Genomic Patterns of Iberian Wild Bees Reveal Levels of Diversity, Differentiation and Population Structure, Supporting the “Refugia within Refugia” Hypothesis
Sousa, Paulo de; Henriques, André; Silva, Sara E.et al.
genetic diversity; Iberian Peninsula; population structure; RADseq; wild bees; Ecology; Ecological Modeling; Agricultural and Biological Sciences (miscellaneous); Nature and Landscape Conservation
Abstract :
[en] We used a population genomic approach to unravel the population structure, genetic differentiation, and genetic diversity of three widespread wild bee species across the Iberian Peninsula, Andrena agilissima, Andrena flavipes and Lasioglossum malachurum. Our results demonstrated that genetic lineages in the Ebro River valley or near the Pyrenees mountains are different from the rest of Iberia. This relatively congruent pattern across species once more supports the hypothesis of “refugia within refugia” in the Iberian Peninsula. The results for A. flavipes and A. agilissima showed an unexpected pattern of genetic differentiation, with the generalist polylectic A. flavipes having lower levels of genetic diversity (Ho = 0.0807, He = 0.2883) and higher differentiation (FST = 0.5611), while the specialist oligolectic A. agilissima had higher genetic diversity (Ho = 0.2104, He = 0.3282) and lower differentiation values (FST = 0.0957). For L. malachurum, the smallest and the only social species showed the lowest inbreeding coefficient (FIS = 0.1009) and the lowest differentiation level (FST = 0.0663). Overall, our results, suggest that this pattern of population structure and genetic diversity could be explained by the combined role of past climate changes and the life-history traits of the species (i.e., size, sociality and host-plant specialization), supporting the role of the Iberian refugia as a biodiversity hotspot.
Disciplines :
Zoology
Author, co-author :
Sousa, Paulo de ; cE3c—Center for Ecology, Evolution and Environmental Changes, CHANGE—Global Change and Sustainability Institute, Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, Lisboa, Portugal
Henriques, André ; cE3c—Center for Ecology, Evolution and Environmental Changes, CHANGE—Global Change and Sustainability Institute, Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, Lisboa, Portugal
Silva, Sara E.; cE3c—Center for Ecology, Evolution and Environmental Changes, CHANGE—Global Change and Sustainability Institute, Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, Lisboa, Portugal
Carvalheiro, Luísa G. ; cE3c—Center for Ecology, Evolution and Environmental Changes, CHANGE—Global Change and Sustainability Institute, Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, Lisboa, Portugal ; Department of Ecology, Universidade Federal de Goiás, Goiânia, Brazil
Smagghe, Guy ; Laboratory of Agrozoology, Department of Plants and Crops, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium ; Molecular and Cellular Life Sciences, Department of Biology, Vrije Universiteit Brussel (VUB), Brussels, Belgium
Michez, Denis ; Université de Mons - UMONS > Faculté des Sciences > Service de Zoologie
Wood, Thomas James ; Université de Mons - UMONS > Faculté des Sciences > Service de Zoologie
Paulo, Octávio S. ; cE3c—Center for Ecology, Evolution and Environmental Changes, CHANGE—Global Change and Sustainability Institute, Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, Lisboa, Portugal
Language :
English
Title :
Genomic Patterns of Iberian Wild Bees Reveal Levels of Diversity, Differentiation and Population Structure, Supporting the “Refugia within Refugia” Hypothesis
Publication date :
June 2023
Journal title :
Diversity
eISSN :
1424-2818
Publisher :
Multidisciplinary Digital Publishing Institute (MDPI)
Fundação para a Ciência e Tecnologia Excellence of Science
Funding text :
This work was supported by the Project ‘Effect of Eutrophication and Climate on Pollinators and ecosystem service provision’ (EUCLIPO), co-funded by national funds through Fundação para a Ciência e Tecnologia (FCT), Portugal (PTDC/BIA-ECO/28360/2017), and by EU ERDF funds within the Portugal 2020 Partnership Agreement and Programa Operacional Regional Lisboa. DM and TJW were partly supported by the FNRS/FWO joint program “EOS—Excellence of Science” for the project “CliPS: Climate change and its effects on Pollination Services (project 30947854)”.
Cardoso P. Barton P.S. Birkhofer K. Chichorro F. Deacon C. Fartmann T. Fukushima C.S. Gaigher R. Habel J.C. Hallmann C.A. et al. Scientists’ Warning to Humanity on Insect Extinctions Biol. Conserv. 2020 242 108426 10.1016/j.biocon.2020.108426
Potts S.G. Biesmeijer J.C. Kremen C. Neumann P. Schweiger O. Kunin W.E. Global Pollinator Declines: Trends, Impacts and Drivers Trends Ecol. Evol. 2010 25 345 353 10.1016/j.tree.2010.01.007
Ollerton J. Winfree R. Tarrant S. How Many Flowering Plants Are Pollinated by Animals? Oikos 2011 120 321 326 10.1111/j.1600-0706.2010.18644.x
Bates A.J. Sadler J.P. Fairbrass A.J. Falk S.J. Hale J.D. Matthews T.J. Changing Bee and Hoverfly Pollinator Assemblages along an Urban-Rural Gradient PLoS ONE 2011 6 e23459 10.1371/journal.pone.0023459 21858128
Winfree R. Bartomeus I. Cariveau D.P. Native Pollinators in Anthropogenic Habitats Annu. Rev. Ecol. Evol. Syst. 2011 42 1 22 10.1146/annurev-ecolsys-102710-145042
Nieto A. Roberts S.P.M. Kemp J. Rasmont P. Kuhlmann M. García Criado M. Biesmeijer J.C. Bogusch P. Dathe H.H. De la Rúa P. et al. European Red List of Bees Publication Office of the European Union Luxembourg 2014 9789279445125
Danforth B.N. Cardinal S. Praz C. Almeida E.A.B. Michez D. The Impact of Molecular Data on Our Understanding of Bee Phylogeny and Evolution Annu. Rev. Entomol. 2013 58 57 78 10.1146/annurev-ento-120811-153633
Geldmann J. González-Varo J.P. Conserving Honey Bees Does Not Help Wildlife Science 2018 359 392 393 10.1126/science.aar2269
Wood T.J. Michez D. Paxton R.J. Drossart M. Neumann P. Gérard M. Vanderplanck M. Barraud A. Martinet B. Leclercq N. et al. Managed Honey Bees as a Radar for Wild Bee Decline? Apidologie 2020 51 1100 1116 10.1007/s13592-020-00788-9
López-Uribe M.M. Ricigliano V.A. Simone-Finstrom M. Defining Pollinator Health: A Holistic Approach Based on Ecological, Genetic, and Physiological Factors Annu. Rev. Anim. Biosci. 2020 8 269 294 10.1146/annurev-animal-020518-115045
Pauls S.U. Nowak C. Balint M. Pfenninger M. The Impact of Global Climate Change on Genetic Diversity within Populations and Species Mol. Ecol. 2013 22 925 946 10.1111/mec.12152
Maebe K. Karise R. Meeus I. Mänd M. Smagghe G. Pattern of Population Structuring between Belgian and Estonian Bumblebees Sci. Rep. 2019 9 9651 10.1038/s41598-019-46188-7
Maebe K. Meeus I. Ganne M. De Meulemeester T. Biesmeijer K. Smagghe G. Microsatellite Analysis of Museum Specimens Reveals Historical Differences in Genetic Diversity between Declining and More Stable Bombus Species PLoS ONE 2015 10 e0127870 10.1371/journal.pone.0127870
Maebe K. Meeus I. Vray S. Claeys T. Dekoninck W. Boevé J.L. Rasmont P. Smagghe G. A Century of Temporal Stability of Genetic Diversity in Wild Bumblebees Sci. Rep. 2016 6 38289 10.1038/srep38289
Dreier S. Redhead J.W. Warren I.A. Bourke A.F.G. Heard M.S. Jordan W.C. Sumner S. Wang J. Carvell C. Fine-Scale Spatial Genetic Structure of Common and Declining Bumble Bees across an Agricultural Landscape Mol. Ecol. 2014 23 3384 3395 10.1111/mec.12823
Lozier J.D. Revisiting Comparisons of Genetic Diversity in Stable and Declining Species: Assessing Genome-Wide Polymorphism in North American Bumble Bees Using RAD Sequencing Mol. Ecol. 2014 23 788 801 10.1111/mec.12636
Orr M.C. Hughes A.C. Chesters D. Pickering J. Zhu C.D. Ascher J.S. Global Patterns and Drivers of Bee Distribution Curr. Biol. 2021 31 451 458.e4 10.1016/j.cub.2020.10.053
Taberlet P. Fumagalli L. Wust-Saucy A.G. Cosson J.F. Comparative Phylogeography and Postglacial Colonization Routes in Europe Mol. Ecol. 1998 7 453 464 10.1046/j.1365-294x.1998.00289.x
Hewitt G. The Genetic Legacy of the Quaternary Ice Ages Nature 2000 405 907 913 10.1038/35016000
Gómez A. Lunt D.H. Refugia within Refugia: Patterns of Phylogeographic Concordance in the Iberian Peninsula Phylogeography of Southern European Refugia Weiss S. Ferrand N. Springer Berlin/Heidelberg, Germany 2007 155 188 9781402049033
Blondel J. Aronson J. Bodiou J.-Y. Boeuf G. The Mediterranean Region Biological Diversity in Space and Time 2nd ed. Oxford University Press Oxford, UK 2010
Miraldo A. Hewitt G.M. Paulo O.S. Emerson B.C. Phylogeography and Demographic History of Lacerta Lepida in the Iberian Peninsula: Multiple Refugia, Range Expansions and Secondary Contact Zones BMC Evol. Biol. 2011 11 170 10.1186/1471-2148-11-170
Chávez-Galarza J. Henriques D. Johnston J.S. Carneiro M. Rufino J. Patton J.C. Pinto M.A. Revisiting the Iberian Honey Bee (Apis mellifera iberiensis) Contact Zone: Maternal and Genome-Wide Nuclear Variations Provide Support for Secondary Contact from Historical Refugia Mol. Ecol. 2015 24 2973 2992 10.1111/mec.13223
Silva S.E. Seabra S.G. Carvalheiro L.G. Nunes V.L. Marabuto E. Mendes R. Rodrigues A.S.B. Pina-Martins F. Yurtsever S. Laurentino T.G. et al. Population Genomics of Bombus Terrestris Reveals High but Unstructured Genetic Diversity in a Potential Glacial Refugium Biol. J. Linn. Soc. 2020 129 259 272 10.1093/biolinnean/blz182
Hewitt G.M. Some Genetic Consequences of Ice Ages, and Their Role, in Divergence and Speciation Biol. J. Linn. Soc. 1996 58 247 276 10.1006/bijl.1996.0035
Packer L. Zayed A. Grixti J.C. Ruz L. Owen R.E. Vivallo F. Toro H. Conservation Genetics of Potentially Endangered Mutualisms: Reduced Levels of Genetic Variation in Specialist versus Generalist Bees Conserv. Biol. 2005 19 195 202 10.1111/j.1523-1739.2005.00601.x
Dellicour S. Michez D. Mardulyn P. Comparative Phylogeography of Five Bumblebees: Impact of Range Fragmentation, Range Size and Diet Specialization Biol. J. Linn. Soc. 2015 116 926 939 10.1111/bij.12636
Dellicour S. Michez D. Rasplus J.-Y. Mardulyn P. Impact of Past Climatic Changes and Resource Availability on the Population Demography of Three Food-Specialist Bees Mol. Ecol. 2015 24 1074 1090 10.1111/mec.13085
Lepais O. Darvill B. O’Connor S. Osborne J.L. Sanderson R.A. Cussans J. Goffe L. Goulson D. Estimation of Bumblebee Queen Dispersal Distances Using Sibship Reconstruction Method Mol. Ecol. 2010 19 819 831 10.1111/j.1365-294X.2009.04500.x
López-Uribe M.M. Jha S. Soro A. A Trait-Based Approach to Predict Population Genetic Structure in Bees Mol. Ecol. 2019 28 1 11 10.1111/mec.15028
Falk S.J. Field Guide to the Bees of Great Britain and Ireland Bloomsbury Publishing London, UK 2015 Volume 14 9781472967053
Güler Y. Sorkun K. Analysis of Pollen Collected by Andrena flavipes Panzer (Hymenoptera: Andrenidae) in Sweet Cherry Orchards, Afyonkarahisar Province of Turkey Psyche 2010 2010 160789 10.1155/2010/160789
Paxton R.J. Giovanetti M. Andrietti F. Scamoni E. Scanni B. Mating in a Communal Bee, Andrena agilissima (Hymenoptera Andrenidae) Ethol. Ecol. Evol. 1999 11 371 382 10.1080/08927014.1999.9522820
Polidori C. Rubichi A. Barbieri V. Trombino L. Donegana M. Floral Resources and Nesting Requirements of the Ground-Nesting Social Bee, Lasioglossum malachurum (Hymenoptera: Halictidae), in a Mediterranean Semiagricultural Landscape Psyche 2010 2010 851947 10.1155/2010/851947
Hajibabaei M. Janzen D.H. Burns J.M. Hallwachs W. Hebert P.D.N. DNA Barcodes Distinguish Species of Tropical Lepidoptera Proc. Natl. Acad. Sci. USA 2006 103 968 971 10.1073/pnas.0510466103
Folmer O. Black M. Hoeh W. Lutz R. Vrijenhoek R. DNA Primers for Amplification of Mitochondrial Cytochrome c Oxidase Subunit I from Diverse Metazoan Invertebrates Mol. Mar. Biol. Biotechnol. 1994 3 294 299
Sequencher® Version 5.4.6; DNA Sequence Analysis Software Gene Codes Corporation Ann Arbor, MI, USA 2016
Larsson A. AliView: A Fast and Lightweight Alignment Viewer and Editor for Large Datasets Bioinformatics 2014 30 3276 3278 10.1093/bioinformatics/btu531
Chen S. Zhou Y. Chen Y. Gu J. Fastp: An Ultra-Fast All-in-One FASTQ Preprocessor Bioinformatics 2018 34 i884 i890 10.1093/bioinformatics/bty560
Danecek P. Auton A. Abecasis G. Albers C.A. Banks E. DePristo M.A. Handsaker R.E. Lunter G. Marth G.T. Sherry S.T. et al. The Variant Call Format and VCFtools Bioinformatics 2011 27 2156 2158 10.1093/bioinformatics/btr330
Lischer H.E.L. Excoffier L. PGDSpider: An Automated Data Conversion Tool for Connecting Population Genetics and Genomics Programs Bioinformatics 2012 28 298 299 10.1093/bioinformatics/btr642
Cabreros I. Storey J.D. A Likelihood-Free Estimator of Population Structure Bridging Admixture Models and Principal Components Analysis Genetics 2019 212 1009 1029 10.1534/genetics.119.302159
Pina-Martins F. Silva D.N. Fino J. Paulo O.S. Structure_threader: An Improved Method for Automation and Parallelization of Programs Structure, FastStructure and MavericK on Multicore CPU Systems Mol. Ecol. Resour. 2017 17 e268 e274 10.1111/1755-0998.12702
Jombart T. Adegenet: A R Package for the Multivariate Analysis of Genetic Markers Bioinformatics 2008 24 1403 1405 10.1093/bioinformatics/btn129
R Core Team R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria Available online: https://www.r-project.org (accessed on 26 March 2020)
Malinsky M. Trucchi E. Lawson D.J. Falush D. RADpainter and FineRADstructure: Population Inference from RADseq Data Mol. Biol. Evol. 2018 35 1284 1290 10.1093/molbev/msy023 29474601
Goudet J. HIERFSTAT, a Package for R to Compute and Test Hierarchical F-Statistics Mol. Ecol. Notes 2005 5 184 186 10.1111/j.1471-8286.2004.00828.x
Kamvar Z.N. Tabima J.F. Grunwald N.J. Poppr: An R Package for Genetic Analysis of Populations with Clonal, Partially Clonal, and/or Sexual Reproduction PeerJ 2014 2 e281 10.7717/peerj.281 24688859
Jost L. GST and Its Relatives Do Not Measure Differentiation Mol. Ecol. 2008 17 4015 4026 10.1111/j.1365-294X.2008.03887.x
Winter D.J. Mmod: An R Library for the Calculation of Population Differentiation Statistics Mol. Ecol. Resour. 2012 12 1158 1160 10.1111/j.1755-0998.2012.03174.x
Korunes K.L. Samuk K. Pixy: Unbiased Estimation of Nucleotide Diversity and Divergence in the Presence of Missing Data Mol. Ecol. Resour. 2021 21 1359 1368 10.1111/1755-0998.13326
Exeler N. Kratochwil A. Hochkirch A. Strong Genetic Exchange among Populations of a Specialist Bee, Andrena vaga (Hymenoptera: Andrenidae) Conserv. Genet. 2008 9 1233 1241 10.1007/s10592-007-9450-8
Exeler N. Kratochwil A. Hochkirch A. Does Recent Habitat Fragmentation Affect the Population Genetics of a Heathland Specialist, Andrena fuscipes (Hymenoptera: Andrenidae)? Conserv. Genet. 2010 11 1679 1687 10.1007/s10592-010-0060-5
Jakobsson M. Edge M.D. Rosenberg N.A. The Relationship Between FST and the Frequency of the Most Frequent Allele Genetics 2013 193 515 528 10.1534/genetics.112.144758
Meirmans P.G. Hedrick P.W. Assessing Population Structure: FST and Related Measures Mol. Ecol. Resour. 2011 11 5 18 10.1111/j.1755-0998.2010.02927.x
Friedel A. Paxton R.J. Soro A. Spatial Patterns of Relatedness within Nesting Aggregations of the Primitively Eusocial Sweat Bee Lasioglossum malachurum Insectes Soc. 2017 64 465 475 10.1007/s00040-017-0559-6
Cruickshank T.E. Hahn M.W. Reanalysis Suggests That Genomic Islands of Speciation Are Due to Reduced Diversity, Not Reduced Gene Flow Mol. Ecol. 2014 23 3133 3157 10.1111/mec.12796
Zayed A. Packer L. The Population Genetics of a Solitary Oligolectic Sweat Bee, Lasioglossum (Sphecodogastra) Oenotherae (Hymenoptera: Halictidae) Heredity 2007 99 397 405 10.1038/sj.hdy.6801013
Su T. He B. Zhao F. Jiang K. Lin G. Huang Z. Population Genomics and Phylogeography of Colletes Gigas, a Wild Bee Specialized on Winter Flowering Plants Ecol. Evol. 2022 12 e8863 10.1002/ece3.8863
Smith B.H. Ayasse M. Kin-Based Male Mating Preferences in Two Species of Halictine Bee Behav. Ecol. Sociobiol. 1987 20 313 318 10.1007/BF00300676
Paxton R.J. Ayasse M. Field J. Soro A. Complex Sociogenetic Organization and Reproductive Skew in a Primitively Eusocial Sweat Bee, Lasioglossum malachurum, as Revealed by Microsatellites Mol. Ecol. 2002 11 2405 2416 10.1046/j.1365-294X.2002.01620.x
Paxton R.J. Male Mating Behaviour and Mating Systems of Bees: An Overview Apidologie 2005 36 145 156 10.1051/apido:2005007
Paxton R.J. Thorén P.A. Tengö J. Estoup A. Pamilo P. Mating Structure and Nestmate Relatedness in a Communal Bee, Andrena jacobi (Hymenoptera, Andrenidae), Using Microsatellites Mol. Ecol. 1996 5 511 519 10.1111/j.1365-294X.1996.tb00343.x
Richards M.H. French D. Paxton R.J. It’s Good to Be Queen: Classically Eusocial Colony Structure and Low Worker Fitness in an Obligately Social Sweat Bee Mol. Ecol. 2005 14 4123 4133 10.1111/j.1365-294X.2005.02724.x
Soro A. Ayasse M. Zobel M.U. Paxton R.J. Complex Sociogenetic Organization and the Origin of Unrelated Workers in a Eusocial Sweat Bee, Lasioglossum malachurum Insectes Soc. 2009 56 55 63 10.1007/s00040-008-1037-y