Ancient Mitochondrial Capture as Factor Promoting Mitonuclear Discordance in Freshwater Fishes: A Case Study in the Genus Squalius (Actinopterygii, Cyprinidae) in Greece

. 2016 ; 11 (12) : e0166292. [epub] 20161201

Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid27906993

Hybridization and incomplete lineage sorting are common confounding factors in phylogeny and speciation resulting in mitonuclear disparity. Mitochondrial introgression, a particular case of hybridization, may, in extreme cases, lead to replacement of the mitochondrial genome of one species with that of another (mitochondrial capture). We investigated mitochondrial introgression involving two species of the cyprinid genus Squalius in the western Peloponnese region of Greece using molecular and morphological data. We found evidence of complete mitochondrial introgression of Squalius keadicus into two populations recognized as Squalius peloponensis from the Miras and Pamissos River basins and a divergence of mitochondrial genomes of S. keadicus from the Evrotas basin from that of the introgressed populations dating from the Pleistocene. Secondary contact among basins is a possible factor in connection of the species and the introgression event. Morphological analyses support the hypothesis of mitochondrial introgression, as S. keadicus was different from the other three populations recognized as S. peloponensis, although significant differences were found among the four populations. Isolation by geographical barriers arose during Pleistocene in the western Peloponnese were the source of the evolution of the two reciprocally monophyletic subclades found in the S. keadicus mitochondrial clade, and the morphological differences found among the four populations. Along with the lack of structure in the nuclear genome in the three populations ascribed to S. peloponensis, this suggests an incipient speciation process occurring in these Squalius species in the western Peloponnese.

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Zink RM, Barraclough G. Mitochondrial DNA under siege in avian phylogeography. Mol. Ecol. 2008; 17: 2107–2121. 10.1111/j.1365-294X.2008.03737.x PubMed DOI

Funk DJ, Omland KE. Species-level paraphyly and polyphyly: Frequency, causes, and consequences, with insights from Animal Mitochondrial DNA. Annu. Rev. Ecol. Evol. S. 2003; 34: 397–423.

Chan KMA, Levin SA. Leaky prezygotic isolation and porous genomes: rapid introgression of maternally inheritance DNA. Evolution, 2005; 59: 720–729. PubMed

Toews DPL, Brelsford A. The biogeography of mitochondrial and nuclear discordance in animals. Mol. Ecol. 2012; 21: 3907–3930. 10.1111/j.1365-294X.2012.05664.x PubMed DOI

Joly S, McLenachan PA, Lockhart PJ. A statistical approach for distinguishing hybridization and incomplete lineage sorting. Am. Nat. 2009; 174: 54–70. PubMed

Maddison WP. Gene trees in species trees. Syst. Biol. 1997; 46(3): 523–536.

Degnan JH, Rosenberg NA. Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends Ecol. Evol. 2009; 24(6): 332–340. 10.1016/j.tree.2009.01.009 PubMed DOI

Edwards S, Bensch S. Looking forwards or looking backwards in avian phylogeography? A comment on. Mol. Ecol. 2009; 18(14): 2930–2933. 10.1111/j.1365-294X.2009.04270.x PubMed DOI

Rosenberg NA. 2013. Discordance of species trees with their most likely gene trees: a unifying principle. Mol. Biol. Evol. PubMed PMC

Meng C, Kubatko LS. Detecting hybrid speciation in the presence of incomplete lineage sorting using gene tree incongruence: A model. Theor. Popul. Biol. 2009; 75(1): 35–45. 10.1016/j.tpb.2008.10.004 PubMed DOI

McKay BD, Zink RM. The causes of mitochondrial DNA gene tree paraphyly in birds. Mol. Phylogenet. Evol. 2010; 54: 647–650. 10.1016/j.ympev.2009.08.024 PubMed DOI

Yu Y, Than C, Degnan JH, Nakleh L. Coalescent histories on phylogenetic networks and detection of hybridization despite incomplete lineage sorting. Syst. Biol. 2011; 60(2): 138–149. 10.1093/sysbio/syq084 PubMed DOI PMC

Jan CC, Fernández-Martínez JM. Interespecific hybridization, gene transfer and the development of resistance to the broomrape race F in Spain. Helia. 2002; 25(36): 123–136.

Cunha C, Coelho MM, Carmona JA, Doadrio I. Phylogeographical insights into the origins of the Squalius alburnoides complex via multiple hybridization events. Mol. Ecol. 2004; 13(9): 2807–2817. 10.1111/j.1365-294X.2004.02283.x PubMed DOI

Sousa-Santos C, Collares-Pereira MJ, Almada VC. Evidence of extensive mitocondrial introgression with nearly complete substitution of the typical Squalius pyrenaicus-like mtDNA of the Squalius alburnoides complex (Cyprinidae) in an independent Iberian lineage. J. Fish. Biol. 2006; 68(SB): 292–301.

Rhymer JM, Simberloff D. Extinction by hybridization and introgression. Annu. Rev. Ecol. Syst. 1996; 27: 83–109.

Weisrock DWK, Hozak H, Larson A. Phylogeographic analysis of mitochondrial gene flow and introgression in the salamander Plethodon shermani. Mol. Ecol. 2005; 14: 1457–1472. 10.1111/j.1365-294X.2005.02524.x PubMed DOI

Linnen CR, Farrell BD. Mitonuclear discordance is caused by rampant mitochondrial introgression in Neodiprion (Hymenoptera: Diprionidae) sawflies. Evolution, 2007; 61(6): 1417–1438. 10.1111/j.1558-5646.2007.00114.x PubMed DOI

Bryson RW Jr, Smith BT, Nieto-Montes de Oca A, García-Vázquez UO, Riddle BR. The role of mitochondrial introgression in illuminating the evolutionary history of Neartic treefrogs. Zool. J. Linn. Soc. 2014; 172: 103–116.

Ballard JWO, Whitlock MC. The incomplete natural history of mitochondria. Mol. Ecol. 2004; 13: 729–744. PubMed

Currat M, Ruedi M, Petit RJ, Excoffier L. The hidden side of invasions: massive introgression by local genes. Evolution, 2008; 62(8): 1908–1920. 10.1111/j.1558-5646.2008.00413.x PubMed DOI

Good JM, Hird S, Reid N, Demboski JR, Steppan SJ, Martin-Nims TR, et al. Ancient hybridization and mitochondrial capture between two species of chipmunks. Mol. Ecol. 2008; 17: 1313–1327. 10.1111/j.1365-294X.2007.03640.x PubMed DOI

Rabosky DL, Talaba AL, Donnellan SC. Lovette IJ. Molecular evidence for hybridization between two Australian desert skinks, Ctenotus leonhardii and Ctenotus quattuordecimlineatus (Scindidae: Squamata). Mol. Phylogenet. Evol. 2009; 53: 368–377. 10.1016/j.ympev.2009.06.020 PubMed DOI

Marková S, Dufresne F, Manca M, Kotlík P. Mitochondrial capture misleads about ecological speciation in Daphnia pulex complex. PLoS One, 2013; 8(7): e69497 10.1371/journal.pone.0069497 PubMed DOI PMC

Willis SC, Farias IP, Ortí G. Testing mitochondrial capture and deep coalescence in Amazonian cichlid fishes (Cichlidae: Cichla). Evolution 2014; 68: 256–268. 10.1111/evo.12230 PubMed DOI

Freyhof J, Dietmar L, Pitra C, Ludwig A. Molecules and morphology: Evidence for introgression of mitochondrial DNA in Dalmatian cyprinids. Mol. Phylogenet. Evol. 2005; 37: 347–354. 10.1016/j.ympev.2005.07.018 PubMed DOI

Nevado B, Koblmüller S, Sturmbauer C, Snoeks J, Usano-Alemany J, Verheyen E. Complete mitochondrial DNA replacement in a Lake Tanganyia cichlid fish. Mol. Ecol. 2009; 18: 4240–4255. 10.1111/j.1365-294X.2009.04348.x PubMed DOI

Tang Q-Y, Liu S-Q, Yu D, Liu H-Z, Danley PD. Mitochondrial capture and incomplete lineage sorting in the diversification of balitorine loaches (Cypriniformes, Balitoridae) revealed by mitochondrial and nuclear genes. Zool. Scr. 2012; 41(4): 233–247.

Costedoat C, Pech N, Chappaz R, Gilles A. Novelties in hybrid zones: Crossroads between population genomic and ecological approaches. 2007. PLoS One. 2007; 2(4): e357 10.1371/journal.pone.0000357 PubMed DOI PMC

Aboim MA, Mavárez J, Bernatchez L, Coelho MM. Introgressive hybridization between two Iberian endemic cyprinid fish: a comparison between two independent hybrid zones. J. Evol. Biol. 2010; 23(4): 817–828. 10.1111/j.1420-9101.2010.01953.x PubMed DOI

Sinama M, Gilles A, Costedoat C, Corse E, Olivier J- M, Chappaz R, et al. Non-homogeneus combination of two porous genomes induces complex body shape trajectories in cyprinid hybrids. Front. Zool. 2013; 10:22 10.1186/1742-9994-10-22 PubMed DOI PMC

Geiger M, Schreiner C, Delmastro GB, Herder F. Combining geometric morphometrics with molecular genetics to investigate a putative hybrid complex: a case study with barbels Barbus spp. (Teleostei: Cyprinidae). J. Fish Biol. 2016; 88(3): 1038–1055. 10.1111/jfb.12871 PubMed DOI

Doadrio I, Carmona JA. Genetic diversity in Greek of the genus Leuciscus and its evolutionary and biogeographical implications. J. Fish Biol. 1998; 53(3): 591–613.

Durand JD, Ünlu E, Doadrio I, Pipoyan S, Templeton AR. Origin, radiation, dispersion and allopatric hybridization in the chub Leuciscus cephalus. Proc. R. Soc. Biol. Sci. 2000; 267: 1687–1697. PubMed PMC

Sanjur O, Carmona JA, Doadrio I. Molecular phylogeny of Iberian chub (genus Squalius, Cyprinidae) inferred from molecular data. Mol. Phylogenet. Evol. 2003; 29: 20–30. PubMed

Perea S, Böhme M, Zupančič P, Freyhof J, Šanda R, Özulug M, et al. Phylogenetic relationships and biogeographical patterns in Circum-Mediterranean subfamily Leuciscinae (Teleostei, Cyprinidae) inferred from both mitochondrial and nuclear data. BMC Evol. Biol. 2010; 10: 265 10.1186/1471-2148-10-265 PubMed DOI PMC

Kottelat M, Freyhof J. Handbook of the European Freshwater Fishes. Cornol. Berlin. 2007.

Fountoulis I, Mariolakos I, Ladas I. Quaternary basin sedimentation and geodynamics in SW Peloponnese (Greece) and late stage uplift of Taygetos Mt. B. Geofis. Teor. Appl. 2014; 55(2): 303–324.

Kokkalas S, Xypolias P, Koukovelas I, Doutsos T. Postcollisional contractional and extensional deformation in the Aegean region. In: Dilek Y, Pavlides S, eds. Post Collisional Tectonics & Magmatism in the Mediterranean Region and Asia. Geol. S. Am. S. 2006; 409, 97–123.

Papanikolau D, Fountoulis I, Metaxas C. 2007. Active faults, deformation rates and Quaternary paleogeography at Kyparissiakos Gulf (SW Greece) deduced from onshore and offshore data. Quat. Int. 172: 14–30.

Fountoulis I, Mariolakos I. Neotectonic folds in the central-western Peloponnese, Greece. Z. Dtsch. Ges. Geowiss 2008; 159(3): 485–494.

Koukouvelas I, Kokkalas S, Xypolias P. Surface deformation during the Mw 6.4 (8 June 2008) Movri Mountain earthquarke in the Peloponnese, and its implications for the seismotectonics of western Greece. Inter. Geol. Rev. 2009; 52(2–3): 249–268.

Athanassas C, Fountoulis I. Quaternary neotectonic configuration of the southwestern Peloponnese, Greece, based on luminescence ages of marine terraces. J. Earth Sci. 2013; 24(3): 410–427.

Cuvier G, Valenciennes A. Histoire naturelle des poisons. Tome dix-septième. Suite du livre dix-huitième. Cyprinoïdes. v.17: i-xxiii + 1–497 + 2 pp.; 1844. p. 487–519.

Stephens M, Smith N, Donelly P. A new statistical method for haplotype reconstruction from population data. Am. J. Hum. Genet. 2001; 68: 978–989. 10.1086/319501 PubMed DOI PMC

Stephens M, Donelly P. 2003. A comparison of Bayesian methods for haplotype reconstruction from population genotype data. American Journal of Human Genetics, 73: 1162–1169. 10.1086/379378 PubMed DOI PMC

Librado P, Rozas J. DnaSP v.5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 2009; 25: 1451–1452. 10.1093/bioinformatics/btp187 PubMed DOI

Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994; 22: 4673–4680. PubMed PMC

Kumar S, Stecher G, Tamura K. MEGA v.7: Molecular Evolutionary Genetics Analysis Version 7. Mol. Biol. Evol. 2015. (submitted). PubMed PMC

Bruen TC, Phillipe H, Bryant D. A simple and robust statistical test for detecting the presence of recombination. Genetics 2006; 172(4): 2665–2681. 10.1534/genetics.105.048975 PubMed DOI PMC

Huson DH, Bryant D. Application of phylogenetic networks in Evolutionary Studies. Mol. Biol. Evol. 2006; 23(2): 254–267. 10.1093/molbev/msj030 PubMed DOI

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

Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, et al. MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space. Syst. Biol. 2012; 61(3): 539–542. 10.1093/sysbio/sys029 PubMed DOI PMC

Rambaut A, Drummond AJ. Tracer v.1.6. Available from http://beast.bio.ed.ac.uk./Tracer. 2007.

Stamakis A. RaxML-VI-HPC: Maximum Likelihood-based phylogenetic Analyses with thousands of taxa and Mixed Models. Bioinformatics, 2006; 22(21): 2688–2690. 10.1093/bioinformatics/btl446 PubMed DOI

Stamakis A, Blagojevic F, Nikolopoulos D, Antonopoulos C. Exploring new search algorithms and hadware for phylogenetics: RaxML Meets the IBM Cell. The Journal of VLSI Signal Processing, 2007; 48: 271–286.

Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu C-H, Xie D, et al. BEAST 2: A Software Platform for Bayesian Evolutionary Analysis. PLoS Comput. Biol. 2014; 10(4): e1003537 10.1371/journal.pcbi.1003537 PubMed DOI PMC

Stadler T. On incomplete taxon sampling under birth-death models and connection to the sampling-based coalescent. J. Theor. Biol. 2009; 261: 58–66. 10.1016/j.jtbi.2009.07.018 PubMed DOI

Gaudant J. Contributions à la Paléontologie du Miocène moyen continental du bassin du Tage. II-Observations sur les dents pharyngiennes de Poissons Cyprinidés-Póvoa de Santarém. Ciencias da Terra, 1977; 3: 129–141.

Cabrera L, Gaudant J. 1985. Los Ciprínidos (Pisces) del sistema lacustre Oligocénico-Miocénico de los Monegros (secto SE de la cuenca del Ebro, provincias de Lleida, Tarragona, Huesca y Zaragoza). Acta Geológica Hispánica, 1985; 20(3–4): 219–226.

Böhme, M, Ilg, A. 2003. fosFARbase, www.wahre-staerke.com/ (Accessed April 2016).

Doadrio I, Perea S, Alonso F. A new species of the genus Squalius Bonaparte, 1837 in the Tagus Basin (Central Spain). Graellsia, 2007; 63(1): 89–100.

Burnaby TP. Growth-invariant discriminant functions and generalized distances. Biometrics, 1966; 22: 96–110.

Rohlf FJ, Bookstein FL. A comment on shearing as a method for “size correction”. Syst. Zool. 1987; 36: 357–367.

Hammer Ø, Harper DAT, Ryan D. PAST: Paleontological Statistics Software Package for Education and Data Analysis. Paleontological Electronica, 2001. 41(1): 9pp.

Machordom A, Berrebi P, Doadrio I. Spanish barbell hybridization detected using enzymatic markers: Barbus meridionalis Risso x Barbus haasi Mertens (Osteichthyes, Cyprinidae). Aquat. Living Resour. 1990: 3(4): 295–303.

Cunha C, Bastir M, Coelho MM, Doadrio I. Body shape evolution among ploidy levels of the Squalius alburnoides hybrid complex (Teleostei, Cyprinidae). J. Evol. Biol. 2004; 22: 718–728. PubMed

Aguilar A, Jones WJ. Nuclear and mitochondrial diversification in two native California minnows: insights into taxonomic identity and regional Phylogeography. Mol. Phylogenet. Evol. 2009; 51: 373–381. PubMed

Broughton RE, Vedala KC, Crowl TM, Ritterhouse LL. Current and historical hybridization with differential introgression among three species of cyprinid fishes (genus Cyprinella). Genetica 2011; 139: 699–707. 10.1007/s10709-011-9578-9 PubMed DOI

Leaché AD, McGuire JA. Phylogenetic relationships of horned lizards (Phrynosoma) based on nuclear and mitochondrial data: Evidence for a misleading mitochondrial gene tree. Mol. Phylogenet. Evol. 2006; 39(3): 628–644. 10.1016/j.ympev.2005.12.016 PubMed DOI

Barbanera F, Zuffi MAL, Guerrini M, Gentilli A, Tofanelli S, Fasola M, et al. Molecular Phylogeography of the asp viper Vipera aspis (Linnaeus, 1758) in Italy: evidence for introgressive hybridization and mitochondrial DNA capture. Mol. Phylogenet. Evol. 2009; 52: 103–114. 10.1016/j.ympev.2009.02.006 PubMed DOI

Alexander HJ, Breden F. Sexual isolation and extreme morphological divergence in the Cumaná guppy: a possible case of incipient speciation. J. Evol. Biol. 2004; 17: 1238–1254. 10.1111/j.1420-9101.2004.00788.x PubMed DOI

Meyer A, Salzburger W, Schartl M. Hybrid origin of a swordtail species (Teleostei: Xiphophorus clemenciae) driven by sexual selection. Mol. Ecol. 2006; 15: 721–730. 10.1111/j.1365-294X.2006.02810.x PubMed DOI

Magalhaes IS, Mwaiko S, Schneider V, Seehaunsen O. Divergent selection and phenotypic plasticity during incipient speciation in Lake Victoria cichlid fish. J. Evol. Biol. 2009; 22: 260–274. 10.1111/j.1420-9101.2008.01637.x PubMed DOI

Knudsen R, Klemetsen A, Amundsen P-A, Hermansen B. Incipient speciation through niche expansion: an example from the artic charr in a subartic lake. Proc. R. Soc. Biol. Sci. 2006; 273: 2291–2298. PubMed PMC

Nosil P, Harmon LJ, Seehausen O. Ecological explanations for (incomplete) speciation. Trends Ecol. Evol. 2009; 24(3): 145–156. 10.1016/j.tree.2008.10.011 PubMed DOI

Perdices A, Doadrio I, Economidis PS, Bohlen J, Doadrio I. Pleistocene effects on the European freshwater fish fauna: double origin of the cobitid genus Sabanejewia in the Danube basin (Osteichthyes, Cobitidae). Mol. Phylogenet. Evol. 2003. 26: 289–299. PubMed

Vila M, Vidal-Romaní JR, Björklund M. The importance of time scale and multiple refugia: incipient speciation and admixture of lineages in the butterfly Erebia triaria (Nymphalidae). Mol. Phylogenet. Evol. 2005; 36: 249–260. 10.1016/j.ympev.2005.02.019 PubMed DOI

Bohlen J, Perdices A, Doadrio I, Economidisi PS. Vicariance, colonisation, and fast local speciation in Asia Minor and the Balkans as revealed from the phylogeny of spined loaches (Osteichthyes; Cobitidae). Mol. Phylogenet. Evol. 2006; 39: 552–561. 10.1016/j.ympev.2005.12.007 PubMed DOI

Bryson RW Jr, Nieto-Montes de Oca A, Jaeger JR, Riddle BR. Elucidation of cryptic diversity in a widespread Neartic treefrog reveals episodes of mitochondrial gene capture as frogs diversified across a dynamic landscape. Evolution, 2010; 64: 2315–2330. 10.1111/j.1558-5646.2010.01014.x PubMed DOI

Rheindt FE, Edwards SV. Genetic introgression: an integral but neglected component of speciation in birds. The Auk 2011; 128: 620–632.

Ludwig A, Congiu L, Pitra C. Nonconcordant evolutionary history of maternal and paternal lineages in Adriatic sturgeon. Mol. Ecol. 2003. 12: 3253–3264. PubMed

Cheviron ZA, Brumfield RT. Migration-selection balance and local adaptation of mitochondrial haplotypes in Rufous-collared sparrows (Zonotrichia capensis) along an elevational gradient. Evolution 2009; 63: 1593–1605. 10.1111/j.1558-5646.2009.00644.x PubMed DOI

Hudson RR, Kreitman M, Aguade M. A test of neutral molecular evolution based on nucleotide data. Genetics 1987; 116: 153–159. PubMed PMC

Ntageretzis K, Vött A, Fischer P, Hadler H, Emde K, Röloke BR, et al. Paleotsunami history of the Eos Plain (Evrotas River delta, Peloponnese, Greece). Z. Geomorphol. 2015; 59(4): 253–273.

Athanassas C. Optically stimulated luminescence dating of Late Quaternary marine terraces, sea-level changes and coastal neotectonics in W. Messinia (SW Peloponnese, Greece). Unpublished D. Phil. Thesis. Faculty of Geology and Geoenvironment. National and Kapodistrian University of Athens. Greece. (In Greek). 2010.

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