Skip to main content
Log in

Historical and recent reductions in genetic variation of the Sarotherodon galilaeus population in the Sea of Galilee

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

The Sea of Galilee has great significance as a natural habitat and a freshwater source for Israel. Anthropogenic impacts have been placing significant pressure on the species inhabiting this lake, among which is Sarotherodon galilaeus, an omnivorous fish with a relatively large population and significance for commercial fishing. An alarming decline in annual catch towards 2008 suggested that this unique population might be at risk. With that in mind, we characterized the current genetic variation of this species in Israel with reference to fish from Ghana, based on D-loop and microsatellite markers. Genetic variation and differentiation were found mostly among fish from Ghanaian localities and between fish from Israel and Ghana, whereas fish from all Israeli localities had uniform and limited variation, a signature compatible with historical founder effect followed by local adaptations. Such historical processes could leave a population vulnerable as reflected in the sudden and recent population decline. Comparing genetic variation between archived 30 year-old scales and modern lake fish revealed further reduction in genetic variation coincident with the recent population decline. Thus, a recently occurring genetic bottleneck had placed this unique and isolated population at an even higher risk. We carefully discuss the events leading to the current risk status for S. galilaeus in Israel and highlight the need for vigilant monitoring and active management to support a more sustainable future for this and other fish communities in this important habitat.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data accessibility

D-loop sequences by haplotype names are given in Online resources (Data File S1) and were deposited in the GenBank database under the accession numbers: KY940659-KY940710. Alignment of sequences from old scales to publically available COI sequences and to D-loop haplotypes are given in Online resources (Data File S2 and S3, respectively). Tables containing D-loop haplotype frequency and microsatellite genotypes by fish and population are given in Online resources (Tables S2 and S3, respectively).

References

  • Allan JD, Abell R, Hogan Z, Revenga C, Taylor BW, Welcomme RL, Winemiller K (2005) Overfishing of inland waters. Bioscience 55:1041–1051

    Article  Google Scholar 

  • Allendorf FW, England PR, Luikart G, Ritchie PA, Ryman N (2008) Genetic effects of harvest on wild animal populations. Trends Ecol Evol 23:327–337

    Article  PubMed  Google Scholar 

  • Allendorf FW, Berry O, Ryman N (2014) So long to genetic diversity, and thanks for all the fish. Mol Ecol 23:23–25

    Article  PubMed  Google Scholar 

  • Béné C (2007) Diagnostic study of the Volta Basin fisheries: part 1 overview of the fisheries resources. WorldFish, Volta Basin Focal Project Report No 6. WorldFish Center Regional Offices for Africa and West Asia, Cairo Egypt, and CPWF, Colombo, Sri Lanka

  • Ben-Tuvia A (1960) The biology of the cichlid fishes of lake Tiberias and Huleh. Division of Fisheries, Sea Fisheries Research Station, State of Israel, Ministry of Agriculture

  • Berman T (1998) Lake Kinneret and its catchment: international pressures and environmental impacts. Water Policy 1:193–207

    Article  Google Scholar 

  • Berman T, Zohary T, Nishri A, Sukenik A (2014) General background. In: Zohary T, Sukenik A, Berman T, Nishri A (eds) Lake Kinneret. Springer, Dordrecht, pp 1–15

    Google Scholar 

  • Bijlsma R, Loeschcke V (2012) Genetic erosion impedes adaptive responses to stressful environments. Evol Appl 5:117–129

    Article  CAS  PubMed  Google Scholar 

  • Bouzat JL (2010) Conservation genetics of population bottlenecks: the role of chance, selection, and history. Conserv Genet 11:463–478

    Article  Google Scholar 

  • Chakrabarty P (2004) Cichlid biogeography: comment and review. Fish Fish 5:97–119

    Article  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Article  CAS  PubMed  Google Scholar 

  • Dudgeon D, Arthington AH, Gessner MO, Kawabata Z-I, Knowler DJ, Lévêque C, Naiman RJ, Prieur-Richard A-H, Soto D, Stiassny ML (2006) Freshwater biodiversity: importance, threats, status and conservation challenges. Biol Rev 81:163–182

    Article  PubMed  Google Scholar 

  • Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Frankham R, Briscoe DA, Ballou JD (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Frankham R, Bradshaw CJ, Brook BW (2014) Genetics in conservation management: revised recommendations for the 50/500 rules, Red List criteria and population viability analyses. Biol Conserv 170:56–63

    Article  Google Scholar 

  • Gophen M, Sonin O, Lev M, Snovsky G (2015) Regulated fishery is beneficial for the sustainability of fish population in Lake Kinneret (Israel). Open J Ecol 5:513

    Article  Google Scholar 

  • Goren M, Ortal R (1999) Biogeography, diversity and conservation of the inland water fish communities in Israel. Biol Conserv 89:1–9

    Article  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 Lond Ser B 270:2125–2132

    Article  Google Scholar 

  • Ivanova NV, Zemlak TS, Hanner RH, Hebert PD (2007) Universal primer cocktails for fish DNA barcoding. Mol Ecol Notes 7:544–548

    Article  CAS  Google Scholar 

  • Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laikre L (2010) Genetic diversity is overlooked in international conservation policy implementation. Conserv Genet 11:349–354

    Article  Google Scholar 

  • Lande R, Barrowclough GF (1987) Effective population size, genetic variation, and their use in population management. In: Soule ME (ed) Viable populations for conservation. Cambridge University press, New York, pp 87–124

    Chapter  Google Scholar 

  • Leberg PL (1990) Influence of genetic variability on population growth: implications for conservation. J Fish Biol 37:193–195

    Article  Google Scholar 

  • Lee B-Y, Lee W-J, Streelman JT, Carleton KL, Howe AE, Hulata G, Slettan A, Stern JE, Terai Y, Kocher TD (2005) A second-generation genetic linkage map of tilapia (Oreochromis spp.). Genetics 170:237–244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lemoalle J, de Condappa D (2010) Farming systems and food production in the Volta Basin. Water Int 35:655–680

    Article  Google Scholar 

  • Lévêque C, Oberdorff T, Paugy D, Stiassny MLJ, Tedesco PA (2008) Global diversity of fish (Pisces) in freshwater. Hydrobiologia 595:545–567

    Article  Google Scholar 

  • Lind CE, Brummett RE, Ponzoni RW (2012) Exploitation and conservation of fish genetic resources in Africa: issues and priorities for aquaculture development and research. Rev Aquac 4:125–141

    Article  Google Scholar 

  • Markel D, Shamir U, Green P (2014) Operational management of Lake Kinneret and its watershed. In: Zohary T, Sukenik A, Berman T, Nishri A (eds) Lake Kinneret. Springer, Dordrecht, pp 541–560

    Google Scholar 

  • Markert J, Champlin D, Gutjahr-Gobell R, Grear J, Kuhn A, McGreevy T, Roth A, Bagley M, Nacci D (2010) Population genetic diversity and fitness in multiple environments. BMC Evol Biol 10:205

    Article  PubMed  PubMed Central  Google Scholar 

  • Martínez G, Ehwen SM, Carrillo M, Zanuy S (1998) Protein salting-out method applied to genomic DNA isolation from fish whole blood. Biotechniques 24:238–239

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • O’Brien SJ (1994) A role for molecular genetics in biological conservation. Proc Natl Acad Sci USA 91:5748–5755

    Article  PubMed  PubMed Central  Google Scholar 

  • Ostrovsky I, Zohary T, Shapiro J, Snovsky G, Markel D (2014) Fisheries management. In: Zohary T, Sukenik A, Berman T, Nishri A (eds) Lake Kinneret. Springer, Dordrecht, pp 635–653

    Google Scholar 

  • Pinsky ML, Palumbi SR (2014) Meta-analysis reveals lower genetic diversity in overfished populations. Mol Ecol 23:29–39

    Article  PubMed  Google Scholar 

  • Pisanty S, Yami MB, Talpaz H (1987) Quasi-cyclic fluctuations in St. Peter’s fish stock in Lake Kinneret and their management implications. A—The cycles, and the effect of effort. Fish Fish Breed Isr 20:26–38

    Google Scholar 

  • Por FD (2012) The legacy of tethys: an aquatic biogeography of the levant. Springer, New York

    Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Purcell MK, Kornfield I, Fogarty M, Parker A (1996) Interdecadal heterogeneity in mitochondrial DNA of Atlantic haddock (Melanogrammus aeglefinus) from Georges Bank. Mol Mar Biol Biotechnol 5:185–192

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez F, Rexroad CE, Palti Y (2003) Characterization of twenty-four microsatellite markers for rainbow trout (Oncorhynchus mykiss). Mol Ecol Notes 3:619–622

    Article  CAS  Google Scholar 

  • Ryman N (1991) Conservation genetics considerations in fishery management. J Fish Biol 39:211–224

    Article  Google Scholar 

  • Ryman N, Laikre L (1991) Effects of supportive breeding on the genetically effective population size. Conserv Biol 5:325–329

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Serruya C (1978) Lake Kinneret. Springer, New York

    Book  Google Scholar 

  • Shaffer HB, Fisher RN, Davidson C (1998) The role of natural history collections in documenting species declines. Trends Ecol Evol 13:27–30

    Article  CAS  PubMed  Google Scholar 

  • Trewavas E (1983) Tilapiine fishes of the genera Sarotherodon, Oreochromis and Danakilia. British Museum (Natural History), London

    Book  Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Wandeler P, Hoeck PEA, Keller LF (2007) Back to the future: museum specimens in population genetics. Trends Ecol Evol 22:634–642

    Article  PubMed  Google Scholar 

  • Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN (2005) DNA barcoding Australia’s fish species. Philos Trans R Soc B 360:1847–1857

    Article  CAS  Google Scholar 

  • Werner NY, Mokady O (2004) Swimming out of Africa: mitochondrial DNA evidence for late Pliocene dispersal of a cichlid from Central Africa to the Levant. Biol J Linn Soc 82:103–109

    Article  Google Scholar 

  • Zohary T, Ostrovsky I (2011) Ecological impacts of excessive water level fluctuations in stratified freshwater lakes. Inland Waters 1:47–59

    Article  Google Scholar 

  • Zohary T, Gasith A, Markel D, Ostrovsky I (2008) The collapse of the Saint Peter’s fish fishery in Lake Kinneret. Fish Fish Breed Isr 39:1214–1224

    Google Scholar 

  • Zohary TSA, Berman T, Nishri A (2014) Lake Kinneret: ecology and management. Springer, New York

    Book  Google Scholar 

Download references

Acknowledgements

The authors wish to thank all who assisted in sampling of fish: Dr. Daniel Golani (The Hebrew University of Jerusalem), David Cummings (Kinneret Limnological Laboratory, IOLR), Dr. Noam Leader, Dr. Dana Milstein, Dr. Amit Dolev and Gizel Hazzan (Israel National Parks Authority), Menachem Lev (Kibbutz Ein Gev fishing vessel) and colleagues from the laboratory and the Animal Sciences Department. We further thank Prof. Moshe Gophen (Migal - Galilee Research Institute, Kiryat Shemona, Israel) for sharing old archived scales and Dr. Gila Kahila Bar-Gal and Lia Haddas (The Hebrew University of Jerusalem) for helping with DNA extraction from archived scales. We thank the reviewers and editor for their constructive comments. The study was funded by the Chief Scientist of the Israeli Ministry of Agriculture and Rural Development under Grant #186-0001-11 to LD and GH. LD is chair of the Vigevani Senior Lectureship in Animal Sciences.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lior David.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

Fish sampling was done under special permits 2012/38733 and 2014/40233 for sampling protected wildlife as reviewed and approved by the Israel Nature and National Parks Protection Authority.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Borovski, T., Tadmor-Levi, R., Shapiro, J. et al. Historical and recent reductions in genetic variation of the Sarotherodon galilaeus population in the Sea of Galilee. Conserv Genet 19, 1323–1333 (2018). https://doi.org/10.1007/s10592-018-1102-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-018-1102-7

Keywords

Navigation