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Aphanius Fasciatus MARINE ECOLOGY PROGRESS SERIES Vol. 179: 155-162.1999 Published April 15 Mar Ecol Prog Ser Genetic divergence in natural populations of the Mediterranean brackish-water killifish Aphanius fasciatus Ferruccio Maltagliati* Dipartimento di Scienze dell'uomo e dellrAmbiente.Universita di Pisa, Via Volta 6, 1-56126 Pisa, Italy ABSTRACT: Samples of the brackish-water cyprinodontid fish Aphanius fasciatus from 11 Medter- ranean coastal brackish-water habitats were examined for variation at 43 allozyme loci. Sixteen loci were polymorphic in at least 1 population. Estimates of genetic variability revealed low levels of poly- morphism, with mean effective number of alleles per locus ranging from 1.02 (SE 0.01) to 1.10 (SE 0.04) and average expected heterozygosity values from 0.013 (SE 0.007) to 0.062 (SE 0.022). The mean Weir & Cockerham f = 0.060 (SE 0.019) confirmed the general concordance with Hardy-Weinberg equilib- rium within populations assessed by exact tests. The presence of various private alleles and the mean value of the coancestry coefficient, 0- 0.507 (SE 0.078),indicated a marked genetic dvergence among populations. Nei's genetic distance values were characteristic of populations within species, ranging from 0.001 (SE 0.000) to 0.098 (SE 0.044). Genetic affinities obtained by UPGMA cluster analysis were consistent with the geographical distribution of populations. The hgh degree of genetic divergence among A. fasciatus populations corresponds to the naturally fragmented distribution of the species and to restricted gene flow between populations, due to the limited dispersal potential of the species. Fur- thermore, genetic and geographical distances between populations are consistent with the prediction that the species is genetically structured by isolation by distance. KEY WORDS: Isolation by distance . Genetic structure . Heterozygosity . Life history traits . Cyprino- dontidae . Allozymes . Mediterranean INTRODUCTION isolation of natural populations is particularly consider- able where strong habitat constraints exist, such as in The study of the population genetic structure of a fresh- or brackish-water habitats. In fact, the evolu- species and the mechanisms that could have generated tionary and ecological importance of these habitats that pattern requlres knowledge of the geographical depends on the ways in which species use them and on distribution of genetic variation. The study of the the extent of the portion of the life cycle spent in such genetic structure of a species, which can be caused by habitats. both life history traits and habitat constraints, may Aphanius fasciatus Nardo, 1827, is a cyprinodontid allow us to infer the extent to which these aspects euryhaline fish naturally located in many brackish- affect the distribution of genetic variation (Soule & water habitats along Mediterranean coasts. It is an Wilcox 1986, Lande 1988). In particular, the dispersal endemic species found in the whole Mediterranean potential related to life history characteristics appears region, with the exception of the easternmost and to play an important role in determining the genetic westernmost coasts, where it is replaced by A. dispar variability and population structure of fish species (Riippel, 1828) and A. iberus (Valenciennes, 1846), (Gyllensten 1985, Waples 1987, Ward et al. 1994).The respectively (Villwock 1982, Bianco 1995).A. fasciatus may spend its whole life cycle in brackish waters, showing fidelity to its habitats. The species has a rela- 0 inter-Research iSSS Resale of full arlcle not perrnjtted 156 Mar Ecol Prog Ser 179: 155-162, 1999 tively sedentary life history, with large demersal eggs and without larval dispersal stages. Despite adults 0CCL 100 200 showing high mobility, it has been hypothesised that Km their migration from one population to another occurs only as a consequence of occasional and stoch.astic events, such as exceptional rainfalls or floods, which force migration along coastal seawater andlor through transitory inland water pathways (Maltagliati 1998a,b). Therefore, all the above-mentioned characteristics, together with the natural fragmentation of brackish- water habitats, favour isolation of populations. Since Aphanius fasciatus is important neither as a source of food nor for aquariology purposes, the translocation of individuals, which could result in the establishment of less fit genotypes reducing popula- tion fitness through the disruption of coadapted genomes (Shaklee et al. 1993),can be excluded. Thus, Ty rrhenian this fish is particularly appropriate for the study of the genetic variation resulting from natural events, given that populations have not been manipulated and can be considered to reflect the natural distribution of genotypes. Previous preliminary allozyme investiga- tions have shown considerable levels of population genetic divergence in A. fasciatus, allowing the hypothesis of a species genetic structure following the isolation by distance (Maltagliati 1998a,b). The aim of this work was to extend the study of the genetic variability within and among populations of Aphanius fasciatus by means of allozyme markers, in order to gain information on the genetic structure of l O0E the species and on the relationships among natural Fig. 1. Localities where Aphanius fasciatus was sampled. The populations of this teleost. Furthermore, the present numbers of individuals analysed for each locality are in study highlights the importance of interactions parentheses. See 'Materials and methods' for explanation of between life history characteristics, species biology, population abbreviations and environmental constraints in determining the genetic structure and the dispersal potential of A. fas- ciatus. lagoon (COM, 44" 41' N. 12" 11' E). Thirty individuals collected in the CAS, ELB, ORB, PI0 and SAB popula- tions have been analysed in previous research, repre- MATERIALS AND METHODS senting pilot studies for the present investigation (Mal- tagliati 1998a,b).Samples were obtained using either a Sample collection. Samples of Aphanius fasciatus hand-net or small fish-traps, baited with anchovy fillets were collected from natural populations in 11 brack- and placed in shallow water with abundant benthic ish-water habitats of the central Mediterranean (Fig. 1) vegetation. Live specimens of some samples were in the period between October 1994 and June 1996. brought to the laboratory and killed in distilled water The sites were Biguglia coastal pond (BIG, 42"38'N, and ice, others were shipped to the laboratory in dry 09" 28' E); a man-made canal near the city of Piombino ice. All individuals were placed in separate plastic (PIO, 42" 57' N, 10" 29' E); a brackish microhabitat at bags and stored at -80°C until processed for electro- Elba Island (ELB, 42" 48' N, 10" 19' E);the eastern basin phoresis. of Orbetello lagoon (ORB, 42" 26' N, 11" 12' E); Sabau- Electrophoretic methods. Cellulose acetate electro- dia lake (SAB, 41" 18' N, 13"OZ'E); Casaraccio coastal phoresis was conducted following the procedures out- pond (CAS, 40" 54' N, 08" 15' E); Marsala lagoon (MAR, lined in Maltagliati (1998a).Twenty-two enzymatic sys- 37" 50' N, 12" 29' E); the lake of Tunis (TUN, 36" 49' N, tems were analysed: alcohol dehydrogenase (ADH, 10" 16' E); Monastir lagoon (MON, 35" 46' N, 10" 47' E); E.C. 1.1.1.1);adenylate kinase (AK, E.C. 2.7.4.3);al- Lesina lake (LES, 41" 53' N. 15" 22' E); and Comacchio dolase (ALDO, E.C. 4.1.2.13); aldehyde oxidase (AO, Maltagliati: Genetic diverge]~ce in Aphan~us fasciatus 157 E.C. 1.2.3.1);creatine kinase (CK, E.C. 2.7.3.2);fructose mine genetic affinities among populations, Nei's (1978) biphosphatase (FBP, E.C. 3.1.3.11); fumarate hydratase genetic distance was calculated and standard errors (FH, E.C. 4.2.1.2); glyceraldehyde-3-phosphate dehy- were obtained by jackknifing over loci. On the basis of drogenase (GAPDH, E.C. 1.2.1.12); glucose dehydroge- the matrix of Nei's genetic distances a UPGMA nase (GDH, E.C. 1.1.1.47); glycerate dehydrogenase (unweighted pair-group method using arithmetic aver- (GLYDH, E.C. 1.l .l .29); glycerol-3-phosphate dehydro- age) dendrogram was constructed and subjected to a genase (GPD, E.C. 1.1.1.8); glucose-6-phosphate bootstrapping analysis with 1000 replicates. Finally, to dehydrogenase (GGPDH, E.C. 1.1.1.49); glucose-6- verify the correlation between genetic and geographi- phosphate isomerase (GPI, E.C. 5.3.1.g); isocitrate cal distance matrices, Mantel's test of the association dehydrogenase (NADP') (IDH, E.C. 1.1.1.42);L-lactate between 2 parameters in data matrices with internal dehydrogenase (LDH, E.C. 1.1.1.27);malate dehydro- correlation (Manly 1991) was carried out. Probabilities genase (MDH, E.C. 1.1.1.37);malic enzyme (ME, E.C. were read directly from the distribution of 5000 ran- 1.1.1.40);mannose-6-phosphate isomerase (MPI, E.C. domised matrices computed by permutations. 5.3.1.8); phosphogluconate dehydrogenase (PGDH, E.C. 1.1.1.44); phosphoglucomutase (PGM, E.C. 5.4.2.2);pyrroline dehydrogenase (PYDH, E.C. 1.5.1.12); RESULTS sorbitole dehydrogenase (SORD, E.C. 1.1.1.14). For each locus the most common allele of the refer- Samples were surveyed for 43 presumptive gene loci ence population (Orbetello lagoon population) was of which 16 were polymorphic in at least 1 population designated as '100, the other alleles were designated (Table 1). Heterozygotes were 2-banded (implying a as greater or lower values according to their elec- monomeric quaternary structure) for FBP', MPI' and trophoretic mobility. Calibration of alleles was accom- PGM' ; 3-banded (dimeric structure) for G6PDH-1' , plished by running specimens from different popula- G6PDH-2', GPI-1 ', GPI-2' , ME-2' , ME-3'; 5-banded tions on the same cellulose acetate membrane. (tetrameric structure) for LDH-1' and LDH-3'; and Nomenclature of enzymes, loci and alleles followed the broad but undefined (implying a multimeric but uncer- recommendations of Shaklee et al.
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