Skip to main content

Advertisement

SpringerLink
Log in

Genetic diversity of the killifish Aphanius fasciatus paralleling the environmental changes of Tarquinia salterns habitat

  • Original Research
  • Published:
Genetica Aims and scope Submit manuscript

Abstract

The habitat in the Natural Reserve of the Tarquinia salterns, located on the Tyrrhenian coast of central Italy, has undergone dramatic alterations over the last 10 years. After salt production was terminated in 1997 the site was abandoned until 2002, with consequent degradation of habitat quality and stiffening of the environmental conditions. From 2003 to 2006 ecological rehabilitation of the site was carried out, restoring water circulation to its previous equilibrium. The genetic variation in the killifish Aphanius fasciatus inhabiting the salterns was monitored using allozymes from 1998. The results showed that the genetic variability of the killifish strongly reduced through time: a high number of rare alleles were lost and both heterozygosity and allele richness were significantly decreased. The most recent samples, taken after the ecological restoration, showed that to date the genetic erosion of A. fasciatus gene pool has slowed down, since no significant differences have been detected for any genetic variability parameter. Concerning the mechanisms leading to the impoverishment of the genetic variability, the strong loss of rare alleles suggests a role of genetic drift, which accords with the fluctuation of the effective population size recorded over the period of study and with the low gene flow typical of this species. The low levels of gene flow reported for this species imply that once lost, the genetic variability can rarely be restored through immigration from highly variable populations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Barcia AR, López GE, Hernández D, García-Machado E (2005) Temporal variation of the population structure and genetic diversity of Farfantepenaeus notialis assessed by allozyme loci. Mol Ecol 14:2933–2942

    Article  CAS  Google Scholar 

  • Belfiore NM, Anderson SL (2001) Effects of contaminants on genetic patterns in aquatic organisms: a review. Mutat Res 489:97–122

    Article  CAS  PubMed  Google Scholar 

  • Bickham JW, Sandhu S, Hebert PDN, Chikhi L, Athwal R (2000) Effects of chemical contaminants on genetic diversity in natural populations: implications for biomonitoring and ecotoxicology. Mutat Res 463:33–51

    Article  CAS  PubMed  Google Scholar 

  • Blasi S (2006) Structure, seasonal fluctuations and response to disturbance of macroinvertebrate assemblages in hyperaline mediterranean habitat: Tarquinia saltpans. PhD Thesis, University of Tuscia, Viterbo (Italy), p 145. Available from http://dspace.unitus.it/dspace/handle/2067/109

  • Boessenkool S, Star B, Seddon PJ, Waters JM (2010) Temporal genetic samples indicate small effective population size of the endangered yellow-eyed penguin. Conserv Genet 11:539–546

    Article  Google Scholar 

  • Bramucci S (2009) Analysis of macrozoobentic and planktonic communities in a hypersaline aquatic environment: Tarquinia Salterns. PhD Thesis, University of Tuscia, Viterbo (Italy), p 150

  • Carroll SP, Hendry AP, Reznick DN, Fox CW (2007) Evolution on ecological time-scales. Funct Ecol 21:387–393

    Article  Google Scholar 

  • Cimmaruta R, Iaconelli M, Nascetti G, Bullini L (1998) Diversitá genetica in popolazioni di grandi pelagici del Mediterraneo. Biol Mar Medit 5:300–310

    Google Scholar 

  • Cimmaruta R, Scialanca F, Luccioli F, Nascetti G (2003) Genetic diversity and environmental stress in Italian populations of the cyprinodont fish Aphanius fasciatus. Oceanol Acta 26:101–110

    Article  Google Scholar 

  • Cimmaruta R, Bondanelli P, Nascetti G (2005) Genetic structure and environmental heterogeneity in the European hake (Merluccius merluccius). Mol Ecol 14:2577–2591

    Article  CAS  PubMed  Google Scholar 

  • Cimmaruta R, Bondanelli P, Ruggi A, Nascetti G (2008) Genetic structure and temporal stability in the horse mackerel (Trachurus trachurus). Fish Res 89:114–121

    Article  Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for inferring recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    CAS  PubMed  Google Scholar 

  • DiBattista JD (2008) Patterns of genetic variation in anthropogenically impacted populations. Conserv Genet 9:141–156

    Article  Google Scholar 

  • Eanes WF (2002) Analysis of selection on enzyme polymorphisms. Annu Rev Ecol Syst 30:301–326

    Article  Google Scholar 

  • El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree (Argania spinosa (L.) Skeels) endemic to Morocco. Theor Appl Genet 92:832–839

    Article  Google Scholar 

  • Fischer W, Schneider M, Bauchot ML (1987) Fiches FAO d’identification des espèces pour les besoins de la pêche. Mèditerranèe et Mer Noire, (Zone de la pêche 37). Revision I. Volume II. Vertèbrès. FAO CEE, Rome, pp 761–1529

    Google Scholar 

  • Frankham R (1995) Conservation genetics. Annu Rev Genet 29:305–327

    Article  CAS  PubMed  Google Scholar 

  • Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10:1500–1508

    Article  Google Scholar 

  • Fraser DJ, Hansen MM, Ostergaard S, Tessier N, Legault M, Bernatchez L (2007) Comparative estimation of effective population sizes and temporal gene flow in two contrasting population system. Mol Ecol 16:3866–3889

    Article  PubMed  Google Scholar 

  • Funk WC, Forsman ED, Johnson M, Mullins TD, Haig SM (2010) Evidence for recent population bottlenecks in northern spotted owls (Strix occidentalis caurina). Conserv Genet 11:1013–1021

    Article  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from http://www2.unil.ch/popgen/softwares/fstat.htm. Updated from Goudet (1995) FSTAT version 1.2: a computer program to calculate F-statistics. J Hered 86:485–486

  • Gysels ES, Leentjes V, Volckaert FAM (2004) Small-scale clinal variation, genetic diversity and environmental heterogeneity in the marine gobies Pomatoschistus minutus and P. lozanoi (Gobiidae, Teleostei). Heredity 93:208–214

    Article  CAS  PubMed  Google Scholar 

  • Hartl DL, Clark AG (1989) Principles of population genetics. Sinauer Associates, Sunderland

    Google Scholar 

  • Hauser L, Adcock GJ, Smith PJ, Bernal Ramirez JH, Carvalho GR (2002) Loss of microsatellite diversity and low effective population size in an overexploited population of New Zealand snapper (Pagrus auratus). Proc Natl Acad Sci USA 99:11742–11747

    Article  CAS  PubMed  Google Scholar 

  • Hedgecock D (1994) Does variance in reproductive success limit effective population sizes of marine organisms? In: Beaumont AR (ed) Genetics and evolution of aquatic organisms. Chapman & Hall, London, pp 122–134

    Google Scholar 

  • Hedrick PW (2000) Genetics of populations. Jones and Bartlett Publishers, Sudbury

    Google Scholar 

  • Hewitt GM (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913

    Article  CAS  PubMed  Google Scholar 

  • Hoarau G, Piquet AMT, Rijnsdorp AD, Van Der Veer HW, Stam WT, Olsen JL (2004) Population structure of plaice (Pleuronectes platessa) in northern Europe: a comparison of resolving power between microsatellite and mtDNA data. J Sea Res 51:183–190

    Article  CAS  Google Scholar 

  • Hoarau G, Boon E, Jongma DN, Ferber S, Palsson J, Van der Veer HW, Rijnsdorp AD, Stam WT, Olsen JL (2005) Low effective population size and evidence for inbreeding in an overexploited flatfish, plaice (Pleuronectes platessa L.). Proc R Soc B Biol Sci 272:497–503

    Article  Google Scholar 

  • Hoelzel AL (1999) Impact of population bottlenecks on genetic variation and the importance of life-history; a case study of the northern elephant seal. Biol J Linn Soc 68:23–39

    Article  Google Scholar 

  • Hoffmann AA, Willi Y (2008) Detecting genetic responses to environmental change. Nat Rev Genet 9:421–432

    Article  CAS  PubMed  Google Scholar 

  • Hutchinson WF, van Oosterhout C, Rogers SI, Carvalho GR (2003) Temporal analysis of archived samples indicates marked genetic changes in declining North Sea cod (Gadus morhua). Proc R Soc B Biol Sci 270:2125–2132

    Article  Google Scholar 

  • Kidwell DM, Lewitus AJ, Brandt S, Jewett EB, Mason DM (2009) Ecological impacts of hypoxia on living resources. J Exp Mar Biol Ecol 381(Suppl 1):S1–S3

    Article  Google Scholar 

  • Kimura M, Crow JF (1964) The number of alleles that can be maintained in a finite population. Genetics 49:725–738

    CAS  PubMed  Google Scholar 

  • Krafsur SE (2002) Population structure of the tsetse fly Glossina pallidipes estimated by allozyme, microsatellite and mitochondrial gene diversities. Insect Mol Biol 11:37–45

    Article  CAS  PubMed  Google Scholar 

  • Lardicci C, Rossi F, Castelli A (1997) Analysis of macrozoobenthic community structure after severe dystrophic crises in a mediterranean coastal lagoon. Mar Pollut Bull 34:536–547

    Article  CAS  Google Scholar 

  • Lardicci C, Como S, Corti S, Rossi F (2001) Recovery of the macrozoobenthic community after severe dystrophic crises in a mediterranean coastal lagoon (Orbetello, Italy). Mar Pollut Bull 42:202–214

    Article  CAS  PubMed  Google Scholar 

  • Leonardos I, Sinis A (1998) Reproductive strategy of Aphanius fasciatus Nardo, 1827 (Pisces, Cyprinodontidae) in the Mesolongi and Etolikon lagoons (W. Greece). Fish Res 35:171–181

    Article  Google Scholar 

  • Leonardos I, Sinis A (1999) Population age and sex structure of Aphanius fasciatus Nardo, 1827 (Pisces, Cyprinodontidae) in the Mesolongi and Etolikon lagoons (W. Greece). Fish Res 40:227–235

    Article  Google Scholar 

  • Luikart G, Sherwin WB, Steele BM, Allendorf FW (1998) Usefulness of molecular markers for detecting population bottlenecks via monitoring genetic change. Mol Ecol 7:963–974

    Article  CAS  PubMed  Google Scholar 

  • Maes GE, Raeymaekers JAM, Pampoulie C, Seynaeve A, Goemans G, Belpaire C, Volckaert FAM (2005) The catadromous European eel Anguilla anguilla (L.) as a model for freshwater evolutionary ecotoxicology: relationship between heavy metal bioaccumulation, condition and genetic variability. Aquat Toxicol 73:99–114

    Article  CAS  PubMed  Google Scholar 

  • Maltagliati F (1998a) Preliminary investigation of allozyme genetic variation and population geographical structure in Aphanius fasciatus from Italian brackish-water habitats. J Fish Biol 52:1130–1140

    CAS  Google Scholar 

  • Maltagliati F (1998b) Does the Mediterranean killifish Aphanius fasciatus (Teleostei: Cyprinodontidae) fit the one-dimensional stepping-stone model of gene flow? Environ Biol Fish 53:385–392

    Article  Google Scholar 

  • Maltagliati F (1999) Genetic divergence in natural populations of the Mediterranean brackish-water killifish Aphanius fasciatus. Mar Ecol Prog Ser 179:155–162

    Article  Google Scholar 

  • Maltagliati F, Camilli L (2000) Temporal genetic variation in a population of Aphanius fasciatus (Cyprinodontidae) from a brackish-water habitat at Elba Island (Italy). Env Biol Fish 57:107–112

    Article  Google Scholar 

  • Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10

    Article  Google Scholar 

  • Nevo E (2001) Evolution of genome-phenome diversity under environmental stress. PNAS 98:6233–6240

    Article  CAS  PubMed  Google Scholar 

  • Nevo E, Noy R, Lavie B, Beiles A, Muchtar S (1986) Genetic diversity and resistance to marine pollution. Biol J Linn Soc 29:139–144

    Article  Google Scholar 

  • Nowak C, Vogt C, Pfenninger M, Schwenk K, Oehlmann J, Streit B, Oetken M (2009) Rapid genetic erosion in pollutant-exposed experimental chironomid populations. Environ Pollut 157:881–886

    Article  CAS  PubMed  Google Scholar 

  • Nunney L (1996) The influence of variation in female fecundity on effective population size. Biol J Linn Soc 59:411–425

    Article  Google Scholar 

  • Ozbek O, Millet E, Anikster Y, Arslan O, Feldman M (2007) Spatio-temporal genetic variation in populations of wild emmer wheat, Triticum turgidum ssp. dicoccoides, as revealed by AFLP analysis. Theor Appl Genet 115:19–26

    Article  CAS  PubMed  Google Scholar 

  • Palstra FP, Ruzzante DE (2008) Genetic estimates of contemporary effective population size: what can they tell us about the importance of genetic stochasticity for wild populations persistence? Mol Ecol 17:3428–3447

    Article  PubMed  Google Scholar 

  • Piry SG, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective populations size using allele frequency data. J Hered 90:502–503

    Article  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetic software for exact test and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Ryman N, Utter F, Laikre L (1995) Protection of intraspecific biodiversity of exploited fishes. Rev Fish Biol Fish 5:417–446

    Article  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) ARLEQUIN Ver. 2.000: a software for population genetics data analysis. Genetics and Biometry Laboratory, University of Geneva, Geneva

    Google Scholar 

  • Schwartz MK, Luikart G, Waples RS (2007) Genetic monitoring as a promising tool for conservation and management. TREE 22:25–33

    PubMed  Google Scholar 

  • Smith PJ, Francis RICC, McVeagh M (1991) Loss of genetic diversity due to fishing pressure. Fish Res 10:309–316

    Article  Google Scholar 

  • Spear SF, Petesron CR, Matocq MD, Storfer A (2006) Molecular evidence for historical and recent population size reductions of tiger salamanders (Ambystoma tigrinum) in Yellowstone National Park. Conserv Genet 7:605–611

    Article  Google Scholar 

  • Stanton ML, Roy BA, Thiede DA (2000) Evolution in stressful environments. I. Phenotypic variability, phenotypic selection, and response to selection in five distinct environmental stresses. Evolution 54:93–111

    CAS  PubMed  Google Scholar 

  • Swofford DL, Selander RB (1999) BIOSYS-2: a computer program for the analysis of allelic variation in population genetics. University of Illinois at Urbana-Champaign, Urbana

    Google Scholar 

  • Tortonese E (1986) Cyprinodontidae. In: Whitehead PJP, Bauchot ML, Hureau JC, Nielsen J, Tortonese E (eds) Fishes of the north-eastern Atlantic and the Mediterranean. UNESCO, Paris, pp 1341–1345

    Google Scholar 

  • Turner TF, Wares JP, Gold JR (2002) Genetic effective size is three order of magnitude smaller than adults census size in an abundant, estuarine-dependant marine fish (Sciaenops ocellatus). Genetics 162:1329–1339

    PubMed  Google Scholar 

  • Ungherese G, Mengoni A, Somigli S, Baroni D, Focardi S, Ugolini A (2010) Relationship between heavy metals pollution and genetic diversity in Mediterranean populations of the sandhopper Talitrus saltator (Montagu) (Crustacea, Amphipoda). Environ Pollut 158:1638–1643

    Article  CAS  PubMed  Google Scholar 

  • van Straalen NM, Timmermans JTN (2002) Genetic variation in toxicant-stressed populations: an evaluation of the “genetic erosion” hypothesis. Hum Ecol Risk Assess 5:983–1002

    Article  Google Scholar 

  • Vucetich JA, Waite TA, Nunney L (1997) Fluctuating population size and the ratio of effective to census population size. Evolution 51:2017–2021

    Article  Google Scholar 

  • Wang J (2001) A pseudo-likelihood method for estimating effective population size from temporally spaced samples. Genet Res 78:243–257

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Whitlock MC (2003) Estimating effective population size and migration rates from genetic samples over space and time. Genetics 163:429–446

    CAS  PubMed  Google Scholar 

  • Waples RS (1989) A generalized approach for estimating effective population size from temporal changes in allele frequency. Genetics 121:379–391

    CAS  PubMed  Google Scholar 

  • Waples RS (1991) Genetic methods for estimating the effective size of Cetacean populations. Report Int Whaling Commission Spec Issue 13:279–300

    Google Scholar 

  • Waples RS, Yokota M (2007) Temporal estimates of effective populations size in species with overlapping generations. Genetics 175:219–233

    Article  PubMed  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Willi Y, Van Buskirk J, Schmid B, Fischer M (2007) Genetic isolation of fragmented populations is exacerbated by drift and selection. J Evol Biol 20:534–542

    Article  CAS  PubMed  Google Scholar 

  • Williamson-Natesan EG (2005) Comparison of methods for detecting bottlenecks from microsatellite loci. Conserv Genet 6:551–562

    Article  Google Scholar 

Download references

Acknowledgments

This study forms part of a EU LIFE-NATURA project “Environmental rehabilitation of the Natural Reserve of Tarquinia Salt-works” (LIFE02NAT/IT/8523), carried out with the contribution of the European Commission, Directorate-General Environment. We wish to thank Paola Bondanelli and Alessandra Pontremolesi for their valuable help in data collection and Sara Rosenman for reviewing the English text. We also thank three anonymous referees for their valuable observations.

Author information

Authors and Affiliations

  1. Department of Ecology and Sustainable Economic Development, Tuscia University, Largo dell’Università, 01100, Viterbo, Italy

    Dario Angeletti, Roberta Cimmaruta & Giuseppe Nascetti

Authors
  1. Dario Angeletti
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Roberta Cimmaruta
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Giuseppe Nascetti
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dario Angeletti.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Angeletti, D., Cimmaruta, R. & Nascetti, G. Genetic diversity of the killifish Aphanius fasciatus paralleling the environmental changes of Tarquinia salterns habitat. Genetica 138, 1011–1021 (2010). https://doi.org/10.1007/s10709-010-9487-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-010-9487-3

Keywords

Search

Navigation