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Fragmentation in the clouds? The population genetics of the native bee Partamona bilineata (Hymenoptera: Apidae: Meliponini) in the cloud forests of Guatemala

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Abstract

Habitat fragmentation and loss are important drivers of genetic differentiation, often leading to a decrease in genetic diversity. Yet, natural populations of tropical bees often show a lack of differentiation, even in fragmented landscapes, suggesting resilience to deal with unfavourable land use. It is not clear what leads to this lack of differentiation, but large population sizes, high rates of dispersal and stable demography likely play important roles. Here, we investigate the population genetic structure and infer the present and historic demography of the eusocial stingless bee Partamona bilineata from tropical montane cloud forests in Guatemala. We used microsatellites and mitochondrial DNA to test for genetic differentiation, to infer migration rates, and to evaluate the effects of landscape. We also used demographic modelling to trace population sizes over time. We found that six populations of P. bilineata exhibited only subtle differentiation, with the exception of one site at the edge of the cloud forest, which was clearly distinct from all others. Effective population sizes (number of colonies) appeared to be rather small (18 ± 6 colonies) compared to the original sample size (N = 51 ± 9), but stable over time, and inferred rates of gene flow were low; yet, no genetic bottleneck was detected. A statistical model including elevation was the best in explaining the observed pattern of differentiation. We find that P. bilineata does not exhibit strong genetic structure, making it a resilient species for provision of pollination services. But, at the same time, our data point to the potential vulnerability of this and similar species, as effective population sizes appear to be low and hence populations may be easily affected by future environmental change. As such, P. bilineata may be representative of many other tropical stingless bees, for which lack of differentiation has been invoked.

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References

  • Ayala R (1999) Revision de las abejas sin aguijon de Mexico (Hymenoptera: Apidae: Meliponini). Folia Entomol Mex 106:1

  • Biesmeijer JC, Roberts SPM, Reemer M, Ohlemüller R, Edwards M, Peeters T et al (2006) Parallel declines in pollinators and insect-pollinated plants in britain and the netherlands. Science 313:351–354

    Article  CAS  PubMed  Google Scholar 

  • Boff S, Soro A, & Paxton R (2014) Island isolation reduces genetic diversity and connectivity but does not significantly elevate diploid male production in a neotropical orchid bee. Conserv Genet 15:1123–1135

    Article  CAS  Google Scholar 

  • Brito RM (2005) Analise molecular e populacional de Partamona mulata (Moure in Camargo, 1980) e Partamona helleri (Friese, 1900) (Hymenoptera, Apidae, Meliponini). Universidade de Sao Paulo, Sao Paulo

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

    Article  Google Scholar 

  • Bruno C, Macchiavelli R, Balzarini M (2008) Non-parametric smoothing of multivariate genetic distances in the analysis of spatial population structure at fine scale. Theor Appl Genet 117:435–447

    Article  CAS  PubMed  Google Scholar 

  • Bubb P, May I, Miles L, & Sayer J (2004) Cloud forest Agenda. (pp. 36). Cambridge, UK: United Nations Environment Programme (UNEP) World Conservation Monitoring Centre.

  • CECON (2002) Plan Maestro 2000–2004 Biotopo Universitario “Mario Dary Rivera” para la Conservación del Quetzal. Centro de Estudios Conservacionistas (CECON) (p. 119). Guatemala: Universidad de San Carlos de Guatemala (USAC).

    Google Scholar 

  • Cornuet JM, Aries F (1980) Number of sex alleles in a sample of honey bee colonies. Apidologie 11:87–93

    Article  Google Scholar 

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

    Book  Google Scholar 

  • Darvill B, Knight M, Goulson D (2004) Use of genetic markers to quantify bumblebee foraging range and nest density. Oikos 107:471–478

    Article  Google Scholar 

  • De Palma A, Kuhlmann M, Roberts SPM, Potts SG, Börger L, Hudson L et al (2015) Ecological traits affect the sensitivity of bees to land-use pressures in European agricultural landscapes. J Appl Ecol 52:1567–1577

    Article  PubMed  PubMed Central  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 

  • Drummond A, Suchard M, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973

    Article  CAS  PubMed  PubMed Central  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 M, Lozier J, Hines H, Cameron S (2012) Geographical patterns of genetic divergence in the widespread Mesoamerican bumble bee Bombus ephippiatus (Hymenoptera: Apidae). Mol Phylogenet Evol 64:219–231

    Article  PubMed  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 

  • Enriquez E, Ayala R, Gonzalez V, & Núñez-Farfan J (2015) Alpha and beta diversity of bees and their pollination role on Cucurbita pepo L. (Cucurbitaceae) in the Guatemalan cloud forest. Pan-Pac Entomol 91:211–222.

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Folmer O, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertrebrates. Mol Mar Biol Biotechnol 3:294–299

    CAS  PubMed  Google Scholar 

  • Francisco F, Brito R, Arias M (2006) Alelle number and heterozigosity for microsatellite loci in different stingless bee species (Hymenoptera: Apidae, Meliponini). Neotrop Entomol 35:638–643

  • Frichot E, François O (2015) LEA: an R package for landscape and ecological association studies. Methods Ecol Evol 6:925–929

    Article  Google Scholar 

  • Funk W, Blouin M, Corn P, Maxell B, Pilliod D, 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 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 G( ST ) and D: forget G( ST ) but not all of statistics! Mol Ecol 19:3845–3852

    Article  PubMed  Google Scholar 

  • Green C, Franck P, Oldroyd B (2001) Characterization of microsatellite loci for Trigona carbonaria, a stingless bee endemic to Australia. Mol Ecol Notes 1:89–92

    Article  CAS  Google Scholar 

  • Habel JC, Rödder D, Lens L, Schmitt T (2013) The genetic signature of ecologically different grassland Lepidopterans. Biodivers Conserv 22:2401–2411

    Article  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  Google Scholar 

  • Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174

  • Hijmans RJ, & van Etten J (2012) raster: Geographic analysis and modeling with raster data. R package version 2.0–12. http://CRAN.R-project.org/package=raster.

  • Jaffé R, Pioker-Hara FC, dos Santos CF, Santiago LR, Alves DA, Kleinert AMP et al (2014) Monogamy in large bee societies: a stingless paradox. Naturwissenschaften 101:261–264

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Jaffé R, Pope N, Acosta AL, Alves DA, Arias MC, De la Rúa P 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 

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806

    Article  CAS  PubMed  Google Scholar 

  • Jha S, Kremen C (2013a) Resource diversity and landscape-level homogeneity drive native bee foraging. PNAS 110:555–558

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Johansson M, Primmer CR, Merila J (2007) Does habitat fragmentation reduce fitness and adaptability? A case study of the common frog (Rana temporaria). Mol Ecol 16:2693–2700

    Article  PubMed  Google Scholar 

  • Jones O and 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 

  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S et al (2012) Geneious. Bioinformatics 28:1647–1649

    Article  PubMed  PubMed Central  Google Scholar 

  • Klein AM, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, et al (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc 274:303–313. doi:10.1098/rspb.2006.3721

  • Kohlmann B, Cano E, Delgado L (2003) New species and records of Copris (Coleoptera: Scarabaeidae; Scarabaeinae) from Central America. Zootaxa 167:1–16

    Article  Google Scholar 

  • Laurance WF (1999) Reflections on the tropical deforestation crisis. Biol Cons 91:109–117

    Article  Google Scholar 

  • Laurance WF (2012) Averting biodiversity collapse in tropical forest protected areas. Nature 489:290–294

    Article  CAS  PubMed  Google Scholar 

  • Lopez-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 bumble bee (Apidae: Bombus) species. Mol Ecol 20:4870–4888

    Article  PubMed  Google Scholar 

  • Lynch M, Ritland K (1999) Estimation of pairwise relatedness with molecular markers. Genetics 152:1753–1766

    CAS  PubMed  PubMed Central  Google Scholar 

  • Manel S, Holderegger R (2013) Ten years of landscape genetics. Trends Ecol Evol 28:614–621

    Article  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 

  • Meléndez-Ramirez V, Magaña-Rueda S, Parra-Tabla V, Ayala R, Navarro J (2002) Diversity of native bee visitors of cucurbit crops (Cucurbitaceae) in Yucatán, México. J Insect Conserv 6:135

    Article  Google Scholar 

  • Mittermeier RA, Turner W, Larsen W, Brooks TM, Gascon C (2004) Chap. 1: Global biodiversity conservation: the critical role of hotspots. In: Mittermeier RA, Robles-Gil P, Hoffmann M, Pilgrim JD, Brooks TM, Mittermeier CG et al (eds) Hotspots revisited: earth’s biologically richest and most endangered ecoregions. CEMEX, Mexico City, pp 3–22

    Google Scholar 

  • Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Uppsala University, Evolutionary Biology Centre, Sweden

    Google Scholar 

  • Oliveira EJ, Freitas GS, Fonseca AS, Sousa AC, Campos T, Assis A et al (2009) Isolation and characterization of microsatellite markers from the stingless bee Nannotrigona testaceicornis. Conserv Genet Resour 1:97–99

    Article  Google Scholar 

  • Oosterhout CV, 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  Google Scholar 

  • Ornelas JF, Sosa V, Soltis DE, Daza JM, González C, Soltis PS et al (2013) Comparative phylogeographic analyses illustrate the complex evolutionary history of threatened cloud forest of Northern Mesoamerica. PLoS ONE 8:e56283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palmer KA, Oldroyd BP, Quesada-Euan JJG, Paxton RJ, May-Itza J (2002) Paternity frequency and maternity of males in some stingless bee species. Mol Ecol 11:2107–2113

    Article  CAS  PubMed  Google Scholar 

  • Paxton R, Weissschuh N, Quezada-Euán JJG (1999) Characterization of dinucleotide microsatellite loci for stingless bees. Mol Ecol 8:685–702

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peters JM, Queller DC, Imperatriz-Fonseca VL, Strassmann JE (1998) Microsatellite loci for stingless bees. Mol Ecol 7:783–792

    Article  Google Scholar 

  • Pinheiro J, Bates D, Sarkar D, & 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 

  • Quezada-Euán JJ, May-Itza WJ, Rinco M, de la Rua 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 (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rambaut A (2009) FigTree version 1.3.1 [computer program] http://tree.bio.ed.ac.uk.

  • Rambaut A & Drummond AJ (2009) Tracer version 1.5 [computer program] http://beast.bio.ed.ac.uk

  • 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 

  • RECOSMO (2007) Proyecto Región de Conservación y Desarrollo Sostenible Sarstún-Motagua - RECOSMO. Creación de una red ambientalista regional en Guatemala, Guatemala. pp. 214

    Google Scholar 

  • Rozas J, Sánchez-DelBarrio C, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496-2497

    Article  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 

  • Shirk A, Wallin D, Cushman S, Rice C, Warheit K (2010) Inferring landscape effects on gene flow: a new model selection framework. Mol Ecol 19:3603–3619

  • Slingenberg A, Braat L, van der Windt H, Rademaekers K, Eichler L, & Turner K (2009) Study on understanding the causes of biodiversity loss and the policy assessment framework. European Commission, Brussels. pp. 206

    Google Scholar 

  • Soro A, Quezada-Euán JJG, Theodorou P, Moritz R, Paxton R (2016) The population genetics of two orchid bees suggests high dispersal, low diploid male production and only an effect of island isolation in lowering genetic diversity. Conserv Genet. doi:10.1007/s10592-016-0912-8

    Google Scholar 

  • Souza R, Del Lama M, Cervini M, Mortari N, Eltz T, Zimmermann Y et al (2009) Conservation genetics of neotropical pollinators revisited: microsatellite analysisis suggests that diploid males are rare in orchid bees. Evolution Int J org Evolution 64:3318–3326

    Article  Google Scholar 

  • Suni S, Bronstein JL, Brosi BJ (2014) Spatio-temporal genetic structure of a tropical bee species suggests high dispersal over a fragmented landscape. Biotropica 46:202–209

    Article  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vanbergen A, Baude M, Biesmeijer JC, Britton NF, Brown MJ, Brown M, Bryden J et al (2013) Threats to an ecosystem service: pressures on pollinators. Front Ecol Environ 11:251–259

    Article  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 

  • Veliz M (2012) Diversidad florística de Guatemala. In: Tum C (ed) Biodiversidad de Guatemala vol:67(06–2008). PROBIOMA, Guatemala, pp 261–299

    Google Scholar 

  • Veliz M (2014) Plantas Endemicas de Guatemala. Guatemala: Editorial Universitaria. USAC, Guatemala

    Google Scholar 

  • Viard F, Franck P, Dubois MP, Estoup A, Jarne P (1998) Variation of microsatellite size homoplasy across electromorphs, loci, and populations in three invertebrate species. J Mol Evol 47:42–51

  • Villar-Anleu L (1994) Report from Guatemala: Guatemala profile. In: Vega A (ed) Conservation Corridors in the Central American Region: Proceedings of a Regional Conference sponsored by the Paseo Pantera Project Gainesville. Tropical Research and Development Inc, FL, pp 193–221

  • Vit P, Roubik DW, Pedro SRM (2013) Pot honey; a legacy of stingless bees New York. Springer, New York

    Google Scholar 

  • Walsh P, Metzger D, 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 

  • Waples RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Res 8:753–756

    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 

  • Winfree R, Aguilar R, Vázquez D, LeBuhn G, Aizen MA (2009) A meta-analisis of bees’ responses to anthropogenic disturbance. Ecology 90:2068–2076

    Article  PubMed  Google Scholar 

  • Woodward MR (1996) Trace element and technological analyses of obsidian artifacts from the Northern ridge of Lake Atitlan, Department of Solola, Guatemala. Texas A&M University, Texas, p 154

  • Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

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Acknowledgements

We thank CONCYT-Guatemala-(Grant: FODECYT 26-2012) and the Genetics Society (Heredity fieldwork grant) for financial support for field work. We also thank the Robin Moritz and the Molecular Ecology group at the MLU for assistance in the use of the MegaBACE. Our special thanks go to Dr. Ricardo Ayala for economic support for fieldwork and motivation. We further thank the personnel of Biotopo del Quetzal for essential help in the field. Thanks to Rodolfo Jaffé for suggestions and advice with regards to the IBR analysis and to Panagiotis Theodorou for statistical advice. We also thank the referees and editors for valuable comments that helped improve the manuscript. P.L.G was supported by a stipend from the German Academic Exchange Service (DAAD).

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Landaverde-González, P., Enríquez, E., Ariza, M.A. et al. 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 (2017). https://doi.org/10.1007/s10592-017-0950-x

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