Inter-population differences in otolith morphology are genetically encoded in the killifish Aphanius fasciatus (Cyprinodontiformes);Las diferencias inter-poblacionales en la morfología del otolito de Aphanius fasciatus (Cyprinodontiformes) se codifican genéticamente

Scientia Marina

Volumn 77, Issue 2, 2013, Pages 269-279

  Annabi, Ali ^a   Said, Khaled ^a   Reichenbacher, Bettina ^b  

^a UNIVERSITY OF MONASTIR   (Tunisia)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

Cyprinodontidae; Gene flow; Local adaptation; Mitochondrial markers; Otolith morphometry; Phylogeography

Indexed keywords

DIVERGENCE; GENE FLOW; GENETIC MARKER; GENETIC VARIATION; INTERPOPULATION VARIATION; LOCAL ADAPTATION; MITOCHONDRIAL DNA; MORPHOLOGY; MORPHOMETRY; OTOLITH; PHYLOGEOGRAPHY; TELEOST;

TUNISIA;

APHANIUS FASCIATUS; CYPRINODONTIDAE; CYPRINODONTIFORMES; CYPRINODONTOIDEI; PISCES; TELEOSTEI;

EID: 84879150191     PISSN: 02148358     EISSN: 18868134     Source Type: Journal    
DOI: 10.3989/scimar.03763.02A     Document Type: Article

References (79)

1. Afli A., Ayari R., Zaabi S. 2008. Ecological quality of some Tunisian coast and lagoon locations, by using benthic community parameters and biotic indices. Estuar. Coast. Shelf. Sci. 80: 269-280.
2. Astolfi L., Dupanloup I., Rossi R., Bisol P.M., Faure E., Congiu L. 2005. Mitochondrial variability of sand smelt Atherina boyeri populations from north Mediterranean coastal lagoons. Mar. Ecol. Prog. Ser. 297: 233-243.
3. Astraldi M., Gasparini G.P., Vetrano A., Vignudelli S. 2002. Hydrographic characteristics and interannual variability of water masses in the central Mediterranean: a sensitivity test for long-term changes in the Mediterranean Sea. Deep-Sea Res. I 49: 661-680.
4. Astraldi M., Balopoulos S., Candela J., Font J., Gacic M., Gasparini G.P., Manca B., Theocharis A., Tintoré J. 1999. The role of straits and channels in understanding the characteristics of Mediterranean circulation. Progr. Oceanogr. 44: 65-108.
5. Bekkevold D., André C., Dahlgren T.G., Clausen L.A., Torstensen E., Mosegaard H., Carvalho G.R., Christensen T.B., Norlinder E., Ruzzante D.E. 2005. Environmental correlates of population differentiation in Atlantic herring. Evolution 59: 2656-2668.
6. Béranger K., Mortier L., Crépon M. 2005. Seasonal variability of water transport through the Straits of Gibraltar, Sicily and Corsica, derived from a high-resolution model of the Mediterranean circulation. Progr. Oceanogr. 66: 341-364.
7. Bernardi G. 2000. Barriers to gene flow in Embiotoca jacksoni, a marine fish lacking a pelagic larval stage. Evolution 54: 226-237.
8. Brown W.M. 1983. Evolution of animal mitochondrial DNAs. In: Nei M., Koehn R.K. (eds), Evolution of Genes Proteins. Sinauer, Sunderland, MA. pp. 62-88.
9. Brown W.M., George M., Wilson A.C. 1979. Rapid evolution of animal mitochondrial DNA. Proc. Natl. Acad. Sci. USA 76: 1967-1971.
10. Campana S. 1999. Chemistry and composition of fish otoliths: pathways, mechanisms and applications. Mar. Ecol. Prog. Ser. 188: 263-297.
11. Carvalho G.R. 1993. Evolutionary aspects of fish distribution: genetic variability and adaptation. J. Fish Biol. 43: 53-73.
12. Castonguay M., Simard P., Gagnon P. 1991. Usefulness of Fourier analysis of otolith shape for Atlantic mackerel (Scomber scombrus) stock discrimination. Can. J. Fish. Aquat. Sci. 48: 296-302.
13. Clarke L.M., Thorrold S.R., Conover D.O. 2011. Population differences in otolith chemistry have a genetic basis in Menidia menidia. Can. J. Fish. Aquat. Sci. 68: 105-114.
14. Excoffier L., Laval G., Schneider S. 2005. Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evol. Bioinform. Online 1: 47-50.
15. Ferrito V., Maltagliati F., Mauceri A., Adorno A., Tigano C. 2003. Morphological and genetic variation in four Italian populations of Aphanius fasciatus (Teleostei, Cyprinodontidae). It. J. Zool. 70: 115-121.
16. Ferrito V., Mannino M.C., Pappalardo A.M., Tigano C. 2007. Morphological variation among populations of Aphanius fasciatus Nardo, 1827 (Teleostei, Cyprinodontidae) from the Mediterranean. J. Fish Biol. 70: 1-20.
17. Frankham R. 1995. Conservation genetics. Annu. Rev. Gen. 29: 305-327.
18. Fuller R.C. 2008. Genetic incompatibilities in killifish and the role of environment. Evolution 62: 3056-3068.
19. Ghigliotti L., Mazzei F., Ozouf-Costaz C., Christiansen J.S., Fevolden S.E., Pisano E. 2008. First cytogenetic characterization of the sub-arctic marine fish Mallotus villosus (Müller, 1776), Osmeriformes, Osmeridae. Genet. Mol. Biol. 31: 180-187.
20. Girone A., Nolf D. 2009. Fish otoliths from the Priabonian (Late Eocene) of North Italy and South-East France - Their paleobiogeographical significance. Rev. Micropal. 52: 195-218.
21. Gouy M., Guindon S., Gascuel O. 2010. SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol. Biol. Evol. 27: 221-224.
22. Guindon S., Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52: 696-704.
23. Hall T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41: 95-98.
24. Hrbek T., Meyer A. 2003. Closing of the Tethys sea and phylogeny of Eurasian killifishes (Cyprinodontiformes: Cyprinodontidae). J. Evol. Biol. 16: 17-36.
25. Huelsenbeck J. P., Ronquist F. 2001. MRBAYES: Bayesian inference of phylogeny. Bioinform. 17: 754-755.
26. Humboldt F.H.A., Valenciennes A. 1821. Recherches sur les poissons fluviatiles de l'Amérique Equinoxiale. In: Humboldt F.H.A., de Bonpland A.J.A. (eds), Voyage de Humboldt et Bonpland, Vol. 2. Schoell et Dufour, Paris, p. 160.
27. Kishino H., Miyata T., Hasegawa M. 1990. Maximum likelihood inference of protein phylogeny and the origin of chloroplasts. J. Mol. Evol. 30: 151-160.
28. Kumar S., Tamura K., Nei M. 2004. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform. 5: 150-163.
29. Lambeck K., Esat T.M., Potter E.K. 2002. Links between climate and sea levels for the past three million years. Nature 419: 199-206.
30. Leis J.M., Van Herwerden L., Patterson H.M. 2011. Estimating connectivity in marine fish populations: What works best? Oceanogr. Mar. Biol. Annu. Rev. 49: 193-234.
31. Lombarte A., Palmer M., Matallanas J., Gómez-Zurita J., Morales-Nin B. 2010. Ecomorphological trends and phylogenetic inertia of otolith sagittae in Nototheniidae. Environ. Biol. Fish. 89: 607-618.
32. Maltagliati F. 1999. Genetic divergence in natural populations of the Mediterranean brackish-water killifish Aphanius fasciatus. Mar. Ecol. Prog. Ser. 179: 155-162.
33. Maltagliati F., Domenici P., Franch Fosch C., Cossu P., Casu M., Castelli A. 2003. Small-scale morphological and genetic differentiation in the Mediterranean killifish Aphanius fasciatus (Cyprinodontidae) from a coastal brackish-water pond an adjacent pool in northern Sardinia. Oceanol. Acta 26: 111-119.
34. Martin C.H., Wainwright P.C. 2011. Trophic novelty is linked to exceptional rates of morphological diversification in two adaptive radiations of Cyprinodon pupfish. Evolution 65: 2197-2212.
35. Mejri R., Brutto S.L., Hassine O.K.B., Arculeo M. 2009. A study on Pomatoschistus tortonesei Miller 1968 (Perciformes, Gobiidae) reveals the Siculo-Tunisian Strait (STS) as a breakpoint to gene flow in the Mediterranean basin. Mol. Phyl. Evol. 53: 596-601.
36. Mérigot B., Letourneur Y., Lecomte-Finiger R. 2007. Characterization of local populations of the common sole Solea solea (Pisces, Soleidae) in the NW Mediterranean through otolith morphometrics and shape analysis. Mar. Biol. 151: 997-1008.
37. Messaoudi I., Kessabi K., Kacem A., Said K. 2009. Incidence of spinal deformities in natural populations of Aphanius fasciatus Nardo, 1827 from the Gulf of Gabes, Tunisia. Afr. J. Ecol. 47: 360-366.
38. Milana V., Franchini P., Sola L., Angiulli E., Rossi A.R. 2012. Genetic structure in lagoons: the effects of habitat discontinuity and low dispersal ability on populations of Atherina boyeri. Mar. Biol. 159: 399-411.
39. Monteiro L.R., Di Beneditto A.P.M., Guillermo L.H., Rivera L.A. 2005. Allometric changes and shape differentiation of sagitta otoliths in sciaenid fishes. Fish. Res. 74: 288-299.
40. Nolf D. 1985. Otolithi piscium. Handbook of paleoichthyology. Gustav Fischer, Stuttgart, New York.
41. Nolf D. 1995. Studies on fossil otoliths - The state of the art. In: Secor D.H., Dean J.M., Campana S.E. (eds), Recent Developments in Fish Otolith Research. University of South Carolina Press, Columbia, SC, pp. 513-544.
42. Pappalardo A.M., Ferrito V., Messina A., Guarino F., Patarnello T., de Pinto V., Tigano C. 2008. Genetic structure of the killifish Aphanius fasciatus, Nardo 1827 (Teleostei, Cyprinodontidae), results of mitochondrial DNA analysis. J. Fish Biol. 72: 1154-1173.
43. Popper A.N., Ramcharitar J.U., Campana S.E. 2005. Why otoliths? Insights from inner ear physiology and fisheries biology. Mar. Fresh. Res. 56: 497-504.
44. Posada D. 2008. jModelTest: Phylogenetic Model Averaging. Mol. Biol. Evol. 25: 1253-1256.
45. Reichenbacher B., Sienknecht U. 2001. Allopatric divergence and genetic diversity of Recent Aphanius iberus and fossil Prolebias meyeri (Teleostei, Cyprinodontidae) from southwest and western Europe, as indicated by otoliths. Geobios 34: 69-83.
46. Reichenbacher B., Feulner G.R., Schulz-Mirbach T. 2009a. Geographic Variation in Otolith Morphology Among Freshwater Populations of Aphanius dispar (Teleostei, Cyprinodontiformes) from the Southeastern Arabian Peninsula. J. Morph. 270: 469-484.
47. Reichenbacher B., Kamrani E., Esmaeili H.R., Teimori A. 2009b. The endangered cyprinodont Aphanius ginaonis (Holly, 1929) from southern Iran is a valid species: evidence from otolith morphology. Environ. Biol. Fish. 86: 507-521.
48. Reichenbacher B., Sienknecht U., Küchenhoff H., Fenske N. 2007. Combined otolith morphology and morphometry for assessing taxonomy and diversity in fossil and extant killifish (Aphanius, †Prolebias). J. Morph. 268: 898-915.
49. Rocco L., Ferrito V., Costagliola D., Marsilio A., Pappalardo A.M., Stingo V., Tigano C. 2007. Genetic divergence among and within four Italian populations of Aphanius fasciatus (Teleostei, Cyprinodontiformes). It. J. Zool. 74: 371-379.
50. Ronquist F., Huelsenbeck J.P. 2003. MrBayes 3, Bayesian phylogenetic inference under mixed models. Bioinform. 19: 1572-1574.
51. Ronquist F., Huelsenbeck J.P., Van der Mark P. 2005. MrBayes 3.1 Manual. Available at http://mrbayes.csit.fsu.edu/ Accessed date May 2007.
52. Rozas J., Sánchez-Delbarrio J.C., Messeguer X., Rozas R. 2003. DnaSP, DANN polymorphism analyses by the coalescent and other methods. Bioinform. 19: 2496-2497.
53. Schwarzhans W., Bratishko A. 2011. The otoliths from the middle Paleocene of Luzanivka (Cherkasy district, Ukraine). N. Jb. Geol. Pal. Abh. 261: 83-110.
54. Shimodaira H., Hasegawa H. 1999. Multiple comparisons of loglikelihoods with applications to phylogenetic inference. Mol. Biol. Evol. 16: 1114-1116.
55. Smale M.J., Watson G., Hecht T. (eds). 1995. Otolith atlas of southern African marine fishes (Ichthyological Monographs). J.L.B. Smith Institute of Ichthyology, Grahamstown.
56. Sollner-Webb B., Mougey E.B. 1991. News from the nucleolus: rRNA gene expression. Trends Biochem. Sci. 16: 58-62.
57. SPSS Inc. 2011. SPSS. Ver. 19.0. Base. Chicago, IL: SPSS, Inc.
58. Stepien C. A., Rosenblatt R.H., Bargmeyer B.A. 2001. Phylogeography of the spotted sand bass, Paralabrax maculatofasciatus: divergence of Gulf of California and Pacific coast populations. Evolution 55: 1852-1862.
59. Stransky C., Baumann H., Fevolden S.E., Harbitz A., Høie H., Nedreaas K.H., Salberg A.B., Skarstein T. 2008. Separation of Norwegian coastal cod and Northeast Arctic cod by outer otolith shape analysis. Fish. Res. 90: 26-35.
60. Swofford D.L. 2003. PAUP*: Phylogenetic analysis using parsimony (* and other methods), version 4.0b10. Sinauer Associates, Sunderland, MA.
61. Tamura K., Nei M. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10: 512-526.
62. Teimori A., Schulz-Mirbach T., Esmaeili H.R., Reichenbacher B. 2012a. Geographical differentiation of Aphanius dispar (Teleostei: Cyprinodontidae) from Southern Iran. J. Zool. Sys. Evol. Res. 50: 289-304.
63. Teimori A., Jawad L.A.J., Al-Kkarusi L.H., Al-Mamry J.N., Reichenbacher B. 2012b. Late Pleistocene to Holocene diversification and zoogeography of the Arabian killifish Aphanius dispar inferred from otolith morphology. Sci. Mar. 76: 637-645.
64. Tigano C., Ferrito V., Nicosia R. 1999. Morphological analysis of the pharyngeal jaws in two populations of Aphanius fasciatus Valenciennes, 1821 (Teleostei: Cyprinodontidae). J. Morph. 241: 107-114.
65. Tigano C., Ferrito V., Adorno A., Mannino M.C., Mauceri A. 2001. Pharyngeal and oral jaw differentiation in five populations of Aphanius fasciatus (Teleostei, Cyprinodontidae). It. J. Zool. 68: 201-206.
66. Tigano C., Canapa A., Ferrito V., Barucca M., Arcidiacono I., Olmo E. 2004. Osteological and molecular analysis of three Sicilian populations of Aphanius fasciatus (Teleostei, Cyprinodontidae). It. J. Zool. 71: 107-113.
67. Tigano C., Canapa A., Ferrito V., Barucca M., Arcidiacono I., Deidon A., Schembri P.J., Olmo E. 2006. A study of osteological and molecular differences in populations of Aphanius fasciatus Nardo, 1827, from the central Mediterranean (Teleostei, Cyprinodontidae). Mar. Biol. 149: 1539-1550.
68. Torres G.J., Lombarte A., Morales-Nin B. 2000. Sagittal otolith size and shape variability to identify intraspecific differences in three species of the genus Merluccius. J. Mar. Biol. Ass. U.K. 80: 333-342.
69. Torres-Machorro A.L., Hernandez R., Cevallos A.M., Lopez-Villasenor I. 2010. Ribosomal RNA genes in eukaryotic microorganisms: witnesses of phylogeny? FEMS Microbiol. Rev. 34: 59-86.
70. Triantafyllidis A., Leonardos I., Bista I., Kyriazis I.D., Stoumboudi M.T., Kappas I., Amat F., Abatzopoulos T.J. 2007. Phylogeography and genetic structure of the Mediterranean killifish Aphanius fasciatus (Cyprinodontidae). Mar. Biol. 152: 1159-1167.
71. Tuset V.M., Lombarte A., Assis C. 2008. Otolith atlas for the western Mediterranean, north and central eastern Atlantic. Sci. Mar. 72S1: 7-198.
72. Vignon M., Morat F. 2010. Environmental and genetic determinant of otolith shape revealed by a nonindigenous tropical fish. Mar. Ecol. Prog. Ser. 411: 231-241.
73. Villwock W. 1994. On micropopulations in fish and their effects on differentiation and speciation. In: Remmer H. (ed.), Minimum Animal Populations. Ecol. Stud. 106. Springer, Berlin, pp. 51-65.
74. Volpedo A.V., Cirelli A.F. 2006. Otolith chemical composition as a useful tool for sciaenid stock discrimination in the south-western Atlantic. Sci. Mar. 70: 325-334.
75. Volpedo A.V., Echeverría D.D. (eds) 2000. Catálogo y claves de otolitos para la identificación de peces del Mar Argentino. 1. Peces de importancia comercial. Editorial Dunken, Buenos Aires.
76. Wildekamp R.H. 1993. The genus Aphanius Nardo. In: Watters B.R. (ed.), A World of Killies, Atlas of the Oviparous Cyprinodontiform Fishes of the World. American Killifish Association, Mishawaka, IN., pp. 19-67.
77. Williams D.A., Brown S.D., Crawford D.L. 2008. Contemporary and historical influences on the genetic structure of the estuarine-dependent Gulf killifish Fundulus grandis. Mar. Ecol. Prog. Ser. 373: 111-121.
78. Wilson A.C., Cann R.L., Carr S.M., Geroge M., Gyllensten U.B., Helm-Bychowski K.M., Higuchi R.G., Palumbi S.R., Prager E.M., Sage R.D., Stoneking M. 1985. Mitochondrial DNA and two perspectives on evolutionary genetics. Biol. J. Linn. Soc. 26: 375-400.
79. Woods R.J., Macdonald J.I., Crook D.A, Schmidt D.J., Hughes J.M. 2010. Contemporary and historical patterns of connectivity among populations of an inland river fish species inferred from genetics and otolith chemistry. Can. J. Fish. Aquat. Sci. 67: 1098-1115.