Skip to main content
SpringerLink
Log in

Analysis of a contact area between two distinct evolutionary honeybee units: an ecological perspective

  • ORIGINAL PAPER
  • Published:
Journal of Insect Conservation Aims and scope Submit manuscript

Abstract

Determining the relationships between environmental variables and genetic diversity is critical to understand the processes that drive evolution in species-contact areas. We employed a combination of modeling approaches and multivariate statistical analyses to analyze mtDNA diversity in a hybrid zone between two evolutionary lineages of honeybees in order to interpret the microevolutionary processes that led to the observed spatial pattern of diversity. The model located the west European honeybee lineage mainly across temperate areas characterized by mild winters and high water availability throughout the year, whereas the African lineage was mainly associated with warmer and drier areas. Selection could be playing an important role in shaping the life history evolution, particularly affecting the mitochondria, and also resulting in hitchhiking effects on particular regions of the mitochondrial genome.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Angers B, Magnan P, Plantes M, Bernatchez L (1999) Canonical correspondence analysis for estimating spatial and environmental effects on microsatellite gene diversity in brook charr (Salvelinus fontinalis). Mol Ecol 8:1053–1403

    Article  Google Scholar 

  • Arias M, Rinderer T, Sheppard W (2006) Further characterization of honey bees from the Iberian Peninsula by allozyme, morphometric and mtDNA haplotype analyses. J Apic Res 45(4):188–196

    Article  CAS  Google Scholar 

  • Ballard W, Kreitman M (1995) Is mitochondrial DNA a strictly neutral marker? Trends Ecol Evol 10:485–488

    Article  PubMed  CAS  Google Scholar 

  • Barrett R, Schluter D (2007) Adaptation from standing genetic variation. Trends Ecol Evol 23:38–44

    Article  PubMed  Google Scholar 

  • Boyce M, Vernier P, Nielsen S, Schmiegelow F (2002) Evaluating resource selection functions. Ecol Model 157:281–300

    Article  Google Scholar 

  • Cánovas F, De la Rúa P, Serrano J, Galián J (2002) Variabilidad del ADN mitocondrial en poblaciones de Apis mellifera iberica de Galicia (NW España). Arch Zootec 51:441–448

    Google Scholar 

  • Cánovas F, De la Rúa P, Galián J, Serrano J (2008) Geographical patterns of mitochondrial DNA variation in Apis mellifera iberiensis (Hymenoptera: Apidae). J Zool Syst Evol Res 46:24–30

    Google Scholar 

  • Cánovas F, De la Rúa P, Serrano J, Galián J (2011) Microsatellite variability reveals beekeeping influences on Iberian honeybee populations. Apidologie 42:235–251

    Article  Google Scholar 

  • Chávez-Galarza J, Henriques D, Johnston JS, Azevedo JC, Patton JC, Muñoz I, De la Rúa P, Pinto MA (2013) Signatures of selection in the Iberian honey bee (Apis mellifera iberiensis) revealed by a genome scan analysis of single nucleotide polymorphisms. Mol Ecol 22(23):5890–5907

    Article  PubMed  Google Scholar 

  • Cheesel D (1992) The ade4 package-I: one-table methods. R News 4:5–10

    Google Scholar 

  • Collins WD, Bitz CM, Blackmon ML, Bonan GB, Bretherton CS, Carton JA, Chang P, Doney SC, Hack JJ, Henderson TB, Kiehl JT, Large WG, McKenna DS, Santer BD, Smith RD (2006) The community climate system model version 3 (CCSM3). J Clim 19:2122–2143

    Article  Google Scholar 

  • Danforth B (2007) Bees. Curr Biol 17:156–161

    Article  Google Scholar 

  • De la Rúa P, Galián J, Serrano J (1999) Variabilidad del ADN mitocondrial en poblaciones de abejas de la miel (Apis mellifera L.) de la Región de Murcia. Invest Agric Prod San Anim 14:41–49

    Google Scholar 

  • De la Rúa P, Galián J, Serrano J, Moritz RFA (2001) Molecular characterization and population structure of the honeybees from the Balearic Islands (Spain). Apidologie 32:417–427

    Article  Google Scholar 

  • De la Rúa P, Jiménez Y, Galián J, Serrano J (2004) Evaluation of the biodiversity of honey bee (Apis mellifera) populations from eastern Spain. J Apic Res 43:162–166

    Google Scholar 

  • De la Rúa P, Hernández-García R, Jiménez Y, Galián J, Serrano J (2005a) Biodiversity of Apis mellifera iberica (Hymenoptera: Apidae) from northeastern Spain assessed by mitochondrial analysis. Insect Syst Evol 36:21–28

    Article  Google Scholar 

  • De la Rúa P, Fuchs S, Serrano J (2005b) Biogeography of European honey bees. In: Lodesani M, Costa C (eds) Beekeeping and conserving biodiversity of honeybees. Sustainable bee breeding, theoretical and practical guide. Northern Bee Books, Hebden Bridge, pp 15–52

    Google Scholar 

  • Dowling D, Friberg U, Lindell J (2008) Evolutionary implications of non-neutral mitochondrial genetic variation. Trends Ecol Evol 23:546–554

    Article  PubMed  Google Scholar 

  • Elekonich M, Roberts S (2005) Honey bees as a model for understanding mechanisms of life history transitions. Comp Biochem Physiol A 141:362–371

    Article  Google Scholar 

  • Elith J, Phillips S, Hastie T, Dudík M, Chee Y, Yates CJ (2011) A statistical explanation of MaxEnt for ecologists. Divers Distrib 17(1):43–57

    Article  Google Scholar 

  • El-Niweiri M, Moritz R (2011) Mating in the rain? Climatic variance for polyandry in the honeybee (Apis mellifera jemenitica). Pop Ecol 53(3):421–427

    Article  Google Scholar 

  • Engel MS (1999) The taxonomy of recent and fossil honey bees (Hymenoptera: Apidae; Apis). J Hymenopt Res 8(2):165–196

    Google Scholar 

  • Fielding A, Bell J (1997) A review of methods for the assessment of prediction errors in conservation presence/absence models. Environ Conserv 24:38–49

    Article  Google Scholar 

  • Franck P, Garnery L, Solignac M, Cornuet J (1998) The origin of West European subspecies of honeybees (Apis mellifera): new insights from microsatellite mitochondrial data. Evolution 52(4):1119–1134

    Article  CAS  Google Scholar 

  • Franck P, Garnery L, Loiseau A, Hepburn HR, Solignac M, Cornuet JM (2001) Genetic diversity of the honeybee in Africa: microsatellite mitochondrial data. Heredity 86:420–430

    Article  PubMed  CAS  Google Scholar 

  • Garnery L, Solignac M, Celebrano G, Cornuet JM (1993) A simple test using restricted PCR-amplified mitochondrial DNA to study the genetic structures of Apis mellifera L. Experientia 49:1016–1021

    Article  CAS  Google Scholar 

  • Garnery L, Frank P, Baudry E, Vautrin D, Cornuet J, Solignac M (1998a) Genetic diversity of the west European honeybee (Apis mellifera mellifera and A. m. iberica). I. Mitochondrial DNA. Genet Sel Evol 30(1):31–47

    Article  Google Scholar 

  • Garnery L, Frank P, Baudry E, Vautrin D, Cornuet J, Solignac M (1998b) Genetic diversity of the west European honeybee (Apis mellifera mellifera A. m. iberica). II. Microsatellite loci. Genet Sel Evol 30(1):49–74

    Article  Google Scholar 

  • González-Trueba J, Martín-Moreno R, de Pisón EM, Serrano E (2008) ‘Little Ice Age’ glaciation and current glaciers in the Iberian Peninsula. Holocene 18:551–568

    Article  Google Scholar 

  • Gordo O, Sanz J (2005) Phenology and climate change: a long- term study in a Mediterranean locality. Oecologia 146:484–495

    Article  PubMed  Google Scholar 

  • Gordo O, Sanz J (2006) Temporal trends in phenology of the honey bee Apis mellifera (L.) and the small white Pieris rapae (L.) in the Iberian Peninsula (1952–2004). Ecol Entomol 31:261–268

    Article  Google Scholar 

  • GRASS Development Team (2008) Geographic resources analysis support system (GRASS GIS) software. Open source geospatial foundation. http://grass.osgeo.org

  • Hanotte O, Bradley D, Ochieng J, Verjee Y, Hill E, Rege EO (2002) African pastoralism: genetic imprints of origins and migrations. Science 296:336–339

    Article  PubMed  CAS  Google Scholar 

  • Hastie T, Tibshirani R (1990) Generalized additive models. Chapman and Hall, London

    Google Scholar 

  • Hasumi H, Emori S (2004) K-1 coupled GCM (MIROC) description. Center for Climate System Research, University of Tokyo, Tokyo p 34

  • Hickling R, Roy D, Hill J, Fox R, Thomas C (2006) The distributions of a wide range of taxonomic groups are expanding polewards. Glob Chang Biol 12:450–455

    Article  Google Scholar 

  • Hijmans R, Cameron S, Parra L, Jones P, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978

    Article  Google Scholar 

  • Hirzel A, Le Lay G, Helfer V, Randin C, Guisan A (2006) Evaluating the ability of habitat suitability. Ecol Model 199:142–152

    Article  Google Scholar 

  • Jombart T, Pontier D, Dufour A (2009) Genetic markers in the playground of multivariate analysis. Heredity 102(4):330–341

    Article  PubMed  CAS  Google Scholar 

  • Kindt R, Coe R (2005) Tree diversity analysis: a manual and software for common statistical methods for ecological and biodiversity studies. World Agroforestry Centre, Nairobi

    Google Scholar 

  • Kovac H, Stabentheiner A, Schmaranzer S (2010) Thermoregulation of water foraging honeybees-balancing of endothermic activity with radiative heat gain and functional requirements. J Insect Physiol 56(12):1834–1845

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Le Conte Y, Navajas M (2008) Climate change: impact on honey bee populations and diseases economically valuable species. Rev Sci Technol 27(2):499–510

    Google Scholar 

  • Lehmann A, Overton JM, Leathwik JR (2002) GRASP: generalized regression analysis and spatial predictions. Ecol Model 157:187–205

    Google Scholar 

  • Lodesani M, Costa C (2005) Beekeeping and conserving biodiversity of honeybees. Sustainable bee breeding, theoretical and practical guide. Northern Bee Books, Hebden Bridge

    Google Scholar 

  • Markham C (1970) Seasonality of precipitation in the United States. Ann Assoc Amer Geograph 60:593–597

    Article  Google Scholar 

  • Miguel I, Iriondo M, Garnery L, Sheppard WS, Estonba A (2007) Gene flow within the M evolutionary lineage of Apis mellifera: role of the Pyrenees, isolation by distance and post-glacial recolonization routes in the Western Europe. Apidologie 38:141–155

    Article  CAS  Google Scholar 

  • Miguel I, Baylac M, Iriondo M, Manzano C, Garnery L, Estonba A (2011) Both geometric morphometric and microsatellite data consistently support the differentiation of the Apis mellifera M evolutionary branch. Apidologie 42(2):150–161

    Article  Google Scholar 

  • Pinto MA, Henriques D, Neto M, Guedes H, Muñoz I, Azevedo J, de la Rúa P (2013) Maternal diversity patterns of Ibero-Atlantic populations reveal further complexity of Iberian honeybees. Apidologie 44:430–439

    Article  Google Scholar 

  • R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/. ISBN 3-900051-07-0

  • Ruttner F (1988) Biogeography and taxonomy of honeybees. Springer, Berlin

    Book  Google Scholar 

  • Ruttner F, Tassencourt L, Louveaux J (1978) Biometrical-statistical analysis of the geographic variability of Apis mellifera L. Apidologie 9(4):363–381

    Article  Google Scholar 

  • Schütt B (2005) Late quaternary environmental change on the Iberian Peninsula. Erde 136:3–14

    Google Scholar 

  • Segurado P, Araujo MB (2004) An evaluation of methods for modelling species distributions. J Biogeogr 31:1555–1568

    Article  Google Scholar 

  • Smith D, Glenn T (1995) Allozyme polymorphisms in Spanish honeybees (Apis mellifera iberica). J Hered 86:12–16

    PubMed  CAS  Google Scholar 

  • Smith D, Palopoli M, Taylor B, Garnery L, Cornuet J, Solignac M, Brown WM (1991) Geographical overlap of two mitochondrial genomes in Spanish honeybees (Apis mellifera iberica). J Hered 82:96–100

    PubMed  CAS  Google Scholar 

  • Thomas C, Bodsworth E, Wilson R, Simmons A, Davies Z, Conradt L (2001) Ecological and evolutionary processes at expanding range margins. Nature 411:577–581

    Article  PubMed  CAS  Google Scholar 

  • Venables W, Ripley B (2004) Modern applied statistics with S. Springer, New York

    Google Scholar 

  • Whitfield C, Behura S, Berlocher S, Clark A (2006) Thrice out of Africa : ancient and recent expansions of the honey bee, Apis mellifera. Science 314:642–645

    Article  PubMed  CAS  Google Scholar 

  • Wood S (2006) Generalized additive models: an introduction with R. Chapman and Hall, London

    Google Scholar 

  • Wood S, Augustin N (2002) GAMs with integrated model selection using penalized regression splines and applications to environmental modelling. Ecol Model 157:157–177

    Article  Google Scholar 

  • Zayed A, Whitfield C (2008) A genome-wide signature of positive selection in ancient and recent invasive expansions of the honey bee Apis mellifera. Proc Natl Acad Sci USA 105:3421–3426

    Article  PubMed  CAS  PubMed Central  Google Scholar 

Download references

Acknowledgments

We thank all the bee-keepers and associations (particularly Coordinadora de Organizaciones de Agricultores y Ganaderos, COAG) that generously contributed samples and their time. We thank O. Rodríguez, J. Ornia, E. Muñiz and U. Mediel. Thanks to R. Angus, who helped us improve the manuscript with their comments and suggestions during the revision process. This work was supported by projects RZ00-013 (Spanish National Institute of Agricultural Investigation, INIA) and EVK2 2000-00628 (BABE, V European Union Framework). F. Cánovas is supported by a post-doctoral fellowship from the FCT (Fundacão para Ciência e Tecnologia, Portugal). This study was conducted entirely using open source software.

Author information

Authors and Affiliations

  1. Centro de Ciências do Mar do Algarve, CCMAR, Campus de Gambelas, 8005-139, Faro, Portugal

    Fernando Cánovas

  2. Department of Zoology and Physic Anthropology, University of Murcia, 30100, Espinardo, Murcia, Spain

    Pilar De la Rúa, José Serrano & José Galián

Authors
  1. Fernando Cánovas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pilar De la Rúa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. José Serrano
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. José Galián
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fernando Cánovas.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLS 78 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cánovas, F., De la Rúa, P., Serrano, J. et al. Analysis of a contact area between two distinct evolutionary honeybee units: an ecological perspective. J Insect Conserv 18, 927–937 (2014). https://doi.org/10.1007/s10841-014-9701-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10841-014-9701-1

Keywords

Search

Navigation