Abstract
The distribution of many species is fragmented due to human activities and isolated populations are often affected by genetic changes. Small populations are endangered by inbreeding depression, often leading to a low mean fitness of small populations and to an increased extinction risk. Using museum samples of protected Microtus oeconomus mehelyi from the years 1950, 1964 and 2000, we studied the population which inhabits the Kis Balaton area that has considerably changed by human activity in the last centuries. The detected effective population size, differences in allele frequencies, associations between alleles and a high genetic differentiation may be explained by 50 years of random genetic drift in this population in the significantly altered Kis Balaton area. We have detected a genetic difference between Kis Balaton populations and published populations from Hungary, Austria and Slovakia. Using linkage disequilibrium and temporal approaches, the estimates of the effective population size are below 100/1000, thresholds to limit inbreeding depression and to retain evolutionary potential. Taking the fragmented occurrence of Microtus oeconomus mehelyi in central Europe into account, it is possible that also other populations may also undergo the same processes after significant isolation.
Similar content being viewed by others
Availability of data and materials
Microtus oeconomus genotypes are available on Mendeley Data, V1, https://doi.org/10.17632/yx2zmhmxkc.1, Microtus oeconomus samples are in the Hungarian Natural History Museum.
Code availability
Not applicable.
References
Allendorf FW (1986) Genetic drift and the loss of alleles versus heterozygosity. Zoo Biol 5(2):181–190. https://doi.org/10.1002/zoo.1430050212
Allendorf FW, Luikart G (2009) Conservation and the genetics of populations. Wiley, Malden
Ambros M (2010) Country assessment on the example of the presence of the Pannonian Root Vole (Microtus oeconomus méhelyi). Ústav krajinnej ekológie SAV, Nitra
Bonferroni CE (1936) Teoria statistica delle classi e calcolo delle probabilità. Pubblicazioni Del R Istituto Superiore Di Scienze Economiche e Commerciali Di Firenze 8:3–62
Borbás V (1900) A Balaton tavának és partmellékének növényföldrajza és edényes növényzete. (Phyto-geography and the vascular plants of Lake Balaton and its littoral zone). A Balaton Tudományos Tanulmányozásának Eredményei 2(2):432
Brunhoff C, Galbreath KE, Fedorov VB, Cook JA, Jaarola M (2003) Holarctic phylogeography of the root vole (Microtus oeconomus): implications for late quaternary biogeography of high latitudes. Mol Ecol 12(4):957–968. https://doi.org/10.1046/j.1365-294X.2003.01796.x
Caballero A (1994) Developments in the prediction of effective population size. Heredity 73(6):657–679
Charlesworth B (2009) Effective population size and patterns of molecular evolution and variation. Nat Rev Gen 10(3):195–205
Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144(4):2001–2014
Crow JF, Denniston C (1988) Inbreeding and variance effective population numbers. Evolution 42(3):482–495
Dąbrowski MJ, Pilot M, Kruczyk M, Żmihorski M, Umer HM, Gliwicz J (2014) Reliability assessment of null allele detection: inconsistencies between and within different methods. Mol Ecol Resour 14(2):361–373. https://doi.org/10.1111/1755-0998.12177
Di Rienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Freimer NB (1994) Mutational processes of simple sequence repeat loci in human populations. Prof Natl Acad Sci USA 91:3166–3170. https://doi.org/10.1073/pnas.91.8.3166
Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR (2014) NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14(1):209–214. https://doi.org/10.1111/1755-0998.12157
Dömötörfy Z, Reeder D, Pomogyi P (2003) Changes in the macro-vegetation of the Kis-Balaton Wetlands over the last two centuries: a GIS perspective. Hydrobiologia 506(1):671–679
England PR, Cornuet JM, Berthier P, Tallmon DA, Luikart G (2006) Estimating effective population size from linkage disequilibrium: severe bias in small samples. Conserv Genet 7(2):303. https://doi.org/10.1371/journal.pone.0069078
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14(8):2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Fløjgaard C, Normand S, Skov F, Svenning JC (2009) Ice age distributions of European small mammals: insights from species distribution modelling. J Biogeogr 36(6):1152–1163. https://doi.org/10.1111/j.1365-2699.2009.02089.x
Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10(6):1500–1508. https://doi.org/10.1046/j.1523-1739.1996.10061500.x
Frankham R (2005) Genetics and extinction. Biol Conserv 126(2):131–140. https://doi.org/10.1016/j.biocon.2005.05.002
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. https://doi.org/10.1016/j.biocon.2013.12.036
Franklin IR (1980) Evolutionary change in small populations. Conserv Biol Evolut Ecol Perspect 395
Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86(6):485–486
Gubányi A, Dudich A, Stollmann A, Ambros M (2009) Distribution and conservation management of the root vole (Microtus oeconomus) populations along the Danube in Central Europe (Rodentia: Arvicolinae). Lynx 40:29–42
Hare MP, Nunney L, Schwartz MK, Ruzzante DE, Burford M, Waples RS, Ruegg K, Palstra F (2011) Understanding and estimating effective population size for practical application in marine species management. Conserv Biol 25(3):438–449
Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59(8):1633–1638. https://doi.org/10.1111/j.0014-3820.2005.tb01814.x
Hill WG (1981) Estimation of effective population size from data on linkage disequilibrium. Gen Res 38(3):209–216. https://doi.org/10.1017/S0016672300020553
Horváth GF, Herczeg R (2013) Site occupancy response to natural and anthropogenic disturbances of root vole: conservation problem of a vulnerable relict subspecies. J Nat Conserv 21(5):350–358. https://doi.org/10.1016/j.jnc.2013.03.004
Jorde PE, Ryman N (1996) Demographic genetics of brown trout (Salmo trutta) and estimation of effective population size from temporal change of allele frequencies. Genetics 143(3):1369–1381
Jorde PE, Ryman N (2007) Unbiased estimator for genetic drift and effective population size. Genetics 177(2):927–935. https://doi.org/10.1534/genetics.107.075481
Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17(18):4015–4026. https://doi.org/10.1111/j.1365-294X.2008.03887.x
Jost L, Archer F, Flanagan S, Gaggiotti O, Hoban S, Latch E (2018) Differentiation measures for conservation genetics. Evol Appl 11(7):1139–1148
Kalinowski ST, Taper ML (2006) Maximum likelihood estimation of the frequency of null alleles at microsatellite loci. Conserv Genet 7(6):991–995. https://doi.org/10.1007/s10592-006-9134-9
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(5):1179–1191. https://doi.org/10.1111/1755-0998.12387
Lonsinger RC, Adams JR, Waits LP (2018) Evaluating effective population size and genetic diversity of a declining kit fox population using contemporary and historical specimens. Ecol Evol 8(23):12011–12021. https://doi.org/10.1002/ece3.4660
Luikart G, Sherwin WB, Steele BM, Allendorf FW (1998) Usefulness of molecular markers for detecting population bottlenecks via monitoring genetic change. Mol Ecol 7(8):963–974. https://doi.org/10.1046/j.1365-294x.1998.00414.x
Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220
Mueller AK, Chakarov N, Krüger O, Hoffman JI (2016) Long-term effective population size dynamics of an intensively monitored vertebrate population. Heredity 117(4):290–299. https://doi.org/10.1038/hdy.2016.67
Navidi W, Arnheim N, Waterman MS (1992) A multiple-tubes approach for accurate genotyping of very small DNA samples by using PCR: statistical considerations. Am J Hum Genet 50(2):347. https://doi.org/10.1016/j.tree.2007.08.017
Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci 70(12):3321–3323
Nei M, Tajima F (1981) Genetic drift and estimation of effective population size. Genetics 98(3):625–640
Newman D, Pilson D (1997) Increased probability of extinction due to decreased genetic effective population size: experimental populations of Clarkia pulchella. Evolution 51(2):354–362. https://doi.org/10.1111/j.1558-5646.1997.tb02422.x
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 population persistence? Mol Ecol 17:3428–3447. https://doi.org/10.1111/j.1365-294X.2008.03842.x
Peakall ROD, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6(1):288–295. https://doi.org/10.1111/j.1471-8286.2005.01155.x
Pollak E (1983) A new method for estimating the effective population size from allele frequency changes. Genetics 104(3):531–548
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959
Qanbari S (2020) On the extent of linkage disequilibrium in the genome of farm animals. Front Genet 10:1304. https://doi.org/10.3389/fgene.2019.01304
Rousset F (2008) Genepop´007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Resour 8:103–106. https://doi.org/10.1111/j.1471-8286.2007.01931.x
Sládkovičová VH, Dąbrowski MJ, Žiak D, Miklós P, Gubányi A, La Haye MJ, Bekker D, Thissen J, Herzig-Straschil B, Kocian L, Gliwicz J (2018) Genetic variability of the cold-tolerant Microtus oeconomus subspecies left behind retreating glaciers. Mamm Biol 88(1):85–93. https://doi.org/10.1016/j.mambio.2017.11.0071
Sládkovičová VH, Žiak D, Miklós P, Kameniar O, Kocian Ľ (2019) Age determination and individual growth rate of Microtus oeconomus mehelyi based on live-trapping. Biologia 74(5):487–492. https://doi.org/10.2478/s11756-018-00188-6
Summers K, Amos W (1997) Behavioral, ecological, and molecular genetic analyses of reproductive strategies in the Amazonian dart-poison frog, Dendrobates ventrimaculatus. Behav Ecol 8(3):260–267. https://doi.org/10.1093/beheco/8.3.260
Sved JA (1971) Linkage disequilibrium and homozygosity of chromosome segments in finite populations. Theor Popul Biol 2(2):125–141. https://doi.org/10.1016/0040-5809(71)90011-6
Taberlet P, Griffin S, Goossens B, Questiau S, Manceau V, Escaravage N, Waits LP, Bouvet J (1996) Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Res 24(16):3189–3194. https://doi.org/10.1093/nar/24.16.3189
Takezaki N, Nei M, Tamura K (2014) POPTREEW: web version of POPTREE for constructing population trees from allele frequency data and computing some other quantities. Mol Biol Evol 31(6):1622–1624. https://doi.org/10.1093/molbev/msu093
Tátrai I, Mátyás K, Korponai J, Paulovits G, Pomogyi P (2000) The role of the Kis-Balaton Water Protection System in the control of water quality of Lake Balaton. Ecol Eng 16(1):73–78. https://doi.org/10.1016/S0925-8574(00)00091-4
Thissen JB, Bekker DL, Spreitzer K, Herzig-Straschil B (2015) The distribution of the Pannonic root vole (Microtus oeconomus mehelyi Ehik, 1928) in Austria. Lutra 58(1):3–22
Valiére N (2002) Gimlet: a computer program for analysing genetic individual identification data. Mol Ecol Notes 2:377–379
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
Waits LP, Luikart G, Taberlet P (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10(1):249–256. https://doi.org/10.1046/j.1365-294X.2001.01185.x
Wandeler P, Hoeck PE, Keller LF (2007) Back to the future: museum specimens in population genetics. Trends in Ecol Evol 22(12):634–642
Waples RS (1989) A generalized approach for estimating effective population size from temporal changes in allele frequency. Genetics 121(2):379–391
Waples RS (2005) Genetic estimates of contemporary effective population size: to what time periods do the estimates apply? Mol Ecol 14(11):3335–3352. https://doi.org/10.1111/j.1365-294X.2005.02673.x
Waples RS (2006) A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci. Conserv Genet 7(2):167. https://doi.org/10.1007/s10592-005-9100-y
Waples RS, Anderson EC (2017) Purging putative siblings from population genetic data sets: a cautionary view. Mol Ecol 26(5):1211–1224. https://doi.org/10.1111/mec.14022
Waples RS, Do CHI (2008) LDNe: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Resour 8:753–756. https://doi.org/10.1111/j.1755-0998.2007.02061.x
Waples RS, Do CHI (2010) Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evol Appl 3(3):244–262. https://doi.org/10.1111/j.1752-4571.2009.00104.x
Waples RS, England PR (2011) Estimating contemporary effective population size on the basis of linkage disequilibrium in the face of migration. Genetics 189(2):633–644. https://doi.org/10.1534/genetics.111.132233
Waples RS, Yokota M (2007) Temporal estimates of effective population size in species with overlapping generations. Genetics 175(1):219–233. https://doi.org/10.1534/genetics.106.065300
Wright S (1931) Evolution in Mendelian populations. Genetics 16(2):97
Wright S (1968) The theory of gene frequencies. University of Chicago Press, Chicago
Wright S (1978) Evolution and the genetics of populations: a treatise in four volumes: Vol. 4: variability within and among natural populations. University of Chicago Press, Chicago
Zlinszky A, Mücke W, Lehner H, Briese C, Pfeifer N (2012) Categorizing wetland vegetation by airborne laser scanning on Lake Balaton and Kis-Balaton, Hungary. Remote Sens 4(6):1617–1650. https://doi.org/10.3390/rs4061617
Acknowledgements
We thank Virág Krízsik, Mária Tuschek, Tamás Görföl and Dick Bekker. The research was supported by the Synthesys project HU-TAF-5271 http://www.synthesys.info/ which is financed by European Community Research Infrastructure Action under the FP7 “Capacities” Program Part of the calculations were performed in the Computing Centre of the Slovak Academy of Sciences using the supercomputing infrastructure acquired in project ITMS 26230120002 and 26210120002 (Slovak infrastructure for high-performance computing) supported by the Research & Development Operational Programme funded by the ERDF.
Funding
The Synthesys project HU-TAF-5271.
Author information
Authors and Affiliations
Contributions
VS—designed and performed research, analyzed data, wrote the paper. DŽ—collected samples. PM—collected samples. AG—collected samples. GH—collected samples.
Corresponding author
Ethics declarations
Conflict of interest
Not applicable.
Ethics approval
Not applicable.
Consent to participate
All authors approved the manuscript and its submission.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Handling editor: Allan McDevitt.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Sládkovičová, V., Žiak, D., Miklós, P. et al. The history of genetic diversity and effective population size of an isolated Microtus oeconomus population on Kis Balaton. Mamm Biol 102, 87–98 (2022). https://doi.org/10.1007/s42991-021-00199-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42991-021-00199-y