wide-ranging phylogeographic structure of invasive red lionfish in the Western Atlantic and Greater Caribbean. Mar Biol 162:773–781. doi:10.1007/s00227-015-2623-y
Crow JF, Kimura M (1970) An introduction to population genetics theory. The Blackburn Press, Caldwell
Excoffier L, Ray N (2008) Surfing during population expansions promotes genetic revolutions and structuration. Trends Ecol Evol 23:347–351
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491
Ferreira CE, Luiz OJ, Floeter SR, Lucena MB, Barbosa MC, Rocha CR, Rocha LA (2015) First record of invasive lionfish (Pterois volitans) for the Brazilian Coast. PLoS ONE 10:e0123002. doi:10.1371/journal.pone.0123002
Fisher RA, Ford B (1950) The Sewall Wright effect. Heredity 4:117–119
Freshwater WD et al (2009) Mitochondrial control region sequence analyses indicate dispersal from the US East Coast as the source of the invasive Indo-Pacific lionfish Pterois volitans in the Bahamas. Mar Biol 156:1213–1221. doi:10.1007/s00227-009-1163-8
Gold J, Richardson L (1998) Mitochondrial DNA diversification and population structure in fishes from the Gulf of Mexico and Western Atlantic. J Hered 89:404–414
Hallatschek O, Nelson DR (2008) Gene surfing in expanding populations. Theor Popul Biol 73:158–170
Hallatschek O, Hersen P, Ramanathan S, Nelson DR (2007) Genetic drift at expanding frontiers promotes gene segregation. Proc Natl Acad Sci USA 104:19926–19930
Hamner RM, Freshwater DW, Whitfield PE (2007) Mitochondrial cytochrome b analysis reveals two invasive lionfish species with strong founder effects in the western Atlantic. J Fish Biol 71:214–222. doi:10.1111/j.1095-8649.2007.01575.x
Herke S, Foltz D (2002) Phylogeography of two squid (Loligo pealei and L. plei) in the Gulf of Mexico and northwestern Atlantic Ocean. Mar Biol 140:103–115. doi:10.1007/s002270100680
Karlsson S, Saillant E, Gold JR (2009) Population structure and genetic variation of lane snapper (Lutjanus synagris) in the northern Gulf of Mexico. Mar Biol 156:1841–1855. doi:10.1007/s00227-009-1217-y
Keeney DB, Heupel MR, Hueter RE, Heist EJ (2005) Microsatellite and mitochondrial DNA analyses of the genetic structure of blacktip shark (Carcharhinus limbatus) nurseries in the northwestern Atlantic, Gulf of Mexico, and Caribbean Sea. Mol Ecol 14:1911–1923. doi:10.1111/j.1365-294X.2005.02549.x
Morris JA, Shertzer KW, Rice JA (2010) A stage-based matrix population model of invasive lionfish with implications for control. Biol Invas 13:7–12. doi:10.1007/s10530-010-9786-8
Portnoy DS, Gold JR (2012) Evidence of multiple vicariance in a marine suture-zone in the Gulf of Mexico. J of Biogeogr 39:1499–1507. doi:10.1111/j.1365-2699.2012.02699.x
Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283
Schofield P (2009) Geographic extent and chronology of the invasion of non-native lionfish. Aquat Invas. doi:10.3391/ai.2009.4.3
Toledo-Hernández C (2014) Population ecology and genetics of the invasive lionfish in Puerto Rico. Aquat Invas 9:227–237. doi:10.3391/ai.2014.9.2.12
Wright S (1937) The distribution of gene frequencies in populations. Proc Natl Acad Sci USA 23:307–320
Acknowledgments
We thank the FGBNMS staff for help with collections and samples from the FGBNMS, and G. Palmer, A. Downey-Wall and J. Selwyn for collections and samples from Panama.
Funding
This study was funded by start up funds provided to JDH by Texas A&M University–Corpus Christi.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
All authors declare that they have no conflict of interest.
Ethical approval
All applicable international, national and/or institutional guidelines for the care and use of animals were followed. (IACUC protocol #05-14).
Additional information
Responsible Editor: T. Reusch.
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
Johnson, J., Bird, C.E., Johnston, M.A. et al. Regional genetic structure and genetic founder effects in the invasive lionfish: comparing the Gulf of Mexico, Caribbean and North Atlantic. Mar Biol 163, 216 (2016). https://doi.org/10.1007/s00227-016-2981-0
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-016-2981-0