Genetic structure of Mexican lionfish populations in the southwest Gulf of Mexico and the Caribbean Sea

Autoři: Elizabeth Labastida-Estrada aff001;  Salima Machkour-M’Rabet aff001;  Laura Carrillo aff002;  Yann Hénaut aff003;  Delma Nataly Castelblanco-Martínez aff004
Působiště autorů: Laboratorio de Ecología Molecular y Conservación, Departamento de Conservación de la Biodiversidad, El Colegio de la Frontera Sur, Chetumal, Quintana Roo, Mexico aff001;  Departamento de Sistemática y Ecología Acuática, El Colegio de la Frontera Sur, Chetumal, Quintana Roo, Mexico aff002;  Laboratorio de Conducta Animal, El Colegio de la Frontera Sur, Chetumal, Quintana Roo, Mexico aff003;  Consejo Nacional de Ciencia y Tecnología / Universidad de Quintana Roo, Chetumal, Quintana Roo, Mexico aff004
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article


The recent expansion of the invasive lionfish throughout the Western Hemisphere is one of the most extensively studied aquatic invasions. Molecular studies have improved our understanding of larval dispersal, connectivity, and biogeographical barriers among lionfish populations, but none have included Mexican localities, an important area for the larval dispersal of Pterois volitans through the Western Caribbean and the Gulf of Mexico. Here, we present a genetic analysis of lionfishes collected along Mexican coasts, examining their connectivity with other Caribbean localities (Belize, Cuba, Puerto Rico) and the role of ocean currents on population structure. We collected 213 lionfish samples from seven locations comprising four countries. To evaluate genetic structure, mitochondrial control region and nuclear inter-simple sequence repeat markers were used. We found that lionfish collected along Mexican coasts show a similar haplotype composition (H02 followed by H01 and H04) to other Caribbean locations, and the H03 rare haplotype was not found. Haplotype composition in the southwest Gulf of Mexico suggests a discontinuity between the southern and northern areas of the Gulf of Mexico. The southern area clustered more strongly to the Caribbean region, and this is supported by the complexity of water circulation in the semi-enclosed region of the Gulf of Mexico. Mitochondrial genetic diversity parameters show small values, whereas nuclear markers produce medium to high values. Only nuclear markers highlighted significant genetic differentiation between the southwest Gulf of Mexico and Caribbean region, confirming a phylogeographic break between both regions. Separate analysis of Caribbean locations indicates restricted larval exchange between southern and northern regions of the Mesoamerican Barrier Reef System, potentially in response to regional oceanographic circulation.

Klíčová slova:

Genetic loci – Haplotypes – Mexican people – Mitochondrial DNA – Phylogeography – Population genetics – Gulf of Mexico – Caribbean


1. Sala OE, Chapin FS, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, et al. Global biodiversity scenarios for the year 2100. Science. 2000; 287: 1770–1774. doi: 10.1126/science.287.5459.1770 10710299

2. Havel JE, Kovalenko KE, Thomaz SM, Amalfitano S, Kats LB. Aquatic invasive species: challenges for the future. Hydrobiologia. 2015; 750: 147–170.

3. Kolar CS, Lodge DM. Ecological predictions and risk assessment for alien fishes in North America. Science. 2002; 298: 1233–1236. doi: 10.1126/science.1075753 12424378

4. Hulme PE. Trade, transport and trouble: managing invasive species pathways in an era of globalization. J App Ecol. 2009; 46: 10–18.

5. Roman J, Darling JA. Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol. 2007; 22: 454–464. doi: 10.1016/j.tree.2007.07.002 17673331

6. Pérez-Portela R, Bumford A, Coffman B, Wedelich S, Davenport M, Fogg A. Genetic homogeneity of the invasive lionfish across the Northwestern Atlantic and the Gulf of Mexico based on Single Nucleotide Polymorphisms. Sci Rep. 2018; 1: 5062.

7. Hixon MA, Green SJ, Albins MA, Akins JL, Morris JA Jr. Lionfish: a major marine invasion. Mar Ecol Prog Ser. 2016; 558: 161–165.

8. Betancur-R R, Hines A, Acero AP, Ortí G, Wilbur AE, Freshwater DW. Reconstructing the lionfish invasion: insights into Greater Caribbean biogeography. J Biogeogr. 2011; 38: 1281–1293.

9. Butterfield JS, Díaz-Ferguson E, Silliman BR, Saunders JW, Buddo D, Mignucci-Giannoni AA, et al. Wide-ranging phylogeographic structure of invasive red lionfish in the Western Atlantic and Greater Caribbean. Mar Biol. 2015; 162: 773–781.

10. Sellers AJ, Ruiz GM, Leung B, Torchin ME. Regional variation in parasite species richness and abundance in the introduced range of the invasive lionfish, Pterois volitans. PLoS One. 2015; 10: e0131075. doi: 10.1371/journal.pone.0131075 26098309

11. Fogg AQ, Ruiz CF, Curran SS, Bullard SA. Parasites from the Red Lionfish, Pterois volitans from the Gulf of Mexico. Gulf Caribb Res. 2016; 27: SC1–SC5.

12. Malpica-Cruz L, Chaves LC, Côté IM. Managing marine invasive species through public participation: Lionfish derbies as a case study. Mar Policy. 2016; 74: 158–164.

13. García-Rivas MC, Machkour-M’Rabet S, Pérez Lachaud G, Schmitter-Soto JJ, Doneys C, St-Jean N, et al. What are the characteristics of lionfish and other fishes that influence their association in diurnal refuges? Mar Biol Res. 2017; 13: 899–908.

14. García-Rivas MC, Machkour-M’Rabet S, Pérez-Lachaud G, Schmitter-Soto JJ, Céréghino R, Doneys C, et al. Age-dependent strategies related to lionfish activities in the Mexican Caribbean. Environ Biol Fish. 2018; 101: 563–578.

15. Freshwater DW, Hines A, Parham S, Wilbur A, Sabaoun M, Woodhead J, et al. 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. 2009; 156: 1213–1221.

16. Schultz TF, Fitzpatrick CK, Freshwater DW, Morris JA. Characterization of 18 polymorphic microsatellite loci from invasive lionfish (Pterois volitans and P. miles). Conserv Genet Res. 2013; 5: 599–601.

17. Labastida E, Cobián D, Hénaut Y, García-Rivas MC, Chevalier PP, Machkour-M’Rabet S. The use of ISSR markers for species determination and a genetic study of the invasive lionfish in Guanahacabibes, Cuba. Lat Am J Aquat Res. 2015; 43: 1011–1018.

18. Del Río-Portilla MA, Vargas-Peralta CE, Machkour-M’Rabet S, Hénaut Y, García-De-León FJ. Lionfish, Pterois volitans Linnaeus 1758, the complete mitochondrial DNA of an invasive species. Mitochondrial DNA Part A. 2016; 27: 1423–1424.

19. Harms-Tuohy CA, Schizas NV, Appeldoorn RS. Use of DNA metabarcoding for stomach content analysis in the invasive lionfish Pterois volitans in Puerto Rico. Mar Ecol Prog Ser. 2016; 558: 181–191.

20. Méndez IAG, Rivera-Madrid R, Díaz-Jaimes P, Aguilar-Espinosa M, Arias-González JE. Applying an easy molecular method to differentiate Pterois volitans from Pterois miles by RFLPs. Conserv Genet Res. 2017; 9: 493–497.

21. Johnson J, Bird CE, Johnston MA, Fogg AQ, Hogan JD. Regional genetic structure and genetic founder effects in the invasive lionfish: comparing the Gulf of Mexico, Caribbean and North Atlantic. Mar Biol. 2016; 163: 216.

22. Jud ZR, Layman CA. Site fidelity and movement patterns of invasive lionfish, Pterois spp., in a Florida estuary. J Exp Mar Biol Ecol. 2012; 414: 69–74.

23. Keeney DB, Heupel MR, Hueter RE, Heist EJ. 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. 2005; 14: 1911–1923. doi: 10.1111/j.1365-294X.2005.02549.x 15910315

24. Machkour-M’Rabet S, Cruz-Medina J, García-De León FJ, De Jesús-Navarrete A, Hénaut Y. Connectivity and genetic structure of the queen conch on the Mesoamerican Reef. Coral Reefs. 2017a; 36: 535–548.

25. Sanvicente-Añorve L, Zavala-Hidalgo J, Allende-Arandía ME, Hermoso-Salazar M. Connectivity patterns among coral reef systems in the southern Gulf of Mexico. Mar Ecol Prog Ser. 2014; 498: 27–41.

26. Salas-Monreal D, Marin-Hernandez M, Salas-Perez JJ, Salas-de-Leon DA, Monreal-Gomez MA, Perez-España H. Coral reef connectivity within the Western Gulf of Mexico J Marine Syst. 2018; 179: 88–89.

27. Kitchens LL, Paris CB, Vaz AC, Ditty JG, Cornic M, Cowan JH, et al. Occurrence of invasive lionfish (Pterois volitans) larvae in the northern Gulf of Mexico: characterization of dispersal pathways and spawning areas. Biol Invasions. 2017; 19: 1971–1979.

28. Côté IM, Smith NS. The lionfish Pterois sp. invasion: Has the worst-case scenario come to pass? J Fish Biol. 2018; 92:660–689. doi: 10.1111/jfb.13544 29537091

29. Cowen RK, Sponaugle S. Larval dispersal and marine population connectivity. Ann Rev Mar Sci. 2009; 1: 443–66. doi: 10.1146/annurev.marine.010908.163757 21141044

30. Cowen RK. Oceanographic influences on larval dispersal and retention and their consequences for population connectivity. In: Sale PF, editor. Coral Reef Fishes. Academic Press, 2001. pp.149–170.

31. Carrillo L, Johns EM, Smith RH, Lamkin JT, Largier JL. Pathways and hydrography in the Mesoamerican Barrier Reef System part 1: circulation. Cont Shelf Res. 2015; 109: 164–176.

32. Sturges W, Lugo-Fernandez A. Circulation in the Gulf of Mexico: observations and models. Geophys Monogr Ser 161. Washington D.C: American Geophysical Union; 2005.

33. Badan A, Candela J, Sheinbaum J, Ochoa JO. Upper-Layer Circulation in the Approaches to Yucatan Channel. In: Sturges W, Lugo-Fernandez A, editors. Circulation in the Gulf of Mexico: Observations and Models. American Geophysical Union; 2005. pp. 57–69.

34. Briones-Fourzán P, Candela J, Lozano-Alvarez E. Postlarval settlement of the spiny lobster Panulirus argus along the Caribbean coast of Mexico: patterns, influence of physical factors, and possible sources of origin. Limnol Oceanog. 2008; 53: 970–985.

35. Cossu P, Dedola GL, Scarpa F, Sanna D, Lai T, Maltagliati F, et al. Patterns of spatial genetic variation in Patella ulyssiponensis: insights from the western Mediterranean marine ecoregion. Hydrobiologia. 2015; 755: 39–55.

36. Toledo-Hernández C, Vélez-Zuazo X, Ruiz-Diaz CP, Patricio AR, Mège P, Navarro M, et al. Population ecology and genetics of the invasive lionfish in Puerto Rico. Aquat Invasions. 2014; 9: 227–237.

37. Ng WL, Tan SG. Inter-simple sequence repeat (ISSR) markers: are we doing it right. ASM Sci J. 2015; 9:30–39.

38. Bonin A, Bellemain E, Bronken Eidesen P, Pompanon F, Brochmann C, Taberlet P. How to track and assess genotyping errors in population genetics studies. Mol Ecol. 2004; 13:3261–3273. doi: 10.1111/j.1365-294X.2004.02346.x 15487987

39. Pompanon F, Bonin A, Bellemain E, Taberlet P. Genotyping errors: causes, consequences and solutions. Nat Rev Genet. 2005; 6:847 doi: 10.1038/nrg1707 16304600

40. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004; 32: 1792–1797. doi: 10.1093/nar/gkh340 15034147

41. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013; 30: 2725–2729. doi: 10.1093/molbev/mst197 24132122

42. Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009; 25: 1451–1452. doi: 10.1093/bioinformatics/btp187 19346325

43. Excoffier L, Lischer HE. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res. 2010; 10: 564–567.

44. Rice WR, Analyzing tables of statistical tests. Evolution. 1989; 43:223–225. doi: 10.1111/j.1558-5646.1989.tb04220.x 28568501

45. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 2003; 52: 696–704. doi: 10.1080/10635150390235520 14530136

46. Darriba D, Taboada GL, Doallo R, Posada D. JModelTest 2: more models, new heuristics and parallel computing. Nat Methods. 2012; 9: 772–772.

47. Clement M, Posada D, Crandall KA. TCS: a computer program to estimate gene genealogies. Mol Ecol. 2000; 9: 1657–1660. doi: 10.1046/j.1365-294x.2000.01020.x 11050560

48. Foll M, Gaggiotti O. A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics. 2008; 180: 977–993. doi: 10.1534/genetics.108.092221 18780740

49. Yeh FC, Yang R, Boyle TJB. Population genetic analysis of co-dominant and dominant markers and quantitative traits. Belg J Bot. 1999; 129: 157.

50. Peakall R, Smouse PE. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes. 2006; 6: 288–295.

51. Peakall R, Smouse PE. GENALEX 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics. 2012; 28: 2537–2539. doi: 10.1093/bioinformatics/bts460 22820204

52. Luque C, Legal L, Staudter H, Gers C, Wink M. ISSR (Inter Simple Sequence Repeats) as genetic markers in Noctuids (Lepidoptera). Hereditas. 2002; 136: 251–253. doi: 10.1034/j.1601-5223.2002.1360312.x 12471674

53. Maltagliati F, Lai Y, Casu M, Valdesalici S, Castelli A. Identification of endangered Mediterranean cyprinodontiform fish by means of DNA inter-simple sequence repeats (ISSRs). Biochem. Syst. Ecol. 2006; 34: 626–634.

54. Casu M, Lai T, Curini-Galletti M, Ruiu A, Pais A. Identification of Mediterranean Diplodus spp. and Dentex dentex (Sparidae) by means of DNA inter-simple sequence repeat (ISSR) markers. J Exp Mar Biol Ecol. 2009; 368: 147–152.

55. Vázquez De La Cerda AM, Reid RO, DiMarco SF, Jochens AE. Bay of Campeche circulation: An update. In: Sturges W, Lugo-Fernandez A, editors. Circulation in the Gulf of Mexico: Observations and Models. American Geophysical Union; 2005. pp. 279–293.

56. Schmitz WJ, Biggs DC, Lugo‐Fernandez A, Oey LY, Sturges W. A synopsis of the circulation in the Gulf of Mexico and on its continental margins. In: Sturges W, Lugo-Fernandez A, editors. Circulation in the Gulf of Mexico: Observations and Models. American Geophysical Union; 2005. pp. 11–29.

57. Carrillo L, Horta-Puga G, Carricart-Ganivet JP. Climate and oceanography. In: Tunnell JW Jr, Chávez EA, Withers K, editors. Coral reefs of the southern Gulf of Mexico. Texas A&M University Press; 2007. pp. 34–40.

58. Zavala-Hidalgo J, Morey SL, O’Brien JJ. Seasonal circulation on the western shelf of the Gulf of Mexico using a high‐resolution numerical model. J Geophys Res-Oceans. 2003; 108: 3389.

59. Nybom H. Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Mol Ecol. 2004; 13: 1143–1155. doi: 10.1111/j.1365-294X.2004.02141.x 15078452

60. Santander-Monsalvo J, López-Huerta I, Aguilar-Perera A, Tuz-Sulub A. First record of the red lionfish (Pterois volitans [Linnaeus, 1758]) off the coast of Veracruz, Mexico. Bioinvasions Rec. 2012; 1: 121–124.

61. Machkour-M’Rabet S, Henaut Y, Calmé S, Legal L. When landscape modification is advantageous for protected species. The case of synanthropic tarantula, Brachypelma vagans. J Insect Conserv. 2012; 16: 479–488.

62. Aguilar-Perera A, Tuz-Sulub A. Non-native, invasive red lionfish (Pterois volitans [Linnaeus, 1758]: Scorpaenidae), is first recorded in the southern Gulf of Mexico, off the northern Yucatan Peninsula, Mexico. Aquat Invasions. 2010; 5: S9–S12.

63. Casu M, Rivera-Ingraham GA, Cossu P, Lai T, Sanna D, Dedola GL, et al. Patterns of spatial genetic structuring in the endangered limpet Patella ferruginea: implications for the conservation of a Mediterranean endemic. Genetica. 2011; 139: 1293–1308. doi: 10.1007/s10709-012-9631-3 22286933

64. Karl SA, Toonen RJ, Grant WS, Bowen BW. Common misconceptions in molecular ecology: echoes of the modern synthesis. Mol Ecol. 2012; 21:4171–4189. doi: 10.1111/j.1365-294X.2012.05576.x 22574714

65. Labastida-Estrada E, Machkour-M’Rabet S, Díaz-Jaimes P, Cedeño-Vázquez JR, Hénaut Y. Genetic structure, origin, and connectivity between nesting and foraging areas of hawksbill turtles of the Yucatan Peninsula. A study for conservation and management. Aquat Conserv. 2019; 29: 211–222.

66. Carricart-Ganivet JP. Sea surface temperature and the growth of the West Atlantic reef-building coral Montastraea annularis. J. Exp. Mar. Biol. Ecol. 2004; 302: 249–260.

67. Gasmi S, Ferval M, Pelissier C, D’amico F, Maris T, Tackx M, et al. Genetic diversity among the Eurytemora affinis species complex in the Scheldt estuary and its tributaries using ISSR-PCR marker assay. Estuar Coastal Shelf Sci. 2014; 145: 22–30.

68. Machkour-M’Rabet S, Vilchis-Nestor CA, Barriga-Sosa IDLA, Legal L, Hénaut Y. A molecular approach to understand the riddle of the invasive success of the tarantula, Brachypelma vagans, on Cozumel Island, Mexico. Biochem Syst Ecol. 2017b; 70: 260–267.

69. Sheinbaum J, Athié G, Candela J, Ochoa J, Romero-Arteaga A. (2016). Structure and variability of the Yucatan and Loop Currents along the slope and shelf break of the Yucatan Channel and Campeche Bank. Dynam Atmos Oceans; 76: 217–239.

70. Vásquez-Yeomans L, Carrillo L, Morales S, Malca E, Morris JA, Schultz T, et al. First larval record of Pterois volitans (Pisces: Scorpaenidae) collected from the ichthyoplankton in the Atlantic. Biol invasions. 2011; 13: 2635–2640.

71. Carrillo L, Johns EM, Smith RH, Lamkin JT, Largier JL. Pathways and hydrography in the Mesoamerican Barrier Reef System part 2: Water masses and thermohaline structure. Cont Shelf Res. 2016; 120: 41–58.

72. Martínez S, Carrillo L, Marinone SG. Potential connectivity between marine protected areas in the Mesoamerican Reef for two species of virtual fish larvae: Lutjanus analis and Epinephelus striatus. Ecol Indic. 2019; 102: 10–20.

73. Shanks AL. Pelagic larval duration and dispersal distance revisited. Biol Bull. 2009; 216: 373–385. doi: 10.1086/BBLv216n3p373 19556601

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