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Conservation Genetics

, Volume 15, Issue 6, pp 1491–1502 | Cite as

Insights into the biodiversity of the Succulent Karoo hotspot of South Africa: the population genetics of a rare and endemic halictid bee, Patellapis doleritica

  • Belinda KahntEmail author
  • Antonella Soro
  • Michael Kuhlmann
  • Michael Gerth
  • Robert J. Paxton
Research Article

Abstract

Population genetic analyses are especially relevant for species considered threatened or highly endemic and for which other forms of biological information are lacking. Patellapis doleritica is a recently described communally nesting halictid bee of conservation concern because it is rare and endemic to the Succulent Karoo of South Africa. Moreover, its dispersal is considered to be restricted by its specialised nesting requirements and inclement weather conditions during its limited annual flight period, traits which may be common to other bee species of the region. We hypothesised that gene flow in P. doleritica was low, leading to marked genetic differentiation. Using 7 microsatellites, we investigated its mating and population genetic structure in 258 individuals (171 females and 87 males) from 7 populations spanning most of its known range. Deviation from Hardy–Weinberg equilibrium (FIS = + 0.254) suggested P. doleritica to be inbred, as in many other communal nesting bee species. Global FST (0.028) and global G′ST (0.216) revealed modest but significant differentiation between most populations, even across the very limited range of the species (ca. 25 km), with one genetically extreme outlier population. Despite inbreeding, we detected a surprisingly low frequency of diploid males (2 %). Patellapis doleritica nevertheless deserves special conservation attention since it is an endemic species with a low overall abundance and therefore possibly prone to environmental change and local extinction.

Keywords

Genetic differentiation Gene flow Halictidae Microsatellite Inbreeding Diploid male Triploid female 

Notes

Acknowledgments

We thank Martin Schlegel for laboratory support and both him and Christoph Bleidorn for stimulating discussion and suggestions. Our thanks also go to Kim Timmermann, who provided us with literature on P. doleritica, Annemarie Geißler, Panagiotis Theodorou and Petra Leibe for their technical assistance. We also appreciate the very helpful correspondence with Patrick Meirmans, Nils Ryman and Michael Matschiner over research reported in this paper. MK is much indebted to the farmers in the vicinity of Nieuwoudtville and the Hantam Botanical Garden who provided access to their land for this study and Northern Cape Nature Conservation Service for giving their permission to collect bees. Hergen Erhardt and Ulrike Gigengack enthusiastically helped to collect bees at various occasions for this and other projects in the wider Nieuwoudtville area.

Supplementary material

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References

  1. Allendorf FW, Luikart G (2006) Conservation and the genetics of populations. Wiley-Blackwell, OxfordGoogle Scholar
  2. Ayabe T, Hoshiba H, Ono M (2004) Cytological evidence for triploid males and females in the bumblebee, Bombus terrestris. Chromosome Res 12:215–223PubMedCrossRefGoogle Scholar
  3. Bartomeus I, Ascher JS, Gibbs J, Danforth BN, Wagner DL, Hedtke SM, Winfree R (2013) Historical changes in northeastern US bee pollinators related to shared ecological traits. Proc Natl Acad Sci 110:4656–4660PubMedCentralPubMedCrossRefGoogle Scholar
  4. Biesmeijer JC, Roberts SP, Reemer M, Ohlemueller R, Edwards M, Peeters T, Schaffers A, Potts SG, Kleukers R, Thomas CD, Settele J, Kunin WE (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313:351–354PubMedCrossRefGoogle Scholar
  5. Born J, Linder HP, Desmet P (2006) The greater cape floristic region. J Biogeogr 34:147–162CrossRefGoogle Scholar
  6. Brookfield JFY (1996) A simple new method for estimating null allele frequency from heterozygote deficiency. Mol Ecol 5:453–455PubMedCrossRefGoogle Scholar
  7. Brown MJ, Paxton RJ (2009) The conservation of bees: a global perspective. Apidologie 40:410–416CrossRefGoogle Scholar
  8. Carvalheiro LG, Kunin WE, Keil P, Aguirre-Gutiérrez J, Ellis WN, Fox R, Groom Q, Hennekens S, Van Landuy W, Maes D, Van de Meutter F, Michez D, Rasmont P, Ode B, Potts SG, Reemer M, Roberts SPM, Schaminée J, WallisDeVries MF, Biesmeijer JC (2013) Species richness declines and biotic homogenisation have slowed down for NW-European pollinators and plants. Ecol Lett 16:870–878PubMedCentralPubMedCrossRefGoogle Scholar
  9. Černá K, Straka J, Munclinger P (2013) Population structure of pioneer specialist solitary bee Andrena vaga (Hymenoptera: Andrenidae) in central Europe: the effect of habitat fragmentation or evolutionary history? Conserv Genet 14:875–883CrossRefGoogle Scholar
  10. Charlesworth D, Willis JH (2009) The genetics of inbreeding depression. Nat Rev Genet 10:783–796PubMedCrossRefGoogle Scholar
  11. Cook JM (1993) Sex determination in the Hymenoptera: a review of models and evidence. Heredity 71:421–435CrossRefGoogle Scholar
  12. Cook JM, Crozier RH (1995) Sex determination and population biology in the Hymenoptera. Trends Ecol Evol 10:281–286PubMedCrossRefGoogle Scholar
  13. Cowan DP, Stahlhut JK (2004) Functionally reproductive diploid and haploid males in an inbreeding hymenopteran with complementary sex determination. Proc Natl Acad Sci USA 101:10374–10379PubMedCentralPubMedCrossRefGoogle Scholar
  14. Darvill B, Ellis JS, Lye GC, Goulson D (2006) Population structure and inbreeding in a rare and declining bumblebee, Bombus muscorum, (Hymenoptera: Apidae). Mol Ecol 15:601–611PubMedCrossRefGoogle Scholar
  15. Davis ES, Murray TE, Fitzpatrick U, Brown MJF, Paxton RJ (2010) Landscape effects on extremely fragmented populations of a rare solitary bee, Colletes floralis. Mol Ecol 19:4922–4935PubMedCrossRefGoogle Scholar
  16. Dicks LV, Abrahams A, Atkinson J, Biesmeijer J, Bourn N, Brown C, Brown M, Carvell C, Connolly C, Cresswell J, Croft P, Darvill B, de Zylva P, Effingham P, Fountain M, Goggin A, Harding D, Harding T, Hartfield C, Heard MS, Heathcote R, Heaver D, Holland J, Howe M, Hughes B, Huxley T, Kunin WE, Little J, Mason C, Memmott J, Osborne J, Pankhurst T, Paxton RJ, Pocock M, Potts SG, Power E, Raine N, Ranelagh E, Roberts S, Saunders R, Smith K, Smith RM, Sutton P, Tilley L, Tinsley A, Tonhasca A, Vanbergen AJ, Webster S, Wilson A, Sutherland WJ (2013) Identifying key knowledge needs for evidence-based conservation of wild insect pollinators: a collaborative cross-sectoral exercise. Insect Conserv Divers 6:339–353CrossRefGoogle Scholar
  17. Dieringer D, Schlötterer C (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169CrossRefGoogle Scholar
  18. Doums C, Ruel C, Clémencet J, Fédérici P, Cournault L, Aron S (2013) Fertile diploid males in the ant Cataglyphis cursor: a potential cost of thelytoky? Behav Ecol Sociobiol 67:1983–1993CrossRefGoogle Scholar
  19. Eardley C, Gikungu M, Schwarz MP (2009) Bee conservation in sub-Saharan Africa and Madagascar: diversity, status and threats. Apidologie 40:355–366CrossRefGoogle Scholar
  20. Fitzpatrick Ú, Murray TE, Paxton RJ, Breen J, Cotton D, Santorum V, Brown MJ (2007) Rarity and decline in bumblebees: a test of causes and correlates in the Irish fauna. Biol Conserv 136:185–194CrossRefGoogle Scholar
  21. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299PubMedGoogle Scholar
  22. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  23. Gerth M, Geißler A, Bleidorn C (2011) Wolbachia infections in bees (Anthophila) and possible implications for DNA barcoding. Syst Biodivers 9:319–327CrossRefGoogle Scholar
  24. Google Corporation (2012) Google Earth 6.2. http://www.google.com/earth/download/ge/. Accessed July 2012
  25. Gustincich S, Manfioletti G, Del Sal G, Schneider C, Carninci P (1991) A fast method for high-quality genomic DNA extraction from whole human blood. Biotechniques 11:298–300PubMedGoogle Scholar
  26. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  27. Hebert PDN, Ratnasingham S, deWaard JR (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc R Soc Lond B 270:S596–S599CrossRefGoogle Scholar
  28. Hedrick PW (2000) Genetics of populations. Jones and Bartlett, SudburyGoogle Scholar
  29. Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638PubMedCrossRefGoogle Scholar
  30. Heimpel GE, de Boer JG (2008) Sex determination in the Hymenoptera. Annu Rev Entomol 53:209–230PubMedCrossRefGoogle Scholar
  31. Hoffman JI, Amos W (2005) Microsatellite genotyping errors: detection, approaches, common sources and consequences for paternal exclusion. Mol Ecol 14:599–612PubMedCrossRefGoogle Scholar
  32. Hutchison DW, Templeton AR (1999) Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution 53:1898–1914CrossRefGoogle Scholar
  33. Kuhlmann M (2008) Bees at the Cape-climate as a driving force of evolution? In: Schwenninger HR, Krogmann L, Mauss V (eds) Beiträge der Hymenopterologen-Tagung in Stuttgart (3.-5.10.2008). Deutsche Gesellschaft für allgemeine und angewandte Entomologie e.V., Müncheberg, pp 10–12Google Scholar
  34. Kuhlmann M (2009) Patterns of diversity, endemism and distribution of bees (Insecta: Hymenoptera: Anthophila) in southern Africa. S Afr J Bot 75:726–738CrossRefGoogle Scholar
  35. Kuhlmann M, Guo D, Veldtman R, Donaldson J (2012) Consequences of warming up a hotspot: Species range shifts within a centre of bee diversity. Divers Distrib. doi: 10.1111/j.1472-4642.2011.00877.x Google Scholar
  36. Linder PH, Johnson SD, Kuhlmann M, Matthee CA, Nyffeler R, Swartz ER (2010) Biotic diversity in the Southern African winter-rainfall region. Curr Opin Environ Sustain 2:109–116CrossRefGoogle Scholar
  37. Lombard AT, Hilton-Taylor C, Rebelo AG, Pressey RL, Cowling RM (1999) Reserve selection in the Succulent Karoo, South Africa: coping with high compositional turnover. Plant Ecol 142:35–55CrossRefGoogle Scholar
  38. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  39. Matschiner M, Salzburger W (2009) TANDEM: integrating automated allele binning into genetics and genomics workflows. Bioinformatics 25:1982–1983PubMedCrossRefGoogle Scholar
  40. Meirmans PG, Hedrick PW (2011) Assessing population structure: FST and related measures. Mol Ecol Resour 11:5–18PubMedCrossRefGoogle Scholar
  41. Meirmans PG, Van Tienderen PH (2004) Genotype and genodive: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794CrossRefGoogle Scholar
  42. Michener CD (1974) The social behaviour of the bees. A comparative study. The Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  43. Michener CD (2007) The bees of the world. The Johns Hopkins University Press, BaltimoreGoogle Scholar
  44. Murray TE, Fitzpatrick U, Brown MJ, Paxton RJ (2008) Cryptic species diversity in a widespread bumble bee complex revealed using mitochondrial DNA RFLPs. Conserv Genet 9:653–666CrossRefGoogle Scholar
  45. Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GA, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858PubMedCrossRefGoogle Scholar
  46. Pamilo P (1985) Effect of inbreeding on genetic relatedness. Hereditas 103:195–200PubMedCrossRefGoogle Scholar
  47. Paxton RJ (2005) Male mating behaviour and mating systems of bees: an overview. Apidologie 36:145–156CrossRefGoogle Scholar
  48. Paxton RJ, Tengö J (1996) Intranidal mating, emergence, and sex ratio in a communal bee Andrena jacobi Perkins 1921 (Hymenoptera: Andrenidae). J Insect Behav 9:421–440CrossRefGoogle Scholar
  49. Paxton RJ, Thorén PA, Tengö J, Estoup A, Pamilo P (1996) Mating structure and nestmate relatedness in a communal bee, Andrena jacobi (Hymenoptera, Andrenidae), using microsatellites. Mol Ecol 5:511–519PubMedCrossRefGoogle Scholar
  50. Paxton RJ, Kukuk PF, Tengö J (1999) Effects of familiarity and nestmate number on social interactions in two communal bees, Andrena scotica and Panurgus calcaratus (Hymenoptera, Andrenidae). Insect Soc 49:109–118CrossRefGoogle Scholar
  51. Paxton RJ, Thoren PA, Gyllenstrand N, Tengo J (2000) Microsatellite DNA analysis reveals low diploid male production in a communal bee with inbreeding. Biol J Linn Soc 69:483–502CrossRefGoogle Scholar
  52. Paxton RJ, Arévalo E, Field J (2003) Microsatellite loci fort the eusocial Lasioglossum malachurum and other sweat bees (Hymenoptera, Halictidae). Mol Ecol Notes 3:82–84CrossRefGoogle Scholar
  53. Peterson MA, Denno RF (1998) The influence of dispersal and diet breadth on patterns of genetic isolation by distance in phytophagous insects. Am Nat 152:428–446PubMedCrossRefGoogle Scholar
  54. Petit RJ, Deguilloux MF, Chat J, Grivet D, Garnier-Géré P, Vendramin GG (2005) Standardizing for microsatellite length in comparisons of genetic diversity. Mol Ecol 14:885–890PubMedCrossRefGoogle Scholar
  55. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353PubMedCrossRefGoogle Scholar
  56. Procheş S, Cowling RM, du Preez DR (2005) Patterns of geophyte diversity and storage organ size in the winter-rainfall region of southern Africa. Divers Distrib 11:101–109CrossRefGoogle Scholar
  57. Ratnasingham S, Hebert PD (2007) Bold: the barcode of life data system. Mol Ecol Notes 7:355–364. http://www.barcodinglife.org. Accessed July 2012
  58. Rice WR (1990) A consensus combined p-value and the family-wide significance of component tests Biometrics 46:303–308Google Scholar
  59. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228PubMedCentralPubMedGoogle Scholar
  60. Rousset F (2008) Genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106PubMedCrossRefGoogle Scholar
  61. Ryman N, Palm S (2006) POWSIM: a computer program for assessing statistical power when testing for genetic differentiation. Mol Ecol Notes 6:600–602CrossRefGoogle Scholar
  62. Schwarz MP, Richards MH, Danforth BN (2007) Changing paradigms in insect social evolution: insights from halictine and allodapine bees. Annu Rev Entomol 52:127–150PubMedCrossRefGoogle Scholar
  63. Sheffield CS, Hebert PDN, Kevan PG, Packer L (2009) DNA barcoding a regional bee (Hymenoptera: Apoidea) fauna and its potential for ecological studies. Mol Ecol Resour 9:196–207PubMedCrossRefGoogle Scholar
  64. Song H, Buhay JE, Whiting MF, Crandall KA (2008) Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proc Natl Acad Sci USA 105:13486–13491PubMedCentralPubMedCrossRefGoogle Scholar
  65. Soro A, Paxton RJ (2009) Characterization of 14 polymorphic microsatellite loci for the facultatively eusocial sweat bee Halictus rubicundus (Hymenoptera, Halictidae) and their variability in related species. Mol Ecol Notes 9:150–152CrossRefGoogle Scholar
  66. Soro A, Ayasse M, Zobel MU, Paxton RJ (2009) Complex sociogenetic organization and the origin of unrelated workers in a eusocial sweat bee, Lasioglossum malachurum. Insectes Soc 56:55–63CrossRefGoogle Scholar
  67. Soucy SL, Danforth BN (2002) Phylogeography of the socially polymorphic sweat bee Halictus rubicundus (Hymenoptera: Halictidae). Evolution 56:330–341PubMedCrossRefGoogle Scholar
  68. Spielman D, Brook BW, Frankham R (2004) Most species are not driven to extinction before genetic factors impact them. Proc Natl Acad Sci USA 101:15261–15264PubMedCentralPubMedCrossRefGoogle Scholar
  69. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molar evolutionary genetics analysis using likelihood, distance, and parsimony methods. Mol Biol Evol 28:2731–2739PubMedCentralPubMedCrossRefGoogle Scholar
  70. Timmermann K (2008) The bee genus Patellapis Friese: taxonomic revision of three subgenera and first ecological investigations. Dissertation, University of MünsterGoogle Scholar
  71. Timmermann K, Kuhlmann M (2008) The biology of a Patellapis (s. str.) species (Hymenoptera: Apoides: Halictidae): sociality described for the first time in this bee genus. Apidologie 39:189–197CrossRefGoogle Scholar
  72. Timmermann K, Kuhlmann M (2009) Taxonomic revision of the African bee subgenera Patellapis, Chaetalictus and Lomatalictus (Hymenoptera: Halictidae, genus Patellapis Friese 1909). Zootaxa 2099:1–188Google Scholar
  73. Ulrich Y, Perrin N, Chapuisat M (2009) Flexible social organization and high incidence of drifting in the sweat bee, Halictus scabiosae. Mol Ecol 18:1791–1800PubMedCrossRefGoogle Scholar
  74. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley PF (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  75. van Wilgenburg E, Driessen G, Beukeboom L (2006) Single locus complementary sex determination in Hymenoptera: an ‘unintelligent’ design? Front Zool 3:1–15PubMedCentralPubMedCrossRefGoogle Scholar
  76. Vanbergen AJ (2013) Insect pollinators initiative. Threats to an ecosystem service: pressures on pollinators. Front Ecol Environ 11:251–259CrossRefGoogle Scholar
  77. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  78. Zayed A (2009) Bee genetics and conservation. Apidologie 40:237–262CrossRefGoogle Scholar
  79. Zayed A, Packer L (2005) Complementary sex determination substantially increases extinction proneness of haplodiploid populations. Proc Natl Acad Sci USA 102:10742–10746PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Belinda Kahnt
    • 1
    • 2
    Email author
  • Antonella Soro
    • 2
  • Michael Kuhlmann
    • 3
  • Michael Gerth
    • 1
  • Robert J. Paxton
    • 2
    • 4
  1. 1.Molecular Evolution & Systematics of Animals, Institute of BiologyUniversity of LeipzigLeipzigGermany
  2. 2.General Zoology, Institute of BiologyMartin-Luther-University Halle-WittenbergHalleGermany
  3. 3.Department of Life SciencesThe Natural History MuseumLondonUK
  4. 4.German Centre for Integrative Biodiversity Research (iDiv), Halle-Jena-LeipzigLeipzigGermany

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