Diversification and gene flow of tilapia species driven by ecological changes in lowland and mountain areas of southern Mauritania

  • Jolita Dilytė
  • Stephen Sabatino
  • Raquel Godinho
  • José Carlos BritoEmail author
Natural History Notes


Haplotilapiine are members of Cichlidae (cichlid fishes), one of the most species-rich vertebrate families. Many haplotilapiines diversified via allopatric divergence, sexual selection, hybridization and ecological adaptation, making them excellent models for evolutionary research. One extraordinary example of how haplotilapiine diversified are the species found within the Sahara desert, surviving in isolated wetlands for thousands of years. Seasonal, and longer, climate cycles in these areas have resulted in periods of connectivity and isolation within and between lowland and mountain regions via ephemeral rivers, which highly impacts the potential for migration of water-species. Here we studied how ecological variability and secondary contact have affected the population genetics of haplotilapiine cichlid fishes (Sarotherodon galilaeus), in the lowland Karakoro sub-basin and highland Afollé mountain regions of Mauritania. We used DNA-sequence data of mitochondrial (ND2, N = 59) and nuclear (S7 1st intron, N = 32) genes, and microsatellite markers data (13 novel loci developed for Sarotherodon, N = 61). Our results based on microsatellite data showed two genetically differentiated lowland groups of S. galilaeus that exist in sympatry. Absence of one of these groups in mountain areas can be due to small sample size or local extinction. We found no significant genetic differentiation between lowland and mountain based on microsatellite and mtDNA data, supporting our hypothesis of recent, downstream gene flow. As expected, genetic diversity was significantly lower in mountain population, which can be due to different factors, including stochastic effects or downstream migration increasing diversity via gene flow. Ecological changes (seasonal and long-term) have likely driven divergence and posterior secondary contacts on the studied Sarotherodon lineages at multiple times, leaving open questions for future studies about the specifics of these evolutionary processes. Moreover, the pattern of genetic diversity in lowland and mountain populations highlights the importance of protecting geographically isolated areas for long-term persistence of tilapia species.


Cichlid fishes Haplotilapiine Genetic diversity Divergence Secondary contact 



This work was made in memory of Professor Paulo Alexandrino who was for us a mentor, an inspiration and a very good friend. We thank AS Sow, DV Gonçalves, JC Campos, N Sillero, and P Tarroso for sampling support. Acknowledgements to S Lopes, DV Gonçalves, FMS Martins, JC Campos and P Pereira for lab assistance, data analysis and figure building. Funding provided by National Geographic Society (CRE-8412-08), Mohammed bin Zayed Species Conservation Fund (11052709, 11052707), Fundação para a Ciência e Tecnologia (FCT: PTDC/BIA-BEC/099934/2008, PTDC/BIA-BIC/2903/2012), FEDER through COMPETE-Operational Programme for Competitiveness Factors (FCOMP-01-0124-FEDER-008917, -028276), and by AGRIGEN–NORTE-01-0145-FEDER-000007, supported by Norte Portugal Regional Operational Programme (NORTE2020), under the PORTUGAL 2020 Partnership Agreement, through the European Regional Development Fund (ERDF). Individual support given by FCT (IF/459/2013 and IF/00564/2012). Logistic support for fieldwork was given by SMO Lehlou (Ministère de l’Environnement et du Développement Durable of Mauritania), D Hamidou (University of Nouakchott), and A Araújo (MAVA Foundation).

Supplementary material

10682_2019_10017_MOESM1_ESM.docx (6.5 mb)
Supplementary material 1 (DOCX 6614 kb)


  1. Anderson E, Stebbins G (1954) Hybridization as an evolutionary stimulus. Evolution 8:378–388CrossRefGoogle Scholar
  2. Baena-Díaz F, Ramírez-Barahona S, Ornelas JF (2018) Hybridization and differential introgression associated with environmental shifts in a mistletoe species complex. Sci Rep 8:5591CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bandelt H-J, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bell MA, Travis MP (2005) Hybridization, transgressive segregation, genetic covariation, and adaptive radiation. Trends Ecol Evol 20:358–361CrossRefPubMedPubMedCentralGoogle Scholar
  5. Beveridge MC, McAndrew BJ (2000) Tilapias: biology and exploitation. Springer, New YorkCrossRefGoogle Scholar
  6. Brawand D, Wagner CE, Li YI, Malinsky M, Keller I, Fan S, Simakov O, Ng AY, Lim ZW, Bezault E (2014) The genomic substrate for adaptive radiation in African cichlid fish. Nature 513:375CrossRefPubMedPubMedCentralGoogle Scholar
  7. Brito JC, Godinho R, Martínez-Freiría F, Pleguezuelos JM, Rebelo H, Santos X, Vale CG, Velo-Antón G, Boratyński Z, Carvalho SB, Ferreira S, Gonçalves DV, Silva TL, Tarroso P, Campos JC, Leite JV, Nogueira J, Álvares F, Sillero N, Sow AS, Fahd S, Crochet P-A, Carranza S (2014) Unravelling biodiversity, evolution and threats to conservation in the Sahara-Sahel. Biol Rev 89:215–231CrossRefPubMedPubMedCentralGoogle Scholar
  8. Chow S, Hazama K (1998) Universal PCR primers for S7 ribosomal protein gene introns in fish. Mol Ecol 7:1255–1256PubMedPubMedCentralGoogle Scholar
  9. Clavero M, Esquivias J, Qninba A, Riesco M, Calzada J, Ribeiro F, Fernández N, Delibes M (2015) Fish invading deserts: non-native species in arid Moroccan rivers. Aquat Conserv 25:49–60CrossRefGoogle Scholar
  10. Cooper A, Shine T, McCann T, Tidane D (2006) An ecological basis for sustainable land use of Eastern Mauritanian wetlands. J Arid Environ 67:116–141CrossRefGoogle Scholar
  11. D’Amato ME, Esterhuyse MM, Van Der Waal BC, Brink D, Volckaert FA (2007) Hybridization and phylogeography of the Mozambique tilapia Oreochromis mossambicus in southern Africa evidenced by mitochondrial and microsatellite DNA genotyping. Conserv Genet 8:475–488CrossRefGoogle Scholar
  12. Dunz AR, Schliewen UK (2013) Molecular phylogeny and revised classification of the haplotilapiine cichlid fishes formerly referred to as “Tilapia”. Mol Phylogenet Evol 68:64–80CrossRefPubMedPubMedCentralGoogle Scholar
  13. Earl DA (2012) Structure harvester: a website and program for visualizing Structure output and implementing the Evanno method. Conserv Genet Resour 4:359–361CrossRefGoogle Scholar
  14. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software Structure: a simulation study. Mol Ecol 14:2611–2620CrossRefGoogle Scholar
  15. Ford AGP, Bullena TR, Panga L, Gennerc MJ, Billsd R, Flouria T, Ngatungae BP, Ruberf L, Schliewenh UK, Seehauseng O, Shechongee A, Stiassnyk MLJ, Turnerl GF, Day JJ (2019) Molecular phylogeny of Oreochromis (Cichlidae: Oreochromini) reveals mito-nuclear discordance and multiple colonisation of adverse aquatic environments. Mol Phylogenet Evol 136:215–226CrossRefPubMedPubMedCentralGoogle Scholar
  16. Franck J, Wright JM, McAndrew B (1992) Genetic variability in a family of satellite DNAs from tilapia (Pisces: Cichlidae). Genome 35:719–725CrossRefPubMedPubMedCentralGoogle Scholar
  17. Franck JP, Kornfield I, Wright JM (1994) The utility of SATA satellite DNA sequences for inferring phylogenetic relationships among the three major genera of tilapiine cichlid fishes. Mol Phylogenet Evol 3:10–16CrossRefPubMedPubMedCentralGoogle Scholar
  18. Fryer G, Iles T (1969) Alternative routes to evolutionary success as exhibited by African cichlid fishes of the genus Tilapia and the species flocks of the Great Lakes. Evolution 23:359–369CrossRefPubMedPubMedCentralGoogle Scholar
  19. Gasse F (2000) Hydrological changes in the African tropics since the Last Glacial Maximum. Quat Sci Rev 19:189–211CrossRefGoogle Scholar
  20. Godinho R, López-Bao JV, Castro D, Llaneza L, Lopes S, Silva P, Ferrand N (2015) Real-time assessment of hybridization between wolves and dogs: combining noninvasive samples with ancestry informative markers. Mol Ecol Res 15:317–328CrossRefGoogle Scholar
  21. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9. 3). Accessed 3 Mar 2014
  22. Hillis DM, Moritz C, Mable BK (1996) Molecular systematics. Sinauer Associates, SuderlandGoogle Scholar
  23. Holmes JA (2008) How the Sahara became dry. Science 320:752–753CrossRefPubMedPubMedCentralGoogle Scholar
  24. Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Res 9:1322–1332CrossRefGoogle Scholar
  25. Kide NG, Dunz A, Agnèse JF, Dilyte J, Pariselle A, Carneiro C, Correia E, Brito JC, Yarba LO, Kone Y, Durand JD (2016) Cichlids of the Banc d’Arguin National Park, Mauritania: insight into the diversity of the genus Coptodon. J Fish Biol 88:1369–1393CrossRefPubMedPubMedCentralGoogle Scholar
  26. Klett V, Meyer A (2002) What, if anything, is a Tilapia? Mitochondrial ND2 phylogeny of tilapiines and the evolution of parental care systems in the African cichlid fishes. Mol Biol Evol 19:865–883CrossRefPubMedPubMedCentralGoogle Scholar
  27. Kocher TD (2004) Adaptive evolution and explosive speciation: the cichlid fish model. Nat Rev Genet 5:288–298CrossRefPubMedPubMedCentralGoogle Scholar
  28. Kornfield I, Ritte U, Richler C, Wahrman J (1979) Biochemical and cytological differentiation among cichlid fishes of the Sea of Galilee. Evolution 33:1–14CrossRefPubMedPubMedCentralGoogle Scholar
  29. Kröpelin S, Verschuren D, Lézine A-M, Eggermont H, Cocquyt C, Francus P, Cazet J-P, Fagot M, Rumes B, Russell J (2008) Climate-driven ecosystem succession in the Sahara: the past 6000 years. Science 320:765–768CrossRefPubMedPubMedCentralGoogle Scholar
  30. Leigh J, Bryant D (2015) POPART: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116CrossRefGoogle Scholar
  31. Lévêque C (1990) Relict tropical fish fauna in Central Sahara. Ichthyol Explor Freshw 1:39–48Google Scholar
  32. Liem KF (1973) Evolutionary strategies and morphological innovations: cichlid pharyngeal jaws. Syst Zool 22:425–441CrossRefGoogle Scholar
  33. Lowe RH (1955) Species of Tilapia in East African dams, with a key for their identification. East Afr Agric For J 20:256–262Google Scholar
  34. Marsjan P, Oldenbroek J (2007) Molecular markers, a tool for exploring gene diversity. In: Pilling D, Rischkowsky B (eds) The state of the world’s animal genetic resources for food and agriculture. FAO, Rome, pp 359–379Google Scholar
  35. McAndrew B, Majumdar K (1984) Evolutionary relationships within three Tilapiine genera (Pisces: Cichlidae). Zool J Linn Soc 80:421–435CrossRefGoogle Scholar
  36. Nevado B, Fazalova V, Backeljau T, Hanssens M, Verheyen E (2011) Repeated unidirectional introgression of nuclear and mitochondrial DNA between four congeneric Tanganyikan cichlids. Mol Biol Evol 28:2253–2267CrossRefGoogle Scholar
  37. Park S (2001) The excel microsatellite toolkit (version 3.1). Animal Genomics Laboratory, UCD, IrelandGoogle Scholar
  38. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  39. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  40. Rambaut A, Drummond A (2009) Tracer: MCMC trace analysis tool, version 1.5. Accessed 3 Mar 2014
  41. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249CrossRefGoogle Scholar
  42. Rozas J, Rozas R (1995) DnaSP, DNA sequence polymorphism: an interactive program for estimating population genetics parameters from DNA sequence data. Comput Appl Biosci 11:621–625PubMedPubMedCentralGoogle Scholar
  43. Salzburger W, Baric S, Sturmbauer C (2002) Speciation via introgressive hybridization in East African cichlids? Mol Ecol 11:619–625CrossRefPubMedPubMedCentralGoogle Scholar
  44. Schwarzer J, Misof B, Tautz D, Schliewen UK (2009) The root of the East African cichlid radiations. BMC Evol Biol 9:186CrossRefPubMedPubMedCentralGoogle Scholar
  45. Sodsuk P, McAndrew B (1991) Molecular systematics of three tilapüne genera Tilapia, Sarotherodon and Oreochromis using allozyme data. J Fish Biol 39:301–308CrossRefGoogle Scholar
  46. Stephens M, Donnelly P (2003) A comparison of bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet 73:1162–1169CrossRefPubMedPubMedCentralGoogle Scholar
  47. Streelman JT, Gmyrek S, Kidd M, Kidd C, Robinson R, Hert E, Ambali A, Kocher T (2004) Hybridization and contemporary evolution in an introduced cichlid fish from Lake Malawi National Park. Mol Ecol 13:2471–2479CrossRefPubMedPubMedCentralGoogle Scholar
  48. Sültmann H, Mayer WE (1997) Reconstruction of cichlid fish phylogeny using nuclear DNA markers. In: Kocher T, Stepien C (eds) Molecular systematics of fishes. Academic Press, Cambridge, pp 39–51CrossRefGoogle Scholar
  49. Sültmann H, Mayer WE, Figueroa F, Tichy H, Klein J (1995) Phylogenetic analysis of cichlid fishes using nuclear DNA markers. Mol Biol Evol 12:1033–1047PubMedPubMedCentralGoogle Scholar
  50. Tibihika PD, Waidbacher H, Masembe C, Curto M, Sabatino S, Alemayehu E, Meulenbroek P, Akoll P, Meimberg H (2018) Anthropogenic impacts on the contextual morphological diversification and adaptation of Nile tilapia (Oreochromis niloticus, L. 1758) in East Africa. Environ Biol Fish 101:363–381CrossRefGoogle Scholar
  51. Tobler M, Carson EW (2010) Environmental variation, hybridization, and phenotypic diversification in Cuatro Ciénegas pupfishes. J Evol Biol 23:1475–1489CrossRefPubMedPubMedCentralGoogle Scholar
  52. Trape S (2009) Impact of climate change on the relict tropical fish fauna of Central Sahara: threat for the survival of Adrar mountains fishes, Mauritania. PLoS ONE 4:e4400CrossRefPubMedPubMedCentralGoogle Scholar
  53. Trewavas E (1983) Tilapiine fishes of the genera Sarotherodon, Oreochromis and Danakilia. British Museum Natural History, London, p 583CrossRefGoogle Scholar
  54. Van Oosterhout C, Hutchinson W, Wills D, Shipley P (2006) MICROCHECKER v. 2.2. 3. University of Hull, Kingston-upon-Hull. Accessed 3 Mar 2014
  55. Velo-Antón G, Godinho R, Campos JC, Brito JC (2014) Should I stay or should I go? Dispersal and population structure in small, isolated desert populations of West African Crocodiles. PLoS ONE 9:e94626CrossRefPubMedPubMedCentralGoogle Scholar
  56. Waits LP, Luikart G, Taberlet P (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10:249–256CrossRefPubMedPubMedCentralGoogle Scholar
  57. Weir BS, Cockerham CC (1984) Estimating F-Statistics for the analysis of population structure. Evolution 38:1358–1370PubMedPubMedCentralGoogle Scholar
  58. Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191PubMedPubMedCentralGoogle Scholar
  59. Woolson R (2007) Wilcoxon signed-rank test. In: D'Agostino R, Massaro J, Sullivan L (eds) Wiley encyclopedia of clinical trials. John Wiley Sons, pp 1–3Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.CIBIO/InBIO, Centro de Investigação em Biodiversidade e Recursos GenéticosUniversidade do PortoVairãoPortugal
  2. 2.Departamento de Biologia, Faculdade de CiênciasUniversidade do PortoPortoPortugal
  3. 3.Department of ZoologyUniversity of JohannesburgAuckland ParkSouth Africa

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