The genomics of invasion: characterization of red lionfish (Pterois volitans) populations from the native and introduced ranges

  • M. O. Burford ReiskindEmail author
  • E. M. X. Reed
  • A. Elias
  • J. J. Giacomini
  • A. F. McNear
  • J. Nieuwsma
  • G. A. Parker
  • R. B. Roberts
  • R. E. Rossi
  • C. N. Stephenson
  • J. L. Stevens
  • B. E. Williams
Original Paper


Invasive species are one of the greatest threats to global biodiversity and ecosystem health, and population genetics provides promising tools for understanding the evolutionary process of successful invaders. The well-documented introduction of the red lionfish (Pterois volitans) to the western Atlantic, Gulf of Mexico and Caribbean has decimated native fauna due to the invader’s voracious predation and growth rate. We tested whether our samples were within the region of the source of invasion into the Atlantic and Caribbean and investigated whether hybridization in the native or introduced range was responsible for the success of this invasive species. We used a reduced representation sequencing method to generate over 50,000 single nucleotide polymorphisms and sequence data from two mitochondrial DNA genes to analyze the population patterns. We found one location in the southeastern Pacific that was genetically similar to one location the southwestern Atlantic and evidence of the subsequent spread south to the Gulf of Mexico and the Caribbean, which supports previous findings. Within the native range, we found genetic divergences commensurate with distinct species and evidence of hybridization. We found limited structure within the introduced range and no evidence of Pterois miles or hybrids within this range. Finally, we found signatures of selection between the native and introduced range that may be a result of the introduction. Overall, this study of the red lionfish showed the pattern of introduction and suggested a deeper sampling of genomic data from individuals within the native range may reveal hybridization between species as the source of the aggressive invasion.


Invasion Hybridization Red lionfish Pterois volitans Pterois miles ddRADseq 



We thank M.R. Reiskind and R.R. Dunn for comments on an early version of this manuscript and several anonymous reviewers for their comments that improved this manuscript. The Wynne Innovation Grant from the CALS Dean’s Enrichment Grant program at NCSU awarded to MO Burford Reiskind funded this research. We also thank both the Applied Ecology and Entomology and Plant Pathology Departments at NCSU for providing matching funds to further fund this collaborative research. This study was a project in MO Burford Reiskind’s Conservation Genetics course at NCSU for undergraduate and graduate students.

Data Accessibility

We provided supplemental material with the original submission for the online version of this manuscript. This will include the results of the Genbank blast search for outlier loci. Data from this manuscript will be available through Dr. Martha Burford Reiskind’s DRYAD account. This will include post-STACK analysis input data files for PGDSpider from which subsequent input data files can be generated. The complete list of aligned sequences containing outlier loci. In addition, the raw sequence data generated in this study will be available upon request, as the data files far exceed the limits at DRYAD without addition payment.

Supplementary material

10530_2019_1992_MOESM1_ESM.docx (119 kb)
Supplementary material 1 (DOCX 118 kb)
10530_2019_1992_MOESM2_ESM.xlsx (22 kb)
Supplementary material 2 (XLSX 22 kb)
10530_2019_1992_MOESM3_ESM.jpg (73 kb)
Supplementary material 3 (JPEG 73 kb)


  1. Ahrenholz DW, Morris JA Jr (2010) Larval duration of the lionfish, Pterois volitans along the Bahamian Archipelago. Environ Biol Fish 88:305–309. CrossRefGoogle Scholar
  2. Albins MA (2015) Invasive Pacific lionfish Pterois volitans reduce abundance and species richness of native Bahamian coral-reef fishes. Mar Ecol Prog Ser 522:231–243. CrossRefGoogle Scholar
  3. Albins MA, Hixon MA (2008) Invasive Indo–Pacific lionfish Pterois volitans reduce recruitment of Atlantic coral-reef fishes. Mar Ecol Prog Ser 367:233–238. CrossRefGoogle Scholar
  4. Allendorf FW, Lundquist LL (2003) Introduction: population biology, evolution, and control of invasive species. Con Biol 17:24–30CrossRefGoogle Scholar
  5. Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Genet 11:697–709. CrossRefGoogle Scholar
  6. Allendorf FW, Luikart G, Aitkin SN (2013) Conservation and the genetics of populations, 2nd edn. Blackwell, LondonGoogle Scholar
  7. Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G (2008) LOSITAN: a workbench to detect molecular adaptation based on a Fst -outlier method. BMC Bioinform 9:323. CrossRefGoogle Scholar
  8. Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proc R Soc Lond B Biol Sci 263:1619–1626. CrossRefGoogle Scholar
  9. Benkwitt CE, Albins MA, Buch KL, Ingeman KE, Kindinger TL, Pusack TJ, Stallings CD, Hixon MA (2017) Is the lionfish invasion waning? Evidence from The Bahamas. Coral Reefs 36:1255–1261. CrossRefGoogle Scholar
  10. Bernardi G, Azzurro E, Golani D, Miller MR (2016) Genomic signatures of rapid adaptive evolution in the bluespotted cornetfish, a Mediterranean Lessepsian invader. Mol Ecol 25:3384–3396. CrossRefGoogle Scholar
  11. Betancu-R R, Hines A, Acero AP, Orti G, Wilbur AE, Freshwater DW (2011) Reconstructiong the lionfish invasion: insights into Greater Caribbean biogeography. J Biogeogr 38:11281–11293. Google Scholar
  12. Bouzat J (2010) Conservation genetics of population bottlenecks: the role of chance, selection, and history. Conserv Genet 11:463–478. CrossRefGoogle Scholar
  13. Burford Reiskind MO, Coyle K, Daniels HV et al (2016) Development of a universal double-digest RAD sequencing approach for a group of nonmodel, ecologically and economically important insect and fish taxa. Mol Ecol Resour 16:1303–1314. CrossRefGoogle Scholar
  14. Burford Reiskind MO, Labadie P, Bargielowski I, Lounibos LP, Reiskind MH (2018) Rapid evolution and the genomic consequences of selection against interspecific mating. Mol Ecol. Google Scholar
  15. Butterfield JSS, Díaz-Ferguson E, Silliman BR et al (2015) Wide-ranging phylogeographic structure of invasive red lionfish in the Western Atlantic and Greater Caribbean. Mar Biol 162:773–781. CrossRefGoogle Scholar
  16. Catchen JM, Amores A, Hohenlohe P et al (2011) Stacks: building and genotyping Loci De Novo from short-read sequences. G3 Genes Genom Genet 1:171–182. Google Scholar
  17. Courtenay WR (1995) Marine fish introductions in southeastern Florida. Am Fish Soc Introd Fish Newsl 14:2–3. Google Scholar
  18. Cowen RK, Paris CB, Srinivasan A (2006) Scaling of connectivity in marine populations. Science 311:522–527. CrossRefGoogle Scholar
  19. Cure K, McIlwain JL, Hixon MA (2014) Habitat plasticity in native Pacific red lionfish Pterois volitans facilitates successful invasion of the Atlantic. Mar Ecol Prog Ser 506:243–253. CrossRefGoogle Scholar
  20. Earl DA, Vonholdt BA (2012) Structure Harvester: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. CrossRefGoogle Scholar
  21. Feng K, Luo H, Hou M, Li Y, Chen J, Zhu Z, Hu W (2018) Alternative splicing of GnRH2 and GnRH2-associated peptide plays roles in gonadal differentiation in the rice field eel, Monopterus albus. Gen Comp Endocrinol. Google Scholar
  22. Ferreira CEL, 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 10:1–5. Google Scholar
  23. Fitzpatrick BM, Shaffer HB (2007) Hybrid vigor between native and introduced salamanders raises new challenges for conservation. Proc Natl Acad Sci 104:15793–15798. CrossRefGoogle Scholar
  24. Frankham R (2005) Resolving the genetic paradox in invasive species. Heredity 94:385CrossRefGoogle Scholar
  25. Freshwater DW, Hines A, Parham S, Wilbur A, Sabaoun M, Woodhead J, Akins L, Purdy B, Whitfield PA, Paris CB (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. CrossRefGoogle Scholar
  26. Gaither MR, Bernal MA, Coleman RR, Bowen BW, Jones SA, Simison WB, Rocha LA (2015) Genomic signatures of geographic isolation and natural selection in coral reef fishes. Mol Ecol 24:1543–1557. CrossRefGoogle Scholar
  27. Grosholz ED, Ruiz GM, Dean CA, Shirley KA, Maron JL, Connors PG (2000) The impacts of a nonindigenous marine predator in a California bay. Ecology 81:1206–1224.;2 CrossRefGoogle Scholar
  28. 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. CrossRefGoogle Scholar
  29. 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. CrossRefGoogle Scholar
  30. Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. CrossRefGoogle Scholar
  31. Jud ZR, Layman CA (2012) Site fidelity and movement patterns of invasive lionfish, Pterois spp., in a Florida estuary. J Exp Mar Biol Ecol 414–415:69–74. CrossRefGoogle Scholar
  32. Kearse M, Moir R, Wilson A et al (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649CrossRefGoogle Scholar
  33. Kocher TD, Thomas WK, Meyer A et al (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci 86:6196–6200. CrossRefGoogle Scholar
  34. Kochzius M, Soller R, Khalaf MA, Blohm D (2003) Molecular phylogeny of the lionfish genera Dendrochirus and Pterois (Scorpeanidae, Pteroinae) based on mitochondrial DNA sequences. Mol Phylogenetics Evol 28:396–403CrossRefGoogle Scholar
  35. Kolbe JJ, Glor RE, Schettino LR, Lara AC, Larson A, Losos JB (2004) Genetic variation increases during biological invasion by Cuban lizard. Nature 431:177–181CrossRefGoogle Scholar
  36. Kulbicki M, Beets J, Chabanet P, Cure K, Darling E, Floeter SR, Galzin R, Green A, Harmelin-Vivien M, Hixon M, Letourneur Y, de Loma TL, McClanahan T, McIlwain J, MouTham G, Myers R, O’Leary JK, Planes S, Vigliola L, Wantiez L (2012) Distributions of Indo–Pacific lionfishes Pterois spp. in their native ranges: implications for the Atlantic invasion. Mar Ecol Prog Ser 446:189–205. CrossRefGoogle Scholar
  37. Layman CA, Allgeier JE (2012) Characterizing trophic ecology of generalist consumers: a case study of the invasive lionfish in The Bahamas. Mar Ecol Prog Ser 448:131–141. CrossRefGoogle Scholar
  38. Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391CrossRefGoogle Scholar
  39. Lischer HEL, Excoffier L (2012) PGDSpider: an automated data conversion tool for connecting population genetics and genomics programs. Bioinformatics 28:298–299. CrossRefGoogle Scholar
  40. Maximino C, Lima MG, Olivera KR et al (2011) Adenosine A1 but not A2, receptor blockade increases anxiety and arousal in zebrafish. Basic Clin Pharmacol Toxicol 109:203–207CrossRefGoogle Scholar
  41. Meyer A, Kocher TD, Basasibwaki P, Wilson AC (1990) Monophyletic origin of Lake Victoria cichlid fishes suggested by mitochondrial DNA sequences. Nature 347:550–553CrossRefGoogle Scholar
  42. Meyer A, Morrissey JM, Schartl M (1994) Recurrent origin of a sexually selected trait in Xiphophorus fishes inferred from a molecular phylogeny. Nature 368:539–542CrossRefGoogle Scholar
  43. Morris JA, Akins JL (2009) Feeding ecology of invasive lionfish (Pterois volitans) in the Bahamian archipelago. Environ Biol Fish 86:389. CrossRefGoogle Scholar
  44. Muhlfeld CC, Kalinowski ST, McMahon TE, Taper ML et al (2009) Hybridization rapidly reduces fitness of a native trout in the wild. Biol Lett 5:328–331CrossRefGoogle Scholar
  45. Murray TF, Siebenaller JF (1987) Comparison of the binding properties of A1 adenosine receptors in brain membranes of two congeneric marine fishes living at different depths. J Comp Physiol B Biochem Syst Environ Physiol 157:267–277. CrossRefGoogle Scholar
  46. Nishiguchi R, Azuma M, Yokobori E et al (2012) Gonadotropin-releasing hormone 2 suppresses food intake in the zerbrafish, Danio rerio. Front Endocrinol 3:1–6CrossRefGoogle Scholar
  47. Nolte AW, Freyhof J, Stemshorn KC, Tautz D (2005) An invasive lineage of sculpins, Cottus sp. (Pisces, Teleostei) in the Rhine with new habitat adaptations has originated from hybridization between old phylogeographic groups. Proc R Soc B 272:2379–2387CrossRefGoogle Scholar
  48. Palumbi SR (1996) Nucleic Acids II: the polymerase chain reaction. In: Hillis DM, Moritz C, Mable BK (eds) Molecular systematics, 2nd edn. Sinauer, Sunderland, pp 205–247Google Scholar
  49. Pérez-Portela R, Buford A, Coffman B, Wedelich S, Davenport M, Fogg A, Swenarton MK, Coleman F, Johnston MA, Crawford DL, Oleksiak MF (2018) Genetic homogeneity of the invasive lionfish across the Northwestern Atlantic and the Gulf of Mexico based on single nucleotide polymorphisms. Sci Rep 8:5062. CrossRefGoogle Scholar
  50. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959Google Scholar
  51. Rousset F (2008) genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106. CrossRefGoogle Scholar
  52. Schierenbeck KA, Ellstrand NC (2009) Hybridization and the evolution of invasiveness in plants and other organisms. Biol Invasions 11:1093–1105CrossRefGoogle Scholar
  53. Schofield PJ (2009) Geographic extent and chronology of the invasion of non-native lionfish (Pterois volitans [Linnaeus 1758] and P. miles [Bennett 1828]) in the Western North Atlantic and Caribbean Sea. Aquat Invasions 4:473–479. CrossRefGoogle Scholar
  54. Selwyn JD, Johnson JE, Downey-Wall AM, Bynum AM, Hamner RM, Hogan JD, Bird CE (2017) Simulations indicate that scores of lionfish (Pterois volitans) colonized the Atlantic Ocean. PeerJ 5:e3996. CrossRefGoogle Scholar
  55. Shiganova TA (1998) Invasion of the Black Sea by the Ctenophore Mnemiopsis leidyi and recent changes in pelagic community structure. Fish Oceanogr 7:305–310. CrossRefGoogle Scholar
  56. Toledo-Hernandez C (2014) Population ecology and genetics of the invasive lionfish in Puerto Rico. Aquat Invasions 9:227–237. CrossRefGoogle Scholar
  57. Wakisaka N, Miyasaka N, Koide T et al (2017) An adenosine receptor for olfaction in fish. Curr Biol 27:1437–1447.e4. CrossRefGoogle Scholar
  58. Walker BH, Steffen W (1997) An overview of the implications of global change for natural and mangaged terrestrial ecosystems. Conserv Ecol 2(2).
  59. Whitfield PE, Gardner T, Vives SP, Gilligan MR, Courtenay WR Jr, Ray GC, Hare JA (2002) Biological invasion of the Indo-Pacific lionfish Pterois volitans along the Atlantic coast of North America. Mar Ecol Prog Ser 235:289–297. CrossRefGoogle Scholar
  60. Wilcox CL, Motomura H, Matsunuma M, Bowen BW (2017) Phylogeography of lionfishes (Pterois) indicate taxonomic over splitting and hybrid origin of the invasive Pterois volitans. J Hered 109:162–175. CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • M. O. Burford Reiskind
    • 1
    Email author
  • E. M. X. Reed
    • 1
  • A. Elias
    • 2
  • J. J. Giacomini
    • 1
  • A. F. McNear
    • 1
  • J. Nieuwsma
    • 2
  • G. A. Parker
    • 2
    • 3
  • R. B. Roberts
    • 2
    • 3
  • R. E. Rossi
    • 1
  • C. N. Stephenson
    • 2
  • J. L. Stevens
    • 1
  • B. E. Williams
    • 2
  1. 1.Department of Applied EcologyNorth Carolina State UniversityRaleighUSA
  2. 2.Department of Biological SciencesNorth Carolina State UniversityRaleighUSA
  3. 3.WM Keck Center for Behavioral BiologyNorth Carolina State UniversityRaleighUSA

Personalised recommendations