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Recent low levels of differentiation in the native Bombus ephippiatus (Hymenoptera: Apidae) along two Neotropical mountain-ranges in Guatemala

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Abstract

Recent anthropogenic fragmentation has led to population differentiation threatening viability of many species, including species specialized on mountainous ecosystems. Bombus ephippiatus, a widespread species mostly found in mountains in the Neotropics, seems to use the highlands as island, and deforested lowland areas may represent barriers to their dispersal, leading to isolation and potentially loss of genetic diversity. Yet, lack of knowledge of its population structure does not allow adequate management and conservation. To fill this knowledge gap, we assessed the population structure and inferred dispersion of B. ephippiatus in two mountain-ranges in Guatemala (Volcanic Chain and Sierra de las Minas). This region is characterized by high topographic variation and considerable deforestation strain. We analyzed the effects of elevation and land-use on genetic differentiation of B. ephippiatus populations and inferred its demography in the region. Our results suggest that B. ephippiatus is able to disperse long distances across most landscape types, reflected by its high genetic diversity, high effective population size, considerable gene flow, low population differentiation, as well as the lack of isolation by distance. Hence, B. ephippiatus may be a resilient species for the provision of pollination services. However, we detected a subtle divergence of B. ephippiatus into two clusters, of which Sierra de las Minas has been identified as a regional hotspot of genetic and species endemism. Yet, differentiation is very recent and hence likely caused by lowland deforestation. The combined effects of current forest cover and elevation partially explain the observed subtle patterns of differentiation suggesting that the maintenance of suitable habitat is crucial to ensure population connectivity of this keystone pollinator.

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References

  • Abrahamovich AH, Díaz NB, Morrone JJ (2004) Distributional patterns of the Neotropical and Andean species of the genus Bombus (Hymenoptera: Apidae). Acta Zool Mex 20:99–117

    Google Scholar 

  • Banda HJ, Paxton RJ (1991) Pollination of greenhouse tomatoes by bees. Acta Hortic 288:194–198

    Article  Google Scholar 

  • Birner R, Wittmer H, Berghöfer A, Mühlenberg M (2005) Prospects and challenges for biodiversity conservation in Guatemala. In: Markussen M, Buse R, Garrelts H, Máñez Costa MA, Menzel S, Marggraf R (eds) Valuation and conservation of biodiversity interdisciplinary perspectives on the convention on biological diversity. Springer, Berlin, pp 285–286

    Chapter  Google Scholar 

  • Brown MJF, Paxton RJ (2009) The conservation of bees: a global perspective. Apidologie 40:410–416

    Article  Google Scholar 

  • Cabrera A, Palsbøll P (2017) Inferring past demographic changes from contemporary genetic data: a simulation-based evaluation of the ABC methods implemented in DIYABC. Mol Ecol Resour 17:e94–e110

    Article  CAS  PubMed  Google Scholar 

  • Cano EB, Schuster JC, Morrone JJ (2018) Phylogenetics of Ogyges Kaup and the biogeography of Nuclear Central America (Coleoptera, Passalidae). ZooKeys 737:81–111

    Article  Google Scholar 

  • Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631

    Article  CAS  PubMed  Google Scholar 

  • Cornuet JM, Pudlo P, Veyssier J, Dehne-Garcia A, Gautier M, Leblois R, Marin JM et al (2014) DIYABC v2.0: a software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism. DNA sequence and microsatellite data. Bioinformatics 30:1187–1189

    Article  CAS  PubMed  Google Scholar 

  • Cousseau L, Husemann M, Foppen R, Vangestel C, Lens L (2016) A longitudinal genetic survey identifies temporal shifts in the population structure of Dutch house sparrows. Heredity 117:259–267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crawley MJ (2007) The R book. Wiley, West Sussex

    Book  Google Scholar 

  • Dardón MJ, Yurrita C, Landaverde-Gonzalez P, Vasquez M, Ayala R (2018) Preliminary assessment of bumblebees (Hymenoptera: Apoidea: Bombus Latreille 1802) that occur in Guatemala. Eur J Taxon (in press)

  • Darvill B, Ellis J, Lye G, Goulson D (2006) Population structure and inbreeding in a rare and declining bumblebee, Bombus muscorum (Hymenoptera: Apidae). Mol Ecol 15:601–611

    Article  CAS  PubMed  Google Scholar 

  • Darvill B, O’Connor S, Lye G, Waters J, Lepais O, Goulson D (2010) Cryptic differences in dispersal lead to differential sensitivity to habitat fragmentation in two bumblebee species. Mol Ecol 19:53–63

    Article  CAS  PubMed  Google Scholar 

  • De Palma A, Kuhlmann M, Roberts SPM, Potts SG, Börgre L, Hudson L, Lysenko I, Newbold T, Purvis A (2015) Ecological traits affect the sensitivity of bees to land-use pressures in European agricultural landscapes. J App Ecol 52:1567–1577

    Article  Google Scholar 

  • Dieringer D, Schlötterer C (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169

    Article  CAS  Google Scholar 

  • Duarte O, Gaiotto F, Costa M (2014) Genetic differentiation in the stingless bee, Scaptotrigona xanthotricha Moure, 1950 (Apidae, Meliponini): a species with wide geographic distribution in the Atlantic rainforest. J Hered 105:477–484

    Article  PubMed  Google Scholar 

  • Duennes MD, Vandame RV (2015) Bombus ephippiatus. The IUCN Red List of Threatened Species 2015: e.T21215149A21215217. https://doi.org/10.2305/IUCN.UK.2015-4.RLTS.T21215149A21215217.en

  • Duennes M, Lozier J, Hines H, Cameron S (2012) Geographical patterns of genetic divergence in the widespread Mesoamerican bumblebee Bombus ephippiatus (Hymenoptera: Apidae). Mol Phylogenet Evol 64:219–231

    Article  PubMed  Google Scholar 

  • Duennes M, Petranek C, Pineda E, Mérida-Rivas J, Martínez-López O, Sagot P, Vandame R, Cameron S (2017) Population genetics and geometric morphometrics of the Bombus ephippiatus species complex with implications for its use as a commercial pollinator. Conserv Genet 18:553–572

    Article  Google Scholar 

  • Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • Ellis J, Knight M, Darvill B, Goulson D (2006) Extremely low effective population sizes, genetic structuring and reduced genetic diversity in a threatened bumblebee species, Bombus sylvarum (Hymenoptera: Apidae). Mol Ecol 15:4375–4386

    Article  CAS  PubMed  Google Scholar 

  • Estoup A, Scholl A, Pouvreau A, Solignac M (1995) Monoandry and polyandry in bumblebees (Hymenoptera; Bombinae) as evidenced by highly variable microsatellites. Mol Ecol 4:89–93

    Article  CAS  PubMed  Google Scholar 

  • Estoup A, Solignac M, Cornuet J, Goudet J, Scholl A (1996) Genetic differentiation of continental and island populations of Bombus terrestris (Hymenoptera: Apidae) in Europe. Mol Ecol 5:19–31

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Falush D, Stephens M, Pritchard J (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    CAS  PubMed  PubMed Central  Google Scholar 

  • FAO (2016) FAOSTAT database collections. Food and Agriculture Organization of the United Nations, Rome

  • Fernandes C, Martins C, Ferreira K, del Lama M (2012) Gene variation, population differentiation, and sociogenetic structure of nests of Partamona seridoensis (Hymenoptera: Apidae, Meliponini). Biochem Genet 50:325–335

    Article  CAS  PubMed  Google Scholar 

  • Fitzpatrick BM (2009) Power and sample size for nested analysis of molecular variance. Mol Ecol 18:3961–3966

    Article  PubMed  Google Scholar 

  • Fitzpatrick Ú, Murray T, Paxton R, Breen J, Cotton D, Santorum V, Brown M (2007) Rarity and decline in bumblebees: a test of causes and correlates in the Irish fauna. Biol Conserv 136:185–194

    Article  Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, New York

    Book  Google Scholar 

  • Freitas B, Imperatriz-Fonseca VL, Medina L, de Matos Peixoto AD, Galetto L, Nates-Parra G, Quezada Euán JJG (2009) Diversity, threats and conservation of native bees in the Neotropics. Apidologie 40:332–346

    Article  Google Scholar 

  • Funk WC, Blouin MS, Corn PS, Maxell BA, Pilliod DS, Amish S et al (2005) Population structure of Columbia spotted frogs (Rana luteiventris) is strongly affected by the landscape. Mol Ecol 14:483–496

    Article  CAS  PubMed  Google Scholar 

  • Garibaldi L, Steffan-Dewenter I, Winfree R, Aizen MA, Bommarco R, Cunningham SA, Kremen C, Carvalheiro L et al (2013) Wild pollinators enhance fruit set of crops regardless of honey-bee abundance. Science 339:1608–1611

    Article  CAS  PubMed  Google Scholar 

  • Gerlach G, Jueterbock A, Kraemer P, Deppermann J, Harmand P (2010) Calculations of population differentiation based on GST and D: forget GST but not all of statistics! Mol Ecol 19:3845–3852

    Article  PubMed  Google Scholar 

  • Gilbert K, Andrew R, Bock D, Franklin M, Kane N, Moore J, et al (2012) Recommendations for utilizing and reporting population genetic analyses: the reproducibility of genetic clustering using the program. Mol Ecol 21(20):4925–4930

    Article  PubMed  Google Scholar 

  • Goulson D, Lye GC, Darvill B (2008) Decline and conservation of bumblebees. Annu Rev Entomol 53:191–208

    Article  CAS  PubMed  Google Scholar 

  • Greenleaf S, Williams NM, Rachael W, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153:589–596

    Article  PubMed  Google Scholar 

  • Guillot G, Leblois R, Coulon A, Frantz AC (2009) Statistical methods in spatial genetics. Mol Ecol 18:4734–4756

    Article  PubMed  Google Scholar 

  • Hansen MC, Potapov PV, Moore R, Hancher M, Turubanova SA, Tyukavina A, Thau D, Stehman SV et al (2013) Data available on-line from: high-resolution global maps of 21st-century forest cover change. Science 536:850–853

    Article  CAS  Google Scholar 

  • Harris S (1973) Comments on the application of the Holdridge system for classification of world life zones as applied to Costa Rica. Arct Antarct Alp Res 5:A187–A191

    Google Scholar 

  • Hulce D, Li X, Snyder-Leiby T (2011) GeneMarker Genotyping software: Tools to increase the statistical power of DNA fragment analysis. J Biomol Tech 22:S35–S36

    PubMed Central  Google Scholar 

  • Huth-Schwarz A, León A, Vandame R, Moritz R, Kraus F (2011) Mating frequency and genetic colony structure of the Neotropical bumblebee Bombus wilmattae (Hymenoptera: Apidae). Apidologie 42:519–525

    Article  Google Scholar 

  • Jaffé R, Castilla A, Pope N, Imperatriz-Fonseca VL, Metzger JP, Arias MC, Jha S (2016a) Landscape genetics of a tropical rescue pollinator. Conserv Genet 17:267–278

    Article  Google Scholar 

  • Jaffé R, Pope N, Acosta AL, Alves DA, Arias MC, De la Rúa P, Francisco FO, Giannini TC et al (2016b) Beekeeping practices and geographic distance not land-use, drive gene flow across tropical bees. Mol Ecol 25:5345–5358

    Article  PubMed  Google Scholar 

  • Jha S (2015) Contemporary human-altered landscapes and oceanic barriers reduce bumblebee gene flow. Mol Ecol 24:993–1006

    Article  CAS  PubMed  Google Scholar 

  • Jha S, Kremen C (2013) Urban land-use limits regional bumblebee gene flow. Mol Ecol 22:2483–2495

    Article  PubMed  Google Scholar 

  • Jones OR, Wang J (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resour 10:551–555

    Article  PubMed  Google Scholar 

  • Jost L (2009) D vs. GST: response to Heller and Siegismund (2009) and Ryman and Leimar (2009). Mol Ecol 18:2088–2091

    Article  Google Scholar 

  • Kavanaugh DH (1979) Investigations on present climatic refugia in North America through studies on the distributions of carabid beetles: concepts, methodology and prospectus. In: Erwin TL, Ball GE, Whitehead DR, Halpern AL (eds) Carabid Beetles. Springer, Dordrecht

    Google Scholar 

  • Landaverde-González P, Enríquez E, Ariza MA, Murray T, Paxton RJ, Husemann M (2017) Fragmentation in the clouds? The population genetics of the native bee Partamona bilineata (Hymenoptera: Apidae: Meliponini) in the cloud forests of Guatemala. Conserv Genet 18:631–643

    Article  Google Scholar 

  • López-Uribe M, Zamudio KR, Cardoso C, Danforth B (2014) Climate, physiological tolerance and sex-biased dispersal shape genetic structure of Neotropical orchid bees. Mol Ecol 23:1874–1890

    Article  PubMed  Google Scholar 

  • Lozier J, Strange JP, Stewart IJ, Cameron S (2011) Patterns of range-wide genetic variation in six North American bumblebee (Apidae: Bombus) species. Mol Ecol 20:4870–4888

    Article  PubMed  Google Scholar 

  • Lye GC, Lepais O, Goulson D (2011) Reconstructing demographic events from population genetic data: the introduction of bumblebees to New Zealand. Mol Ecol 20:2888–2900

    Article  CAS  PubMed  Google Scholar 

  • McRae BH, Dickson BG, Keitt TH, Shah VB (2008) Using circuit theory to model connectivity in ecology, evolution and conservation. Ecology 89:2712–2724

    Article  PubMed  Google Scholar 

  • Moradin L, Laverty TM, Kevan P (2000) Bumblebee (Hymenoptera: Apidae) activity and pollination levels in commercial tomato. J Econ Entomol 94:462–467

    Article  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara R, Simpson GL, Solymos P, Henry M, Stevens H, Helene W (2011) vegan: Community Ecology Package. R Package version 2.0-2 ed

  • Pan American Union (1902) Coffee: extensive information and statistics. Washington: Govt. Print. Off., p. 108. Accessed date 15th July 2017

  • Pennell M, Stansbury C, Waits L, Miller C (2013) Capwire: a R package for estimating population census size from non-invasive genetic sampling. Mol Ecol Resour 13:154–157

    Article  PubMed  Google Scholar 

  • Pinheiro J, Bates D, Sarkar D, and R-Core-Team (2016) nlme: linear and nonlinear mixed effects models. R package version 3:1–125

  • Piry S, Luikart G, Cornuet JM (1999) Computer note. BOTTLENECK: a computer program for detecting recent reductions in the effective size using allele frequency data. J Hered 90:502–503

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • QGIS Development Team (2009) QGIS Geographic Information System. Open Source Geospatial Foundation. http://qgis.osgeo.org

  • Quezada-Euán JJ, May-Itzá WdJ, Rincón M, de la Rúa P, Paxton RJ (2012) Genetic and phenotypic differentiation in endemic Scaptotrigona hellwegeri (Apidae: Meliponini): implications for the conservation of stingless bee populations in contrasting environments. Insect Conserv Divers 5:433–443

    Article  Google Scholar 

  • R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Article  Google Scholar 

  • Reber Funk C, Schmid-Hempel R, Schmid-Hempel P (2006) Microsatellite loci for Bombus spp. Mol Ecol Notes 6:83–86

    Article  CAS  Google Scholar 

  • Ryman N, Palm S (2006) POWSIM: a computer program for assessing statistical power when testing for genetic differentiation. Mol Ecol Notes 6:600–602

    Article  Google Scholar 

  • Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234

    Article  CAS  PubMed  Google Scholar 

  • Schuster J, Cano E, Cardona C (2000) Un método sencillo para priorizar la conservación de los bosques nubosos de Guatemala, usando Passalidae (coleoptera) como organismos indicadores. Acta Zool Mex 80:197–209

    Google Scholar 

  • Souza R, Del Lama M, Cervini M, Mortari N, Eltz T, Zimmermann Y, Bach C, Brosi BJ et al (2009) Conservation genetics of Neotropical pollinators revisited: microsatellite analysis suggests that diploid males are rare in orchid bees. Evolution 64:3318–3326

    Article  Google Scholar 

  • Torres-Ruiz A, Jones RW (2012) Comparison of the efficiency of the Bumblebees Bombus impatiens and Bombus ephippiatus (Hymenoptera: Apidae) as pollinators of tomato in greenhouses. J Econ Entomol 105:1871–1877

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Vásquez-Almazán CR, Rovito SM, Good DA, Wake DB (2009) A new species of Cryptotriton (Caudata: Plethodontidae) from Eastern Guatemala. Copeia 2:313–319

    Article  Google Scholar 

  • Veblen T (1978) Forest preservation in the western highlands of Guatemala. Geogr Rev 68:417–434

    Article  Google Scholar 

  • Véliz M (2014) Plantas Endémicas de Guatemala. Editorial Universitaria. USAC, Guatemala

    Google Scholar 

  • Walsh PS, Metzger DA, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–513

    CAS  PubMed  Google Scholar 

  • Weber B, Schaaf P, Valencia VA, Iriondo A, Ortega-Gutiérrez F (2006) Provenance ages of late Paleozoic sandstones (Santa Rosa formation) from the Maya block, SE Mexico. Implications on the tectonic evolution of western Pangea. Revista Mexicana de Ciencias Geológicas 23:262–276

    Google Scholar 

  • Williams P, Osborne JL (2009) Bumblebee vulnerability and conservation world-wide. Apidologie 40:367–387

    Article  Google Scholar 

  • Willmer P, Bataw A, Hughes J (1994) The superiority of bumblebees to honeybees as pollinators: insect visits to raspberry flowers. Ecol Entomol 19:271–284

    Article  Google Scholar 

  • Wilson G, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191

    PubMed  PubMed Central  Google Scholar 

  • Zimmermann Y, Schorkopf D, Moritz R, Pemberton RW, Quezada-Euán JJG, Eltz T (2011) Population genetic structure of orchid bees (Euglossini) in anthropogenically altered landscapes. Conserv Genet 12:1183–1194

    Article  Google Scholar 

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Acknowledgements

We thank to CONCYT-Guatemala (Grant: 32-2012), DIGI-USAC (Grant: 4.8.63.2.27), CONABIO-Mexico (Grant: JE016) and the Genetics Society (Heredity fieldwork grant) for the funding provided. We also thanks to Roberto Garnica, María Dardon, Carmen Yurrita and Mabel Vasquez for help with sampling. Thanks to Thomas Schmitt and one anonymous reviewer for valuable comments on the manuscript and to Silvio Erler and Antonella Soro for ideas and support. P.L.G was supported by a stipend of the German Academic Exchange Service (DAAD).

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Authors and Affiliations

  1. General Zoology, Institute of Biology, Martin-Luther-University Halle-Wittenberg, Hoher Weg 8, 06120, Halle (Saale), Germany

    Patricia Landaverde-González, Lucie M. Baltz & Robert J. Paxton

  2. Unidad de Investigación para el Conocimiento, Uso y Valoración de la Biodiversidad, Centro de Estudios Conservacionistas CECON, Universidad de San Carlos de Guatemala, Avenida La Reforma, 0-63, zona 10, 01010, Guatemala, Guatemala

    Patricia Landaverde-González & Natalia Escobedo-Kenefic

  3. Laboratorio de Entomología y Parasitología (LENAP), Facultad de Ciencias Químicas y Farmacia, Edificio T-10, Universidad de San Carlos de Guatemala, zona 12, 01012, Guatemala, Guatemala

    Patricia Landaverde-González

  4. Departamento Agricultura Sociedad y Ambiente, El Colegio de la Frontera Sur, Carretera Panamericana y Periférico Sur s/n, María Auxiliadora, 29290, San Cristóbal de Las Casas, Chiapas, Mexico

    Jorge Mérida

  5. Centrum für Naturkunde, University of Hamburg, Martin-Luther-King Platz 3, 20146, Hamburg, Germany

    Martin Husemann

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  1. Patricia Landaverde-González
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Landaverde-González, P., Baltz, L.M., Escobedo-Kenefic, N. et al. Recent low levels of differentiation in the native Bombus ephippiatus (Hymenoptera: Apidae) along two Neotropical mountain-ranges in Guatemala. Biodivers Conserv 27, 3513–3531 (2018). https://doi.org/10.1007/s10531-018-1612-0

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