Conservation genetics of regionally extinct peregrine falcons (Falco peregrinus) and unassisted recovery without genetic bottleneck in southern England

Journal article


Weaving, A., Jackson, H. A, Nicholls, M. K., Franklin, J. and Vega, R. 2020. Conservation genetics of regionally extinct peregrine falcons (Falco peregrinus) and unassisted recovery without genetic bottleneck in southern England. Conservation Genetics. https://doi.org/10.1007/s10592-020-01324-z
AuthorsWeaving, A., Jackson, H. A, Nicholls, M. K., Franklin, J. and Vega, R.
Abstract

The peregrine falcon (Falco peregrinus) has been affected by persecution, pollution, trade, and habitat degradation, but it is considered a flagship conservation success story because of successful reintroductions and population recoveries across broad ranges. However, in the UK there were never formal reintroduction programmes for peregrine falcons, and it appears that UK populations – and specifically the Sussex peregrines of the English south coast – recently recovered from a population crash unassisted. To study this, we obtained samples from contemporary populations in southern England, Ireland, continental Europe, domestic-bred peregrine falcons, and from England pre-population crash. Using microsatellite and mtDNA control region data, the genetic diversity and structure, signatures of genetic bottlenecks, and potential origin of the Sussex peregrines was investigated. We found low levels of genetic diversity across all peregrine falcon groups, low but significant genetic differentiation, and a few private alleles, indicating some level of genetic structure among European peregrines. Although we could not pinpoint the origin of the Sussex peregrines, the data suggests that it is not likely to have originated from escaped domestic birds or from adjacent European populations. The results obtained here parallel other studies on peregrines elsewhere showing low genetic diversity but genetic structure. We conclude that not enough time elapsed for genetic erosion to occur due to the population bottleneck, and that at least for the Sussex peregrines there is no need for genetic conservation by wild-take and subsequent captive breeding programmes as long as current protection measures remain in place.

KeywordsConservation; Genetic diversity; Microsatellites; mtDNA control region; Organochlorine pesticides; Raptors; Birds; Ornithology
Year2020
JournalConservation Genetics
PublisherSpringer
ISSN1566-0621
1572-9737
Digital Object Identifier (DOI)https://doi.org/10.1007/s10592-020-01324-z
Official URLhttps://doi.org/10.1007/s10592-020-01324-z
Related URLhttps://europepmc.org/article/ppr/ppr148755
Publication dates
Online13 Jan 2021
Publication process dates
Deposited10 Dec 2020
Accepted07 Dec 2020
Accepted author manuscript
File Access Level
Open
Output statusPublished
References

Amos W, Harwood J (1998) Factors affecting levels of genetic diversity in natural populations. Phil Trans R Soc Lond B 353:177–186. https://doi.org/10.1098/rstb.1998.0200
Banks AN, Crick HQP, Coombes R, et al (2010) The breeding status of Peregrine Falcons Falco peregrinus in the UK and Isle of Man in 2002. Bird Study 57:421–436. https://doi.org/10.1080/00063657.2010.511148
BirdLife International (2019) Falco peregrinus (amended version of 2016 assessment). The IUCN Red List of Threatened Species 2019: e.T45354964A155500538 https://dx.doi.org/10.2305/IUCN.UK.2016-3.RLTS.T45354964A155500538.e... Downloaded on 29 October 2020
Brook BW, Tonkyn DW, O’Grady JJ, Frankham R (2002) Contribution of inbreeding to extinction risk in threatened species. Conserv Ecol 6:16. https://doi.org/10.5751/es-00387-060116
Brown JW, Van Coeverden De Groot PJ, Birt TP, et al (2007) Appraisal of the consequences of the DDT-induced bottleneck on the level and geographic distribution of neutral genetic variation in Canadian peregrine falcons, Falco peregrinus. Mol Ecol 16:327–343. https://doi.org/10.1111/j.1365-294X.2007.03151.x
Cade TJ, Enderson JH, Thelander CG, White CM (eds) (1988) Peregrine falcon populations: their management and recovery. Peregrine Fund, Idaho
Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014
Crick HQP, Ratcliffe DA (1995) The Peregrine Falco peregrinus breeding population of the United Kingdom in 1991. Bird Study 42:1–19. https://doi.org/10.1080/00063659509477143
Di Rienzo A, Peterson AC, Garza JC et al (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci USA 91:3166–3170 https://doi.org/10.1073/pnas.91.8.3166
Do C, Waples RS, Peel D, et al (2014) NeEstimator v2: Re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14:209–214. https://doi.org/10.1111/1755-0998.12157
Eaton M, Aebischer N, Brown A, et al (2015) Birds of Conservation Concern 4: The population status of birds in the UK, Channel Islands and Isle of Man. British Birds 108:708-746
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. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Everitt PJ, Franklin J (2009) First UK record of a wild free-living Peregrine Falcon female breeding and producing young with a hybrid male falcon of domestic origin. In: Sielicki J, Mizera T (ed) Peregrine Falcon populations – status and perspectives in the 21st century, European Peregrine Falcon Working Group, Society for the Protection of Wild Animals "Falcon". Turul/Poznań University of Life Sciences Press, Warsaw-Poznań, pp 585–592
Excoffier L, Lischer HEL (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. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics 164:1567–1587
Fleming LV, Douse AF, Williams NP (2011) Captive breeding of peregrine and other falcons in Great Britain and implications for conservation of wild populations. Endanger Species Res 14:243–257. https://doi.org/10.3354/esr00352
Frankham R (2015) Genetic rescue of small inbred populations: meta-analysis reveals large and consistent benefits of gene flow. Mol Ecol 24:2610–2618. https://doi.org/10.1111/mec.13139
Franklin J, Everitt PJ (2009) Population trends of peregrine falcons on the Sussex coast of the United Kingdom, 1904-2006. In: Sielicki J, Mizera T (ed) Peregrine Falcon populations – status and perspectives in the 21st century, European Peregrine Falcon Working Group, Society for the Protection of Wild Animals "Falcon". Turul/Poznań University of Life Sciences Press, Warsaw-Poznań, pp 87–98
Franklin J, Nicholls MK (2018) Notes on the present-day population of Sussex Peregrines. The Oologist 2:122–127
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925
Hailer F, Helander B, Folkestad AO, et al (2006) Bottlenecked but long-lived: High genetic diversity retained in white-tailed eagles upon recovery from population decline. Biol Lett 2:316–319. https://doi.org/10.1098/rsbl.2006.0453
Hall TA (1999) BIOEDIT: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/ NT. Nucleic Acids Symp Ser 41:95–98
Hoffman JI, Amos W (2005) Microsatellite genotyping errors: Detection approaches, common sources and consequences for paternal exclusion. Mol Ecol 14:599–612. https://doi.org/10.1111/j.1365-294X.2004.02419.x
Holroyd GL, Banasch U (1990) The reintroduction of the peregrine falcon Falco peregrinus anatum into southern Canada. Can Field Nat 104:203–208
Horne G, Fielding AH (2002) Recovery of the Peregrine Falcon Falco peregrinus in Cumbria, UK, 1966–99. Bird Study 49:229–236. https://doi.org/10.1080/00063650209461270
Humphreys L, Wernham C, Crick HQ (2007) Raptor species conservation frameworks: The peregrine conservation framework project progress report-Phase I. British Trust for Ornithology, Scotland
Jacobsen F, Nesje M, Bachmann L, Lifjeld JT (2008) Significant genetic admixture after reintroduction of peregrine falcon (Falco peregrinus) in Southern Scandinavia. Conserv Genet 9:581–591. https://doi.org/10.1007/s10592-007-9373-4
Janes JK, Miller JM, Dupuis JR, et al (2017) The K = 2 conundrum. Mol Ecol 26:3594–3602. https://doi.org/10.1111/mec.14187
Johnson JA, Talbot SL, Sage GK, et al (2010) The use of genetics for the management of a recovering population: Temporal assessment of migratory peregrine falcons in North America. PLoS One 5:e14042. https://doi.org/10.1371/journal.pone.0014042
Kopelman NM, Mayzel J, Jakobsson M, et al (2015) CLUMPAK: A program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191. https://doi.org/10.1111/1755-0998.12387
Kozakiewicz CP, Carver S, Austin JJ, et al (2017) Intrinsic factors drive spatial genetic variation in a highly vagile species, the wedge-tailed eagle Aquila audax, in Tasmania. J Avian Biol 48:1025–1034. https://doi.org/10.1111/jav.01326
Li YL, Liu JX (2018) STRUCTURESELECTOR: A web-based software to select and visualize the optimal number of clusters using multiple methods. Mol Ecol Resour 18:176–177. https://doi.org/10.1111/1755-0998.12719
Librado P, Rozas J (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. https://doi.org/10.1093/bioinformatics/btp187
Madden B, Hunt J, Norriss D (2009) The 2002 survey of the peregrine Falco peregrinus breeding population in the Republic of Ireland. Irish Birds 8:543–548
Maruyama T, Fuerst PA (1984) Population bottlenecks and nonequilibrium models in population genetics. I. Allele numbers when populations evolve from zero variability. Genetics 108:745–763
Maruyama T, Fuerst PA (1985) Population bottlenecks and nonequilibrium models in population genetics. II. Number of alleles in a small population that was formed by a recent bottleneck. Genetics 111:675–689
McGrady MJ, Hines JE, Rollie CJ, et al (2017) Territory occupancy and breeding success of Peregrine Falcons Falco peregrinus at various stages of population recovery. Ibis 159:285–296. https://doi.org/10.1111/ibi.12443
Mearns R, Newton I (1984) Turnover and dispersal in a Peregrine Falco peregrinus population. Ibis 126:347–355 https://doi.org/10.1111/j.1474-919X.1984.tb00255.x
Meijer SN, Halsall CJ, Harner T, et al (2001) Organochlorine pesticide residues in archived UK soil. Environ Sci Technol 35:1989–1995. https://doi.org/10.1021/es0000955
Millsap BA, Allen GT (2006) Effects of falconry harvest on wild raptor populations in the United States: theoretical considerations and management recommendations. Wildl Soc Bull 34:1392–1400. https://doi.org/10.2193/0091-7648(2006)34[1392:eofhow]2.0.co;2
Narum SR, Buerkle CA, Davey JW, Miller MR, Hohenlohe PA. (2013) Genotyping-by-sequencing in ecological and conservation genomics. Mol Ecol 22:2841–2847. doi:10.1111/mec.12350
Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590
Newton I (1988) Changes in the status of the peregrine falcon in Europe: an overview. In: Cade TJ, Enderson JH, Thelander CG, White CM (eds) Peregrine populations, their management and recovery. The Peregrine Fund, Boise, pp 227–234
Nesje M, Røed KH, Bell DA, et al (2000) Microsatellite analysis of population structure and genetic variability in peregrine falcons (Falco peregrinus). Anim Conserv 3:267–275. https://doi.org/10.1017/S1367943000000998
Nicholls MK, Franklin J, Vega R, Jackson H (2017) Return of the Sussex peregrine: where have they come from? In: Proceedings of the International Conference on the Stewardship of Biodiversity and Sustainable Use. Irish Hawking Club and International Association of Falconry and Conservation of Birds of Prey, Moyvalley
Nittinger F, Haring E, Pinsker W, et al (2005) Out of Africa? Phylogenetic relationships between Falco biarmicus and the other hierofalcons (Aves: Falconidae). J Zool Syst Evol Res 43:321–331. https://doi.org/10.1111/j.1439-0469.2005.00326.x
Nomura T (2008) Estimation of effective number of breeders from molecular coancestry of single cohort sample. Evol Appl 1:462–474. https://doi.org/10.1111/j.1752-4571.2008.00015.x
Norriss DW (1995) The 1991 survey and weather impacts on the peregrine Falco peregrinus breeding population in the Republic of Ireland. Bird Study 42:20–30. https://doi.org/10.1080/00063659509477144
Paetkau D, Slade R, Burden M, Estoup A (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: A simulation-based exploration of accuracy and power. Mol Ecol 13:55–65. https://doi.org/10.1046/j.1365-294X.2004.02008.x
Peakall R, Smouse PE (2012) GenALEx 6.5: Genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539. https://doi.org/10.1093/bioinformatics/bts460
Penteriani V, Ferrer M, Delgado MM (2011) Floater strategies and dynamics in birds, and their importance in conservation biology: Towards an understanding of nonbreeders in avian populations. Anim Conserv 14:233–-241. https://doi.org/10.1111/j.1469-1795.2010.00433.x
Piry S, Alapetite A, Cornuet JM, et al (2004) GENECLASS2: A software for genetic assignment and first-generation migrant detection. J Hered 95:536–539. https://doi.org/10.1093/jhered/esh074
Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: A computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503. https://doi.org/10.1093/jhered/90.4.502
Pompanon F, Bonin A, Bellemain E, Taberlet P (2005) Genotyping errors: Causes, consequences and solutions. Nat Rev Genet 6:847–859. https://doi.org/10.1038/nrg1707
Ponnikas S, Ollila T, Kvist L (2017) Turnover and post-bottleneck genetic structure in a recovering population of Peregrine Falcons Falco peregrinus. Ibis 159:311–323. https://doi.org/10.1111/ibi.12460
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959. https://doi.org/10.1111/j.1471-8286.2007.01758.x
Puechmaille SJ (2016) The program structure does not reliably recover the correct population structure when sampling is uneven: Subsampling and new estimators alleviate the problem. Mol Ecol Resour 16:608–627. https://doi.org/10.1111/1755-0998.12512
Raisin C, Dawson DA, Greenwood AG, Jones CG, Groombridge JJ (2009) Characterisation of Mauritius Parakeet (Psittacula eques) microsatellite loci and their cross‐utility in other parrots (Psittacidae, Aves). Mol Ecol Resour 9:1231–1235. https://doi.org/10.1111/j.1755-0998.2009.02621.x
Ramasamy RK, Ramasamy S, Bindroo BB, Naik VG (2014) STRUCTURE PLOT: A program for drawing elegant STRUCTURE bar plots in user friendly interface. SpringerPlus 3:431. https://doi.org/10.1186/2193-1801-3-431
Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100. https://doi.org/10.1093/oxfordjournals.molbev.a004034
Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 94:9197–9201. https://doi.org/10.1073/pnas.94.17.9197
Ratcliffe DA (1963) The status of the Peregrine in Great Britain. Bird Study. https://doi.org/10.1080/00063656309476042
Ratcliffe DA (1972) The Peregrine population of Great Britain in 1971. Bird Study 19:117–156. https://doi.org/10.1080/00063657209476336
Ratcliffe DA (1984) The peregrine breeding population of the United Kingdom in 1981. Bird Study 31:1–18. https://doi.org/10.1080/00063658409476809
Ratcliffe DA (1993) The peregrine falcon, 2nd edn. T & AD Poyser, London
Ratcliffe DA (2003) The peregrine saga. In: Thompson DBA, Redpath S, Fielding AH, Marquiss M, Galbraith CA (eds) Birds of prey in a changing environment. The Stationary Office, Edinburgh, pp 91–98.
Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283. https://doi.org/10.2307/2410454
Rousset F (2008) GENEPOP’007: A complete re-implementation 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
Saar C (1988) Reintroduction of the peregrine falcon in Germany. In: Cade TJ, Enderson JH, Thelander CG, White CM (eds) Peregrine falcon populations: their management and recovery. Peregrine Fund, Idaho, pp 629–636
Sielicki J, Mizera T (2009) Peregrine Falcon populations – status and perspectives in the 21st century, European Peregrine Falcon Working Group, Society for the Protection of Wild Animals "Falcon". Turul/Poznań University of Life Sciences Press, Warsaw-Poznań
Smith GD, Murillo-García OE, Hostetler JA, et al (2015) Demography of population recovery: survival and fidelity of peregrine falcons at various stages of population recovery. Oecologia 178:391–401. https://doi.org/10.1007/s00442-014-3168-3
Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573. https://doi.org/10.1038/sj.hdy.6885180
Sonsthagen SA, Coonan TJ, Latta BC, et al (2012) Genetic diversity of a newly established population of golden eagles on the Channel Islands, California. Biol Conserv 146:116–122. https://doi.org/10.1016/j.biocon.2011.11.031
Talbot SL, Palmer AG, Sage GK, et al (2011) Lack of genetic polymorphism among peregrine falcons Falco peregrinus of Fiji. J Avian Biol 42:415–428. https://doi.org/10.1111/j.1600-048X.2011.05280.x
Talbot SL, Sage GK, Sonsthagen SA, et al (2017) Intraspecific evolutionary relationships among peregrine falcons in western North American high latitudes. PLoS One 12: e0188185. https://doi.org/10.1371/journal.pone.0188185
Tordoff HB, Redig PT (1997) Midwest Peregrine Falcon demography, 1982-1995. J Raptor Res 31:339–346
Tordoff HB, Redig PT (2001) Role of genetic background in the success of reintroduced peregrine falcons. Conserv Biol 15:528–532. https://doi.org/10.1046/j.1523-1739.2001.015002528.x
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. https://doi.org/10.1111/j.1471-8286.2004.00684.x
Wandeler P, Hoeck PEA, Keller LF (2007) Back to the future: museum specimens in population genetics. Trends Ecol Evol 22:634–642.
Wells JH, Ruddock M (2009) Population dynamics of the peregrine falcon in Northern Ireland. In: Sielicki J, Mizera T (ed) Peregrine Falcon populations – status and perspectives in the 21st century, European Peregrine Falcon Working Group, Society for the Protection of Wild Animals "Falcon". Turul/Poznań University of Life Sciences Press, Warsaw-Poznań, pp 281–294
White CM (1994) Family Falconidae. In: del Hoyo J, Elliot A, Sargatal J (eds) Handbook of birds of the world, Volume 2: New World Vultures to Guinea fowl. Lynx Edicions, Barcelona, pp 216–275
White CM, Cade TJ, Enderson JH (2013a) Peregrine falcons of the world. Lynx Edicions, Barcelona
White CM, Sonsthagen SA, Sage GK, et al (2013b) Genetic relationships among some subspecies of the Peregrine Falcon (Falco peregrinus L.), inferred from mitochondrial DNA control-region sequences. The Auk 130:78–87. https://doi.org/10.1525/auk.2012.11173
Wilson MW, Balmer DE, Jones K, et al (2018) The breeding population of Peregrine Falcon Falco peregrinus in the United Kingdom, Isle of Man and Channel Islands in 2014. Bird Study 65:1–19. https://doi.org/10.1080/00063657.2017.1421610
Wink M (2019) Phylogeny of Falconidae and phylogeography of Peregrine Falcons. Ornis Hungarica 26:27–37. https://doi.org/10.1515/orhu-2018-0013
Zink RM, Barrowclough GF (2008) Mitochondrial DNA under siege in avian phylogeography. Mol Ecol 17:2107–2121. https://doi.org/10.1111/j.1365-294X.2008.03737.x

Additional information

This project was partially funded by the Sussex Peregrine Study, code 8309- Research: Other Sources; 10069 – Human & Life Sciences; G90406 - H & LS Research

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Hauffe, H., Giménez, M., Vega, R., White, T. and Searle, J. 2011. Properties of a hybrid zone between highly distinct chromosomal races of the house mouse (Mus musculus domesticus) in northern Italy, and comparisons with other hybrid zones. Cytogenetic and Genome Research. 134 (3), pp. 191-199. https://doi.org/10.1159/000327717
How Varroa Parasitism affects the immunological and nutritional status of the honey bee, Apis mellifera
Aronstein, K., Saldivar, E., Vega, R., Westmiller, S. and Douglas, A. 2012. How Varroa Parasitism affects the immunological and nutritional status of the honey bee, Apis mellifera. Insects. 3 (3), pp. 601-615.
Genetic and morphological variation in a Mediterranean glacial refugium: evidence from Italian pygmy shrews, Sorex minutus (Mammalia: Soricomorpha)
Vega, R., Amori, G., Aloise, G., Cellini, S., Loy, A. and Searle, J. 2010. Genetic and morphological variation in a Mediterranean glacial refugium: evidence from Italian pygmy shrews, Sorex minutus (Mammalia: Soricomorpha). Biological Journal of the Linnean Society. 100 (4), pp. 774-787. https://doi.org/10.1111/j.1095-8312.2010.01454.x
Population genomics applications for conservation: the case of the tropical dry forest dweller Peromyscus melanophrys
Vega, R., Vázquez-Domínguez, E., White, T., Valenzuela-Galván, D. and Searle, J. 2016. Population genomics applications for conservation: the case of the tropical dry forest dweller Peromyscus melanophrys. Conservation Genetics. https://doi.org/10.1007/s10592-016-0907-5
Ecogeographical patterns of morphological variation in pygmy shrews Sorex minutus (Soricomorpha: Soricinae) within a phylogeographic and continental-and-island framework
Vega, R., McDevitt, A., Krystufek, B. and Searle, J. 2016. Ecogeographical patterns of morphological variation in pygmy shrews Sorex minutus (Soricomorpha: Soricinae) within a phylogeographic and continental-and-island framework. Biological Journal of the Linnean Society. https://doi.org/10.1111/bij.12858
Northern glacial refugia for the pygmy shrew (Sorex minutus) in Europe revealed by phylogeographic analyses and species distribution modelling.
Vega, R., Fløjgaard, C., Lira-Noriega, A., Nakazawa, Y., Svenning, J. and Searle, J. 2010. Northern glacial refugia for the pygmy shrew (Sorex minutus) in Europe revealed by phylogeographic analyses and species distribution modelling. Ecography. 33 (2), pp. 260-271. https://doi.org/10.1111/j.1600-0587.2010.06287.x
Multiple refugia and barriers explain the phylogeography of the Valais shrew, Sorex antinorii (Mammalia: Soricomorpha)
Yannic, G., Pellissier, L., Dubey, S., Vega, R., Basset, P., Mazzotti, S., Hauffe, H., Searle, J. and Hausser, J. 2012. Multiple refugia and barriers explain the phylogeography of the Valais shrew, Sorex antinorii (Mammalia: Soricomorpha). Biological Journal of the Linnean Society. 105 (4), pp. 864-880. https://doi.org/10.1111/j.1095-8312.2011.01824.x
Colonisation of Ireland: revisiting ‘the pygmy shrew syndrome’ using mitochondrial, Y chromosomal and microsatellite markers
McDevitt, A., Vega, R., Rambau, R., Yannic, G., Herman, J., Hayden, T. and Searle, J. 2011. Colonisation of Ireland: revisiting ‘the pygmy shrew syndrome’ using mitochondrial, Y chromosomal and microsatellite markers. Heredity. 107 (6), pp. 548-557. https://doi.org/10.1038/hdy.2011.41