Abstract
Genetic variability and population structure in osprey were studied using DNA microsatellite markers. Special emphasis was placed on the subspecies living in the Afro-Palearctic (Pandion haliaetus haliaetus). For comparative purposes, American osprey subspecies (P. h. carolinensis, P. h. ridgway) and Indo/Australian subspecies (P. h. cristatus) were included in this analysis. Twenty DNA microsatellite loci were analysed across a total of 200 individuals. Cluster analysis of genetic distances generally grouped populations of osprey in accordance with their subspecific designation and with previous results from mtDNA analysis. Ospreys from America and Australia were clearly separated from P. h. haliaetus suggesting a more ancient isolation which prevented recent gene flow across these groups. Within P. h. haliaetus, significant genetic differentiation was found between populations in northern and southern Europe, suggesting that the Afro-Palearctic group is structured into two interconnected entities (Mediterranean and continental Europe). Population structuring was supported by an assignment test and by analysis of allele-sharing among individuals. At the Mediterranean scale, no significant differences of allelic information were found between populations. Behaviours such as dispersal, migration and philopatry seem to have played simultaneously and in contrary directions in shaping the genetic structure and diversity of populations. Our results provide essential information for reconstructing gene flow and genetic variability among osprey populations at different scales, which call for caution in the proactive management and conservation of the species, namely in the Mediterranean area.
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Agudo R, Rico C, Hiraldo F, Donázar JA (2011) Evidence of connectivity between continental and differentiated insular populations in a highly mobile species. Divers Distrib 17:1–12. https://doi.org/10.1111/j.1472-4642.2010.00724.x
Alerstam T, Hake M, Kjellén N (2006) Temporal and spatial patterns of repeated migratory journeys by ospreys. Anim Behav 71:555–566
Bai M-L, Schmidt D (2011) Differential migration by age and sex in central European Ospreys Pandion haliaetus. J Ornithol 153:75–84. https://doi.org/10.1007/s10336-011-0697-y
Belkhir K, Borsa P, Chikhi L et al. (2004) GENETIX 4.05, logiciel sous Windows pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000. Université de Montpellier II, Montpellier
Berthold P (2001) Bird Migration: A General Survey, Second edn. Oxford University Press, Oxford
Bretagnolle V, Mougeot F, Thibault JC (2008) Density dependence in a recovering osprey population: demographic and behavioural processes. J Anim Ecol 77:998–1007
Cadahía L, López-López P, Urios V, Soutullo A, Negro JJ (2009) Natal dispersal and recruitment of two Bonelli’s Eagles Aquila fasciata: a four-year satellite tracking study. Acta Ornithol 44:193–198
Clobert J, Danchin E, Dhondt AA, Nichols JD (2001) Dispersal. Oxford University Press, Oxford
Cramp S, Simmons KEL (1980) Handbook of the birds of Europe, the Middle East and North Africa. The birds of the Western Palearctic, vol 2. Oxford University Press, Oxford
Cresswell W (2014) Migratory connectivity of Palaearctic–African migratory birds and their responses to environmental change: the serial residency hypothesis. Ibis 156:493–510
Crooks KR, Sanjayan M (2006) Connectivity conservation. Cambridge University Press, Cambridge
Dawson DA, Kleven O, Dos Remedios N, Horsburgh GJ, Kroglund RT, Santos T, Hewitt CRA (2015) A multiplex microsatellite set for non-invasive genotyping and sexing of the osprey (Pandion haliaetus). Conserv Genet Resour 7:887–894
Dennis R, Dixon H (2001) The experimental reintroduction of Ospreys Pandion haliaetus from Scotland to England. Vogelwelt 122:147–154
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
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
Frankham R, Briscoe DA, Ballou JD (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge
García JT, Alda F, Terraube J, Mougeot F, Sternalski A, Bretagnolle V, Arroyo B (2011) Demographic history, genetic structure and gene flow in a steppe-associated raptor species. BMC Evol Biol 11:333. https://doi.org/10.1186/1471-2148-11-333
Goudet J (2002) FSTAT (version 2.9.3.2): a program to estimate and test gene diversities and fixation indices. F Stat J Hered. 86: 485–486, http://www2.unil.ch/ize/softwares/fsata.html
Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162
Griffiths R, Double MC, Orr K, Dawson RJ (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075
Hanski IA, Giplin M (1997) Metapopulation dynamics: ecology, genetics and evolution. Academic Press, San Diego, CA
Hernández-Matías A, Real J, Pradel R, Ravayrol A, Vincent-Martin N, Bosca F, Cheylan G (2010) Determinants of territorial recruitment in Bonelli’s eagle (Aquila fasciata) populations. Auk 127:173–184
Höglund J (2009) Evolutionary conservation genetics. Oxford University Press, Oxford
Horton TW, Bierregaard O, Zawarreza P, Holdaway RN, Sagar P (2014) Juvenile osprey navigation during transoceanic migration. PLoS ONE 9:e114557
Klaassen RHG, Strandberg R, Hake M, Alerstam T (2008) Flexibility in daily travel routines causes regional variation in bird migration speed. Behav Ecol Sociobiol 62:427–1432
Ladle RJ, Whittaker RJ (2011) Conservation biogeography. Wiley-Blackwell, Oxford. https://doi.org/10.1002/9781444390001
Limiñana R, Garcia JT, Miguel Gonzalez J, Guerrero A, Lavedan J, Damian Moreno J, Roman-Munoz A, Palomares LE, Pinilla A, Ros G, Serrano C, Surroca M, Tena J, Arroyo B (2012) Philopatry and natal dispersal of Montagu’s harriers (Circus pygargus) breeding in Spain: a review of existing data. Eur J Wildlife Res 58:549–555
MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, Princeton
Mackrill TR (2017) Migratory behaviour and ecology of a trans-saharan migrant raptor, the osprey Pandion haliaetus. PhD Thesis, University of Leicester
Malausa T, Gilles A, Meglécz E et al (2011) High-throughput microsatellite isolation through 454 GS-FLX titanium pyrosequencing of enriched DNA libraries. Mol Ecol Resour 11:638–644. https://doi.org/10.1111/j.1755-0998.2011.02992.x
Martell MS, Englund JV, Tordoff HB (2002) An urban Osprey population established by translocation. J Raptor Res 36:91–96
Meirmans PG (2014) Nonconvergence in Bayesian estimation of migration rates. Mol Ecol Resour 14:726–733. https://doi.org/10.1111/1755-0998.12216
Miller MP, Mullins TD, Parrish JW, Walters JR, Haig SM (2012) Variation in migratory behavior influences regional genetic diversity and structure among American Kestrel populations (Falco sparverius) in North America. J Hered 103(4):503–514
Monti F (2012) The Osprey, Pandion haliaetus. State of knowledge and conservation of the breeding population of the Mediterranean basin. Initiative PIM
Monti F, Nibani H, Dominici JM, Rguibi Idrissi H, Thévenet M, Beaubrun PC, Duriez O (2013) The vulnerable Osprey breeding population of the Al Hoceima National Park, Morocco: present status and threats. Ostrich 84(3):199–204
Monti F, Dominici JM, Choquet R, Duriez O, Sammuri G, Sforzi A (2014) The Osprey reintroduction in Central Italy: dispersal, survival and first breeding data. Bird Study 61:465–473
Monti F, Duriez O, Arnal V, Dominici JM, Sforzi A, Fusani L, Gremillet D, Montgelard C (2015) Being cosmopolitan: evolutionary history and phylogeography of a specialized raptor, the osprey Pandion haliaetus. BMC Evol Biol 15:255
Monti F, Grémillet D, Sforzi A, Sammuri G, Dominici JM, Triay Bagur R, Muñoz Navarro A, Fusani L, Duriez O (2018) Migration and wintering strategies in vulnerable Mediterranean Osprey populations. Ibis. https://doi.org/10.1111/ibi.12567
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
Newton I (2003) Population limitation in birds. Academic Press, San Diego
Newton I (2010) Bird migration. Collins, London
Peakall ROD, Smouse PE (2006) Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
Poole AF (1989) Ospreys: a natural and unnatural history. Cambridge University Press, Cambridge
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Rousset F (2008) Genepop’007: a complete reimplementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106
Salanti G, Amountza G, Ntzani EE, Ioannidis JPA (2005) Hardy–Weinberg equilibrium in genetic association studies: an empirical evaluation of reporting, deviations, and power. Eur J Hum Genet 13:840–848. https://doi.org/10.1038/sj.ejhg.5201410
Schmidt-Rothmund D, Dennis R, Saurola P (2014) The osprey in the western palearctic: breeding population size and trends in the early 21st century. J Raptor Res 48:375–386
Strandberg R (2013) Ageing, sexing and subspecific identification of Osprey, and two WP records of American Osprey. Dutch Bird 35:69–87
Väli Ü, Sellis U (2016) Migration patterns of the Osprey Pandion haliaetus on the Eastern European-East African flyway. Ostrich 87:23–28
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
Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163(3):1177–1191
Zwarts L, Bijlsma RG, van der Kamp J, Wymenga E, Zwarts J, Visser D (2009) Living on the edge: wetlands and birds in a changing Sahel. 1st edn. KNNV Publishing, Zeist
Acknowledgements
This research was financially supported by the Foundation Prince Albert II de Monaco and the Associazone Italiana della Fondation Prince Albert II de Monaco ONLUS, the Corsica Natural Regional Park (France), the Maremma Regional Park Agency (Italy) and the Tuscan Archipelago National Park (Italy). FM benefitted from a grant from the Maremma Regional Park and from a mobility grant from the Universitá Italo Francese/Université Franco Italienne.
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Monti, F., Delfour, F., Arnal, V. et al. Genetic connectivity among osprey populations and consequences for conservation: philopatry versus dispersal as key factors. Conserv Genet 19, 839–851 (2018). https://doi.org/10.1007/s10592-018-1058-7
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DOI: https://doi.org/10.1007/s10592-018-1058-7