Conséquences génétiques et morphologiques des glaciations du Quaternaire : une lignée relique du barbeau (Luciobarbus pallaryi, Cyprinidae) dans le bassin du Guir (Algerie)
[en] Climatic variations during the Quaternary period had a considerable impact on landscapes
and habitat fragmentation (rivers) in North Africa. These historical events can have
significant consequences on the genetic structure of the populations. Indeed, geographi-
cally separated and genetically isolated populations tend to differentiate themselves
through time, eventually becoming distinct lineages, allowing new species to emerge in
later generations. The aim of the present study is to use genetic and morphological
techniques to evaluate the major role of the Saalian glaciation (Middle Quaternary) in the
establishment of the geographic space and in the evolution of the intraspecific genetic
diversity, by tracing the demographic history of barbels belonging to the
Luciobarbus pallaryi (Cyprinidae) species in the Guir Basin (Algeria). In this context,
two populations, from two distinct and isolated sites, were studied. Analysis of the
cytochrome b (cyt b) mitochondrial markers and of the ‘‘D-loop’’ control region has shown
that the ‘‘upstream’’ and ‘‘downstream’’ Guir populations are genetically differentiated.
The molecular analyses suggest that the upstream population was disconnected from this
hydrographic system during the Saalian glaciation period of the Quaternary. Subsequently,
it was isolated in the foggaras underground waters in the Great Western Erg, at
approximately 320 000 years BP, creating, through a bottleneck effect, a new allopatric
lineage referred to as ‘‘Adrar’’. Conversely, the high genetic diversity in the upstream Guir
(Bechar) population suggests that the stock is globally in expansion. These barbels (n = 52)
were also examined with meristic, morphometric, osteological, and biological features
Disciplines :
Zoology
Author, co-author :
Brahimi, Amina
Tarai, Nacer
Benhassane, Abdelkrim
Henrard, Arnaud
Libois, Roland ; Université de Liège > Département de Biologie, Ecologie et Evolution > Zoogéographie
Language :
English
Title :
Conséquences génétiques et morphologiques des glaciations du Quaternaire : une lignée relique du barbeau (Luciobarbus pallaryi, Cyprinidae) dans le bassin du Guir (Algerie)
Alternative titles :
[en] Genetic and morphological consequences of Quaternary glaciations: A relic barbel lineage (Luciobarbus pallaryi, Cyprinidae) of Guir Basin (Algeria)
R.G. Harrison, Hybrid zones and the evolutionary process, Oxford University Press, New York, 1993, 374 p.
M. Kirkpatrick, N.H. Barton, Evolution of a species' range, Am. Nat. 150 (1997) 1-23.
F. Dufresne, E. Bourget, L. Bernatchez, Differential patterns of spatial divergence in microsatellite and allozyme alleles: further evidence for locus-specific selection in the acorn barnacle, Semibalanus balanoides Mol. Ecol. 11 (2002) 113-123.
M. Lomolino, B. Riddle, J. Brown, Biogeography, 3rd ed, Sinauer Assoc., Sunderland, MA, USA, 2006.
E. Mayr, Animal species and evolution, Harvard University Press, Cam-bridge, MA, USA, 1963, 812 p.
S. Gavrilets, A. Hastings, Founder effect speciation: a theoretical reas-sessment, Am. Nat. 147 (1996) 466-491.
G.J. Howes, The phylogenetic position of the Yugoslavian Cyprinid fish genus Aulopyge Heckel, 1841, with an appraisal of the genus Barbus Cuvier & Cloquet, 1816, and the subfamily Cyprinidae, Bull. Br. Mus. Nat. Hist. Zool. 52 (1987) 165-196.
P. Berrebi, G. Lamy, G. Cattaneo-Berrebi, J.F. Renno, Variabilite gene-tique de Barbus meridionalis Risso (Cyrinidae) : une espe ce quasi monomorphe, Bull. Fr. Pêche. Piscic. 310 (1988) 77-84.
I. Doadrio, Phylogenetic relationships and classification of west palaeartic species of the genus Barbus (Osteichthyes, Cyprinidae), Aquat. Living Resour. 3 (1990) 265-282.
P. Berrebi, Speciation of the genus Barbus in the north Mediterranean Basin: recent advances from biochemical genetics, Biol. Conserv. 72 (1995) 237-249.
I. Doadrio, R. Bouhadad, A. Machordom, Genetic differentiation and biogeography in Saharan populations of the genus Barbus (Osteich-thyes, Cyprinidae), Folia Zool. 47 (1998) 7-20.
C.S. Tsigenopoulos, P. Berrebi, Molecular phylogeny of North Mediter-ranean freshwater barbs (genus Barbus: Cyprinidae) inferred from cytochrome b sequences: Biogeographic and systematic implications, Mol. Phylogenet. Evol. 14 (2000) 165-179.
A. Machordom, I. Doadrio, Evidence of a cenozoic Betic-Kabilian con-nection based on freshwater fish phylogeography (Luciobarbus, Cypri-nidae), Mol. Phylogenet. Evol. 18 (2001) 252-263.
I. Doadrio, J.A. Carmona, A. Machordom, Haplotype diversity and phylogenetic relationships among Iberian barbels (Barbus, Cyprinidae) reveal two evolutionary lineages, J. Hered. 93 (2002) 140-147.
R. Zardoya, I. Doadrio, Molecular evidence on the evolutionary and biogeographical patterns of European cyprinids, J. Mol. Evol. 49 (1999) 227-237.
C.S. Tsigenopoulos, J.D. Durand, E. Ünlü , P. Berrebi, Rapid radiation of the Mediterranean Luciobarbus species (Cyprinidae) after the Messi-nian salinity crisis of the Mediterranean Sea, inferred from mitochon-drial phylogenetic analysis, Biol. J. Linn. Soc. 80 (2003) 207-222.
P. Nosil, Adaptive population divergence in cryptic color-pattern fol-lowing a reduction in gene flow, Evolution 63 (2009) 1902-1912.
A. Camargo, B. Sinervo, J.W. Sites, Lizards as model organisms for linking phylogeographic and speciation studies, Mol. Ecol. 19 (2010) 3250-3270.
R.R. Schoch, N.B. Frö bisch, Metamorphosis and neoteny: alternative pathways in an extinct amphibian clade, Evolution 60 (2006) 1467-1475.
F. Alayne-Street, L'environnement a l'âge glaciaire, in: A. Sherratt (Ed.), Encyclope die d'arche ologie, Editions du Fanal, Paris, 1981, pp. 52-56.
J. Haffer, Speciation in Amazonian forest birds, Science 165 (1969) 131-137.
G.M. Hewitt, Post-glacial re-colonization of European biota, Biol. J. Linn. Soc. 68 (1999) 87-112.
G.M. Hewitt, The genetic legacy of the Quaternary ice ages, Nature 405 (2000) 907-913.
V. Deffontaine, R. Libois, P. Kotlik, R. Sommer, C. Nieberding, E. Paradis, J.B. Searle, J.R. Michaux, Beyond the Mediterranean peninsulas: evi-dence of central European glacial refugia for a temperate forest mam-mal species, the bank vole (Clethrionomys glareolus), Mol. Ecol. 14 (2005) 1727-1739.
S.R. Palumbi, Nucleic acids II: The polymerase chain reaction, in: D.M. Hillis, C. Moritz, B.K. Mable (Eds.), Molecular Systematic, 2nd ed., Sinauer, Sunderland, MA, USA, 1996.
A. Perdices, I. Doadrio, The molecular systematics and biogeography of the European cobitids based on mitochondrial DNA sequences, Mol. Phylogenet. Evol. 19 (2001) 468-478.
S.A. Nwafili, O.O. Soyinka, T.X. Gao, Levels and patterns of genetic diversity in wild Chrysichthys nigrodigitatus in the Lagos Lagoon complex, Afr. J. Biotechnol. 11 (2012) 15748-15754.
K. Katoh, D.M. Standley, MAFFT Multiple sequence alignment Software Version 7: Improvements in performance and usability, Mol. Biol. Evol. 30 (2013) 772-780.
L. Excoffier, G. Laval, S. Schneider, Arlequin (version 3.0): An integrated software package for population genetics data analysis, Evol. Bioin-form. Online 1 (2005) 47-50.
M. Nei, Molecular Evolutionary Genetics, Columbia University Press, New York, 1987.
F. Tajima, Measurement of DNA polymorphism, in: N. Takahata, A.G. Clark (Eds.), Mechanisms of molecular evolution, Sinauer Associates Inc., Sunderland, 1993, pp. 37-59.
B.S. Weir, C.C. Cockerham, Estimating F-statistics for the analysis of population structure, Evolution 38 (1984) 1358-1370.
M. Kimura, Estimation of evolutionary distances between homologous nucleotide sequences, Proc. Natl. Acad. Sci. USA 78 (1981) 454-458.
K. Tamura, G. Stecher, D. Peterson, A. Filipski, S. Kumar, Molecular Evolutionary Genetics Analysis: MEGA version 6.0, Mol. Biol. Evol. 30 (2013) 2725-2729.
F. Tajima, The effect of change in population size on DNA polymor-phism, Genetics 123 (1989) 597-601.
Y.X. Fu, W.H. Li, Statistical tests of neutrality of mutations, Genetics 133 (1993) 693-709.
Y.X. Fu, Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection, Genetics 147 (1997) 915-925.
A.R. Rogers, H. Harpending, Population growth makes waves in the distribution of pairwise genetic differences, Mol. Biol. Evol. 9 (1992) 552-569.
S. Schneider, L. Excoffier, Estimation of demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: Application to human mitochondrial DNA, Genetics 152 (1999) 1079-1089.
H.J. Bandelt, P. Forster, A. Rö hl, Median-joining networks for inferring intraspecific phylogenies, Mol. Biol. Evol. 16 (1999) 37-48.
J. Felsenstein, Evolutionary tree from DNA sequences: a maximum likelihood approach, J. Mol. Evol. 17 (1981) 368-376.
K. Tamura, M. Nei, Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpan-zees, Mol. Biol. Evol. 10 (1993) 512-526.
D. Darriba, G.L. Taboada, R. Doallo, D. Posada, jModelTest 2: more models, new heuristics and parallel computing, Nat. Methods 9 (2012) 772.
J. Sukumaran, M.T. Holder, SumTrees: Phylogenetic tree Summariza-tion. 4.0.0 (Jan 31 2015), 2015 https://github.com/jeetsukumaran/Dendrophy.
J. Sukumaran, M.T. Holder, DendroPy: a Python library for phylogenetic computing, Bioinformatics 26 (2010) 1569-1571.
F. Ronquist, M. Teslenko, P. Mark, D.L. Ayres, A. Darling, S. Hö hna, B. Larget, L. Liu, M.A. Suchard, J.P. Huelsenbeck, MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large, model space, Syst. Biol. 61 (2012) 539-542.
A. Rambaut, FigTree v1.4.2, 2009 http://tree.bio.ed.ac.uk/software/figtree/.
A.J. Drummond, M.A. Suchard, D. Xie, A. Rambaut, Bayesian phylogenetics with BEAUti and the BEAST 1.7, Mol. Biol. Evol. 29 (2012) 1969-1973.
A. Drummond, S. Ho, M. Phillips, A. Rambaut, Relaxed phylogenetics and dating with confidence, PLoS Biol. 4 (2006) 88.
A. Rambaut, M.A. Suchard, D. Xie, A.J. Drummond, Tracer v1.6, 2014 http://beast.bio.ed.ac.uk/Tracer.
J. Goubier, Bioge ographie, biome trie et biologie du sandre, Lucioperca lucioperca (L.), Osteichthyen, Percide , Univ. Claude-Bernard, Lyon, 1975, [the se de doctorat e s sciences], 259 p.
C. Levêque, D. Paugy, G.G. Teugels, Faune des poissons d'eaux douces et saumâtres d'Afrique de l'Ouest, Musee royal de l'Afrique centrale, Tervuren, Belgium, 1990, 385 p.
M.L.J. Stiassny, G.G. Teugels, C.D. Hopkins, Poissons d'eaux douces et saumâtres de basse Guine e, ouest de l'Afrique centrale, IRD/Museum national d'histoire naturelle/MRAC, Paris & Brussels, 2007, 805 p.
B. Adepo-Goure ne, G. Goure ne, Diffe renciation morphologique des populations naturelles d'une sous-espe ce de tilapia Sarotherodon melanotheron melanotheron Rü ppell, 1852 (Teleostei; Cichlidae) de Côte d'Ivoire, Sci. Nat. 5 (2008) 15-27.
O. Turki, M. M'hetli, A. Chriki, M.M. Kraem, Caracterisation et variation phenotypique et biologique des deux sexes du sandre Sander lucioperca (1758) (teleosteen, percidae) dans la retenue de barrage de Nebhana (Tunisie centrale), Bull. Inst. Nat. Sci. Tech. Mer Salammbô 36 (2009) 75-85.
S.M. Fagnon, A. Chikou, I. Youssao, P. Laleye, Caracte risation morpho-logique des populations de Sarotherodon melanotheron (Pisces, Cichli-dae) en eaux douces et saumâtres au Sud Be nin, Int. J. Biol. Chem. Sci. 7 (2013) 619-630.
A. Vrevene, I. Zamba, V. Mamonekene, T. Geerinckx, Description of Notoglanidium pembetadi new species (Siluriformes: Claroteidae) from the Kouilou-Niari River, Republic of the Congo, Zootaxa 3691 (2013) 153-164.
R.M. Libois, C. Hallet-Libois, R. Rosoux, Elements pour l'identification des restes crâniens des poissons dulcąquicoles de Belgique et du Nord de la France. I. Anguilliformes, Gaste roste iformes, Cyprinodontiformes, Perciformes. Fiches d'oste ologie animale pour l'arche ologie. Se r. A. no 3, CRA-CNRS, Valbonne, 1987, 15 p.
R.M. Libois, C. Hallet-Libois, Elements pour l'identification des restes crâniens des poissons dulcąquicoles de Belgique et du Nord de la France. II. Cypriniformes. Fiches d'oste ologie animale pour l'arche olo-gie. Se r. A. no 4, CRA-CNRS, Valbonne, 1988, 24 p.
V. Mahnert, J. Gery, La mâchoire supe rieure de certains Barbus (Pisces, Cypriniformes) africains, Rev. Suisse Zool. 84 (1977) 229-236.
R. Sokal, J. Rohlf, Biometry, 2nd ed., Freeman & Co, New York, 1981, 859 p.
T. Cucchi, M. Baylac, A. Evin, O. Bignon-Lau, J.-D. Vigne, Morphome trie geome trique et archeozoologie : Concepts, methodes et applications, in: M. Balasse, J.-P. Brugal, Y. Dauphin, E.-M. Geigl, C. Oberlin, I. Reiche (Eds.), Messages d'os-Archeome trie du squelette animal et humain, Editions des archives contemporaines, collection Sciences arche ologi-ques, Paris, 2015, pp. 197-216.
H.F. Gante, Diversification of Circum-mediterranean barbels, changing diversity, in: O. Grillo, G. Venora (Eds.), Changing Diversity in Changing Environment, InTech, 2011, , pp. 283-298. , http://dx.doi.org/10.5772/24639 (Available from: http://www.intechopen.com/books/changing-diversity-in-changing-environment/diversification-of-circum-mediterranean-barbels).
L. Buonerba, Phylogeography of Italian barbels (Cyprinidae, Barbus) inferred by mitochondrial and nuclear markers., University of Insubria, Varese, Italy, 2010, [PhD Thesis], 93 p.
L. Buonerba, L. Pompei, M. Lorenzoni, First record of Iberian barbel Luciobarbus graellsii (Steindachner, 1866) in the Tiber River (Central Italy), BioInvasions Rec 2 (2013) 297-301.
H.F. Gante, A role for introgressive hybridization in the evolution of freshwater fishes: the case-study of Iberian Barbus (Teleostei, Cypri-nidae), Arizona State University, Phoenix, 2009, PhD Thesis, 190 p.
J. Pellegrin, Cyprinidae: Barbus pallaryi, Bull. Soc. Zool. France 43 (1919) 322-324.
J. Pellegrin, Sur une varie te nouvelle du Barbus callensis C.V. provenant de l'oasis de Figuig (Maroc), Bull. Soc. Zool. France 38 (1913) 119-124.
J. Pellegrin, Les barbeaux de l'Afrique du Nord francąise : description d'une espece nouvelle, Bull. Soc. Sci. Nat. Maroc 19 (1939) 1-4.
J.C. Avise, Molecular markers, natural history and evolution, Chapmann & Hall, New York, 1994, 511 p.
J.C. Avise, Phylogeography: the history and formation of species, Harvard Univ. Press, Cambridge, MA, USA, 2000.
B. Simon-Bouhet, P. Garcia-Meunier, F. Viard, Multiple introductions promote range expansion of the mollusk Cyclope neritea (Nassariidae) in France: Evidence from mitochondrial sequence data, Mol. Ecol. 15 (2006) 1699-1711.
J.C. Avise, J.F. Shapira, S.W. Daniel, C.F. Aquadro, R.A. Lansman, Mito-chondrial DNA differentiation during the speciation process in Per-omyscus, Mol. Biol. Evol. 1 (1983) 38-56.
M.E. D'Amato, G.R. Carvalho, Population genetic structure and history of the long-tailed hake, Macruronus magellanicus, in the SW Atlantic as revealed by mtDNA RFLP analysis, ICES J. Mar. Sci. 62 (2005) 247-255.
V. Deffontaine, Histoire e volutive du campagnol roussâtre (Myodes (Clethrionomys) glareolus) en Eurasie, Universite de Lie ge, Belgium, 2008, [The se doct. sciences], 189 p.
W.S. Grant, B.W. Bowen, Shallow population histories in deep evolu-tionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation, J. Hered. 89 (1998) 415-426.
G. Goure ne, G.G. Teugels, Diffe renciation morphologique de souches des tilapias: Oreochromis niloticus et O. aureus (Teleostei; Cichlidae) utilise es en pisciculture, Cybium 17 (1993) 343-355.
R. Libois, M. Fareh, A. Brahimi, R. Rosoux, Regime alimentaire et strate gie trophique saisonnie re de la loutre d'Europe, Lutra lutra, dans le Moyen Atlas (Maroc), Rev. Ecol. (Terre & Vie) 70 (2015) 314-327.
C. Almacą, Sur la systematique des barbeaux marocains (Pisces, Cypri-nidae, Barbus), Arq. Mus. Boc. 1 (7) (1966) 111-121.
C. Almacą, Re vision critique de quelques types de cyprinide s d'Europe et d'Afrique du Nord des collections de Museum national d'histoire naturelle, Bull. Mus. Hist. Nat. Paris 40 (1969) 1116-1144.
M. Boumaza, Recherches sur les eaux courantes de Tunisie : inventaire faunistique, e cologie et bioge ographie, Faculte des sciences, Tunis, 1994, [The se de doctorat d'E tat], 429 p.
M. Boumaza, J.-P. Quignard, Description comparative des deux espe ces de Pseudophoxinus (Pisces, Cyprinidae) de la Tunisie, Bull. Soc. Sci. Nat. Tunisie 26 (1996) 21-27.
J. Dynes, P. Magnan, L. Bernatchez, M.A. Rodrguez, Genetic and mor-phological variations between two forms of lacustrine brook charr, J. Fish. Biol. 54 (1999) 955-972.
T. Dkhil-Abbes, M.M. Kraem, Variabilite morphologique des popula-tions du genre Pseudophoxinus dans les eaux douces tunisiennes, Cybium 35 (2011) 33-38.
C. Almacą, Studies on taxonomy, biogeography, and speciation in Euro-Mediterranean Barbus (Barbus s. s.), Arq. Mus. Boc. 2 (28) (1994) 455-462.
P. Berrebi, Contribution a l'etude du sous genre Labeobarbus (genre Barbus, poissons Cyprinide s) au Maroc, Bull. Inst. Sci. Rabat 5 (1981) 59-72.
P. Berrebi, Speciation of the genus Barbus in the north Mediterranean basin: recent advances from biochemical genetics, Biol. Conserv. 72 (1995) 237-249.
C. Almacą, Sur les barbeaux (genre et sous-genre Barbus de l'Afrique du Nord), Bull. Mus. Hist. Nat. Paris 42 (1970) 141-158.
G.A. Boulenger, Catalogue of the fresh water fish of Africa, Br. Museum Nat. Hist. 2 (1911) 112-113.
J.-J. Albaret, Les peuplements des estuaires et des lagunes, IRD Editions 564 (2006) 355-379.
J.-J. Albaret, P.S. Diouf, Diversite des poissons des lagunes et des estuaires ouest africains, Ann. Mus. r. Afr. centr. Zool. Tervuren 275 (1994) 165-177.
G. Fryer, T.D. Iles, The cichlid fishes of the great lakes of Africa. Their biology and evolution, Oliver & Boyd, Edinburgh, UK, 1972, 641 p.
M. Legendre, L. Trebaol, Efficacite de l'incubation buccale et frequence de ponte de Sarotherodon melanotheron (Rü ppel, 1852) en milieu d'elevage (lagune Ebrie , Côte d'Ivoire), ICLARM Conf. Proc. 41 (1996) 375-386.