Journal Home > Volume 9 , Issue 1
Background

Conservation of small and isolated populations can be challenging since they are prone to loss of genetic diversity due to random genetic drift and inbreeding. Therefore,information from the assessment of genetic diversity and structure are needed for conservation programs to determine the appropriate management strategy for the populations. We investigated the levels of genetic variability in a resident Greylag Goose (Anser anser) population,the southernmost breeding population of the species in Europe and the sole viable population of any goose species in Greece.

Methods

A fragment of mtDNA Control Region and a panel of 11 microsatellite markers were used to search for any signs of genetic impoverishment and population substructure and to reveal the underlying processes through the identification of possible past demographic events.

Results

The population was found to be monomorphic in the amplified fragment of the mitochondrial Control Region,with all individuals sharing a single private haplotype. Analyses showed a lack of any population substructure indicating a panmictic population. Although the population seems to have experienced a strong and recent genetic bottleneck and exhibits a small effective population size,we did not find evidence of either extremely low levels of genetic diversity or inbreeding depression.

Conclusions

The recent demographic decline we detected and the combined influence of residency and anthropogenic factors have probably shaped the current genetic status. Our study population does not need emergency conservation actions but should be regarded as a discrete management unit. Future management strategies should focus on population and genetic monitoring and preventing further abundance declines that would increase the risk of genetic impoverishment.


menu
Abstract
Full text
Outline
About this article

Conservation genetics of a resident population of Greylag Goose (Anser anser) at the southernmost limit of the species' distribution in Europe

Show Author's information Anastasios Bounas1Giorgos Catsadorakis2Annita Logotheti2Berend Voslamber3Antonios Magoulas4Dimitris Tsaparis4 ( )
Molecular Ecology and Conservation Genetics Lab, Department of Biological Applications and Technology, University of Ioannina, 45110 Ioannina, Greece
Society for the Protection of Prespa, Lemos Prespa, 53077 Agios Germanos, Greece
Sovon Dutch Centre for Field Ornithology, Toernooiveld 1, 6525 ED Nijmegen, The Netherlands
Institute of Marine Biology, Biotechnology and Aquaculture (IMBBC), Hellenic Centre for Marine Research (HCMR), 71500 Heraklion, Greece

Abstract

Background

Conservation of small and isolated populations can be challenging since they are prone to loss of genetic diversity due to random genetic drift and inbreeding. Therefore,information from the assessment of genetic diversity and structure are needed for conservation programs to determine the appropriate management strategy for the populations. We investigated the levels of genetic variability in a resident Greylag Goose (Anser anser) population,the southernmost breeding population of the species in Europe and the sole viable population of any goose species in Greece.

Methods

A fragment of mtDNA Control Region and a panel of 11 microsatellite markers were used to search for any signs of genetic impoverishment and population substructure and to reveal the underlying processes through the identification of possible past demographic events.

Results

The population was found to be monomorphic in the amplified fragment of the mitochondrial Control Region,with all individuals sharing a single private haplotype. Analyses showed a lack of any population substructure indicating a panmictic population. Although the population seems to have experienced a strong and recent genetic bottleneck and exhibits a small effective population size,we did not find evidence of either extremely low levels of genetic diversity or inbreeding depression.

Conclusions

The recent demographic decline we detected and the combined influence of residency and anthropogenic factors have probably shaped the current genetic status. Our study population does not need emergency conservation actions but should be regarded as a discrete management unit. Future management strategies should focus on population and genetic monitoring and preventing further abundance declines that would increase the risk of genetic impoverishment.

Keywords: Isolation, Conservation, mtDNA, Genetic variability, Inbreeding, Management units, Microsatellites, Nonmigratory population

References(68)

Allendorf FW, Luikart G. Conservation and the genetics of populations. New York: Wiley; 2009.

Amos W, Balmford A. When does conservation genetics matter? Heredity. 2001;87:257-65.

Baker RR. The evolutionary ecology of animal migration. New York: Holmes & Meier Publishers; 1978.
Belkhir K. GENETIX, logiciel sous WindowsTM pour la génétique des populations. 1999. http://www.univmontp2fr/~genetix. Accessed 24 Mar 2018.
BirdLife International. Birds in Europe: population estimates, trends and conservation status. Cambridge: BirdLife Conservation Series; 2004.

Catsadorakis G. The importance of Prespa National Park for breeding and wintering birds. Hydrobiologia. 1997;351:157-74.

Catsadorakis G, Voslamber B, Logotheti A. First Greylag Geese Anser anser rubrirostris ringed in Greece. Goose Bull. 2012;15:28-31.

Chapman J, Nakagawa S, Coltman D, Slate J, Sheldon B. A quantitative review of heterozygosity-fitness correlations in animal populations. Mol Ecol. 2009;18:2746-65.

Coltman D, Pilkington J, Smith J, Pemberton J. Parasite mediated selection against inbred Soay sheep in a free-living island population. Evolution. 1999;53:1259-67.PubMed

Cornuet JM, Luikart G. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics. 1996;144:2001-14.

Cristescu R, Sherwin WB, Handasyde K, Cahill V, Cooper DW. Detecting bottlenecks using BOTTLENECK 1.2. 02 in wild populations: the importance of the microsatellite structure. Conserv Genet. 2010;11:1043-9.

Crnokrak P, Roff DA. Inbreeding depression in the wild. Heredity. 1999;83:260-70.

David P, Pujol B, Viard F, Castella V, Goudet J. Reliable selfing rate estimates from imperfect population genetic data. Mol Ecol. 2007;16:2474-87.

Di Rienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Freimer NB. Mutational processes of simple sequence repeat loci in human populations. Proc Natl Acad Sci USA. 1994;91:3166-70.

Do C, Waples RS, Peel D, Macbeth G, Tillett BJ, Ovenden JR. NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Res. 2014;14:209-14.

Excoffier L, Lischer HE. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res. 2010;10:564-7.

Falush D, Stephens M, Pritchard JK. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics. 2003;164:1567-87.

Forstmeier W, Schielzeth H, Mueller JC, Ellegren H, Kempenaers B. Heterozygosity-fitness correlations in zebra finches: microsatellite markers can be better than their reputation. Mol Ecol. 2012;21:3237-49.

Fox AD, Ebbinge BS, Mitchell C, Heinicke T, Aarvak T, Colhoun K, Clausen P, Dereliev S, Faragó S, Koffijberg K. Current estimates of goose population sizes in western Europe, a gap analysis and assessment of trends. Ornis Svec. 2010;20:115-27.

Frankham R. Effective population size/adult population size ratios in wildlife: a review. Genet Res. 1995;66:95-107.

Frankham R, Briscoe DA, Ballou JD. Introduction to conservation genetics. Cambridge: Cambridge University Press; 2002.

Freeland JR. Molecular ecology. New York: Wiley; 2005.

Freeman S, Jackson WM. Univariate metrics are not adequate to measure avian body size. Auk. 1990;107:69-74.

Friesen V, Burg T, McCoy K. Mechanisms of population differentiation in seabirds. Mol Ecol. 2007;16:1765-85.

Garza JC, Williamson EG. Detection of reduction in population size using data from microsatellite loci. Mol Ecol. 2001;10:305-18.

Gosler A. Pattern and process in the bill morphology of the Great Tit Parus major. Ibis. 1987;129:451-76.

Goudet J. FSTAT, a program to estimate and test gene diversities and fixation indices version 2.9.3.2. 2002. http://www.2.unil.ch/popgen/softwares/fstat.htm. Accessed 20 Aug 2012.

Grueber CE, Wallis GP, Jamieson IG. Heterozygosity-fitness correlations and their relevance to studies on inbreeding depression in threatened species. Mol Ecol. 2008;17:3978-84.

Harrison XA, Bearhop S, Inger R, Colhoun K, Gudmundsson GA, Hodgson D, McElwaine G, Tregenza T. Heterozygosity-fitness correlations in a migratory bird: an analysis of inbreeding and single-locus effects. Mol Ecol. 2011;20:4786-95.

Hedrick PW, Kalinowski ST. Inbreeding depression in conservation biology. Annu Rev Ecol Evol Syst. 2000;31:139-62.

Heikkinen M, Ruokonen M, Alexander M, Aspi J, Pyhäjärvi T, Searle J. Relationship between wild greylag and European domestic geese based on mitochondrial DNA. Anim Genet. 2015;46:485-97.

Hewitt GM. Post-glacial re-colonization of European biota. Biol J Linn Soc. 1999;68:87-112.

Hill WG. Estimation of effective population size from data on linkage disequilibrium. Genet Res. 1981;38:209-16.

Höglund J, Piertney SB, Alatalo RV, Lindell J, Lundberg A, Rintamäki PT. Inbreeding depression and male fitness in black grouse. Proc R Soc B. 2002;269:711-5.

Horvath MB, Martinez-Cruz B, Negro JJ, Kalmar L, Godoy JA. An overlooked DNA source for non-invasive genetic analysis in birds. J Avian Biol. 2005;36:84-8.

Jonker R, Kraus RH, Zhang Q, Hooft P, Larsson K, Jeugd H, Kurvers R, Wieren S, Loonen M, Crooijmans R. Genetic consequences of breaking migratory traditions in barnacle geese Branta leucopsis. Mol Ecol. 2013;22:5835-47.

Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016;33:1870-4.

Lagnel J. ParaStructure. 2015. https://github.com/jacqueslagnel/parastructure. Accessed 22 Mar 2018.

Leblois R, Pudlo P, Néron J, Bertaux F, Reddy Beeravolu C, Vitalis R, Rousset F. Maximum-likelihood inference of population size contractions from microsatellite data. Mol Biol Evol. 2014;31:2805-23.

Møller AP, Fiedler W, Berthold P. Effects of climate change on birds. Oxford: Oxford University Press; 2010.

Moritz C. Defining 'evolutionarily significant units' for conservation. Trends Ecol Evol. 1994;9:373-5.

Navidi W, Arnheim N, Waterman M. A multiple-tubes approach for accurate genotyping of very small DNA samples by using PCR: statistical considerations. Am J Hum Genet. 1992;50:347.

Nei M, Tajima F. Genetic drift and estimation of effective population size. Genetics. 1981;98:625-40.

Newton I. The migration ecology of birds. London: Academic Press; 2010.

Palacín C, Alonso JC, Martín CA, Alonso JA. Changes in bird-migration patterns associated with human-induced mortality. Conserv Biol. 2017;31:106-15.

Palsbøll PJ, Berube M, Allendorf FW. Identification of management units using population genetic data. Trends Ecol Evol. 2007;22:11-6.

Peakall R, Smouse PE. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics. 2012;28:2537-9.

Pearce JM, Talbot SL, Pierson BJ, Petersen MR, Scribner KT, Dickson DL, Mosbech A. Lack of spatial genetic structure among nesting and wintering King Eiders. Condor. 2004;106:229-40.

Pellegrino I, Cucco M, Follestad A, Boos M. Lack of genetic structure in greylag goose (Anser anser) populations along the European Atlantic flyway. PeerJ. 2015;3:e1161.

Piry S, Luikart G, Cornuet J-M. Computer note. BOTTLENECK: a computer program for detecting recent reductions in the effective size using allele frequency data. J Hered. 1999;90:502-3.

Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155:945-59.

R Core Team. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2017.
Rohwer FC, Anderson MG. Female-biased philopatry, monogamy, and the timing of pair formation in migratory waterfowl. In: Johnston E, Richard F, editors. Current ornithology. Boston: Springer; 1988. p. 187-221.https://doi.org/10.1007/978-1-4615-6787-5_4
DOI

Ruokonen M, Kvist L, Lumme J. Close relatedness between mitochondrial DNA from seven Anser goose species. J Evol Biol. 2000;13:532-40.

Scott DA, Rose PM. Atlas of Anatidae populations in Africa and western Eurasia. Ede: Wetlands International; 1996.

Slate J, David P, Dodds K, Veenvliet B, Glass B, Broad T, McEwan J. Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data. Heredity. 2004;93:255-65.

Stoffel MA, Esser M, Kardos M, Humble E, Nichols H, David P, Hoffman JI. InbreedR: an R package for the analysis of inbreeding based on genetic markers. Methods Ecol Evol. 2016;7:1331-9.

Svensson L. Identification guide to European passerines. Thetford: British Trust for Ornithology; 1992.

Szulkin M, Bierne N, David P. Heterozygosity-fitness correlations: a time for reappraisal. Evolution. 2010;64:1202-17.PubMed

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;22:4673-80.

Toonen RJ, Hughes S. Increased throughput for fragment analysis on an ABI Prism® 377 automated sequencer using a membrane comb and STRand software. Biotechniques. 2001;31:1320-5.PubMed

Valière N. GIMLET: a computer program for analysing genetic individual identification data. Mol Ecol Notes. 2002;2:377-9.

van der Jeugd HP, van der Veen IT, Larsson K. Kin clustering in barnacle geese: familiarity or phenotype matching? Behav Ecol. 2002;13:786-90.

Van Oosterhout C, Hutchinson WF, Wills DP, Shipley P. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes. 2004;4:535-8.

Waples RS. A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci. Conserv Genet. 2006;7:167.

Weiß BM, Poggemann K, Olek K, Foerster K, Hirschenhauser K. Isolation and characterization of microsatellite marker loci in the greylag goose (Anser anser). Mol Ecol Res. 2008;8:1411-3.

Wickham H, Chang W. Ggplot2: an implementation of the grammar of graphics. 2015. http://CRAN.R-project.org/package=ggplot2. Accessed 30 Mar 2018.

Willoughby JR, Sundaram M, Wijayawardena BK, Lamb MC, Kimble SJ, Ji Y, Fernandez NB, Antonides JD, Marra NJ, Dewoody JA. Biome and migratory behaviour significantly influence vertebrate genetic diversity. Biol J Linn Soc. 2017;121:446-57.

Publication history
Copyright
Acknowledgements
Rights and permissions

Publication history

Received: 03 May 2018
Accepted: 13 December 2018
Published: 21 December 2018
Issue date: January 2018

Copyright

© The Author(s) 2018.

Acknowledgements

Acknowledgements

We are especially indebted to Gerard Müskens (Wageningen Environmental Research) who was in charge of the catching efforts and took the samples. Special thanks need to go to the enthusiastic volunteers and friends, Jan Vegelin, Loes van den Bremer, and the late Hennie van den Brink who helped in the catching. The staff of the SPP Olga Alexandrou, Irene Koutseri, Myrsini Malakou, Haris Nikolaou, Lazaros Nikolaou also helped during the catching efforts. The support of the Management Body of the Prespa National Park and the help of local inhabitants are also acknowledged.

Rights and permissions

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Return