Abstract
Limited natal dispersal can lead to marked spatial genetic structure, which potentially provides benefits to individuals through kin cooperation but also costs through kin competition. We often lack information on the spatial genetic structure of natural populations at a fine enough spatial scale to understand whether relatives nest close enough to interact. The primitively eusocial halictid bee Lasioglossum malachurum forms conspicuous nesting aggregations comprising up to thousands of nests. We test for spatial genetic structure in this species by genotyping one worker per nest from four discrete nesting aggregations around Tübingen, Germany, at 14 microsatellite loci. Genotypes were spatially autocorrelated at a very fine scale (<60 cm) within an aggregation for three of four aggregations, though genetic differentiation was non-existent or limited at coarser spatial scales between local or distant aggregations, respectively. Our results suggest that L. malachurum gynes often exhibit extremely limited natal dispersal, possibly because of the benefits of philopatry and kin cooperation or the avoidance of dispersal costs.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alizon S, Taylor P (2008) Empty sites can promote altruistic behavior. Evol Int J Org Evol 62(6):1335–1344. doi:10.1111/j.1558-5646.2008.00369.x
Bitume EV, Bonte D, Ronce O, Bach F, Flaven E, Olivieri I, Nieberding CM (2013) Density and genetic relatedness increase dispersal distance in a subsocial organism. Ecol lett 16(4):430–437. doi:10.1111/ele.12057
Bonte D, van Dyck H, Bullock JM, Coulon A, Delgado M, Gibbs M, Lehouck V, Matthysen E, Mustin K, Saastamoinen M, Schtickzelle N, Stevens VM, Vandewoestijne S, Baguette M, Barton K, Benton TG, Chaput-Bardy A, Clobert J, Dytham C, Hovestadt T, Meier CM, Palmer SCF, Turlure C, Travis JMJ (2012) Costs of dispersal. Biol Rev Camb Philos Soc 87(2):290–312. doi:10.1111/j.1469-185X.2011.00201.x
Busch JD, Waser PM, DeWoody JA (2009) The influence of density and sex on patterns of fine-scale genetic structure. Evol Int J org Evol 63(9):2302–2314. doi:10.1111/j.1558-5646.2009.00721.x
Clobert J, Le Galliard JF, Cote J, Meylan S, Massot M (2009) Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations. Ecol lett 12(3):197–209. doi:10.1111/j.1461-0248.2008.01267.x
Comins HN, Hamilton WD, May RM (1980) Evolutionarily stable dispersal strategies. J Theor Biol 82(2):205–230. doi:10.1016/0022-5193(80)90099-5
Crozier RH, Pamilo P, Crozier YC (1984) Relatedness and microgeographic genetic variation in Rhytidoponera mayri, an Australian arid-zone ant. Behav Ecol Sociobiol 15(2):143–150. doi:10.1007/BF00299382
Dieringer D, Schlötterer C (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3(1):167–169. doi:10.1046/j.1471-8286.2003.00351.x
Dobson FS (1982) Competition for mates and predominant juvenile male dispersal in mammals. Anim Behav 30(4):1183–1192. doi:10.1016/S0003-3472(82)80209-1
Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22(4):1–20
Gandon S (1999) Kin competition, the cost of inbreeding and the evolution of dispersal. J Theor Biol 200(4):345–364. doi:10.1006/jtbi.1999.0994
Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28(4):1140–1162. doi:10.1016/S0003-3472(80)80103-5
Hamilton WD (1971) Geometry for the selfish herd. J Theor Biol 31(2):295–311. doi:10.1016/0022-5193(71)90189-5
Hartl DL, Clark AG (2007) Principles of population genetics, 4th edn. Sinauer Associates, Sunderland
Johnstone RA, Cant MA (2008) Sex differences in dispersal and the evolution of helping and harming. Am Nat 172(3):318–330. doi:10.1086/589899
Kaitala V, Smith BH, Getz WM (1990) Nesting strategies of primitively eusocial bees: a model of nest usurpation during the solitary state of the nesting cycle. J Theor Biol 144(4):445–471. doi:10.1016/S0022-5193(05)80086-4
Kapranas A, Maher AMD, Griffin CT (2016) Higher relatedness mitigates mortality in a nematode with lethal male fighting. J Evol Biol 29(2):344–351. doi:10.1111/jeb.12786
Klahn JE (1979) Philopatric and nonphilopatric foundress associations in the social wasp Polistes fuscatus. Behav Ecol Sociobiol 5(4):417–424. doi:10.1007/BF00292528
Knerer G (1992) The biology and social behaviour of Evylaeus malachurus (K.) (Hymenoptera; Halictidae) in different climatic regions of Europe. Zool Jb Syst 119:261–290
Konovalov DA, Manning C, Henshaw MT (2004) Kingroup: a program for pedigree relationship reconstruction and kin group assignments using genetic markers. Mol Ecol Notes 4(4):779–782. doi:10.1111/j.1471-8286.2004.00796.x
Kukuk PF, Decelles PC (1986) Behavioral evidence for population-structure in Lasioglossum (Dialictus) zephyrum female dispersion patterns. Behav Ecol Sociobiol 19(4):233–239
López-Uribe MM, Morreale SJ, Santiago CK, Danforth BN (2015) Nest suitability, fine-scale population structure and male-mediated dispersal of a solitary ground nesting bee in an urban landscape. PLoS One 10(5):e0125719. doi:10.1371/journal.pone.0125719
Michener CD, Lange RB, Bigarella JJ, Salamuni R (1958) Factors influencing the distribution of bees’ nests in earth banks. Ecology 39(2):207–217. doi:10.2307/1931865
Moore J, Ali R (1984) Are dispersal and inbreeding avoidance related? Anim Behav 32(1):94–112. doi:10.1016/S0003-3472(84)80328-0
Packer L (1983) The nesting biology and social organisation of Lasioglossum (evylaeus) laticeps (Hymenoptera, Halictidae) in England. Insect Soc 30(4):367–375. doi:10.1007/BF02223968
Packer L, Knerer G (1985) Social evolution and its correlates in bees of the subgenus Evylaeus (Hymenoptera; Halictidae). Behav Ecol Sociobiol 17(2):143–149
Packer L, Knerer G (1986) An analysis of variation in the nest architecture of Halictus ligatus in Ontario. Insect Soc 33(2):190–205. doi:10.1007/BF02224597
Pamminger T, Foitzik S, Metzler D, Pennings PS (2014) Oh sister, where art thou? Spatial population structure and the evolution of an altruistic defence trait. J Evol Biol 27(11):2443–2456. doi:10.1111/jeb.12496
Paxton RJ, Arevalo E, Field J (2003) Microsatellite loci for the eusocial Lasioglossum malachurum and other sweat bees (Hymenoptera, Halictidae). Mol Ecol Notes 3(1):82–84. doi:10.1046/j.1471-8286.2003.00357.x
Paxton RJ, Ayasse M, Field J, Soro A (2002) Complex sociogenetic organization and reproductive skew in a primitively eusocial sweat bee, Lasioglossum malachurum, as revealed by microsatellites. Mol Ecol 11(11):2405–2416
Paxton RJ, Thoren PA, Tengo J, Estoup A, Pamilo P (1996) Mating structure and nestmate relatedness in a communal bee, Andrena jacobi (Hymenoptera, Andrenidae), using microsatellites. Mol Ecol 5(4):511–519
Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6(1):288–295. doi:10.1111/j.1471-8286.2005.01155.x
Perrin N, Mazalov V (2000) Local competition, inbreeding, and the evolution of sex-biased dispersal. Am Nat 155(1):116–127. doi:10.1086/303296
Polidori C, Rubichi A, Barbieri V, Trombino L, Donegana M (2010) Floral resources and nesting requirements of the ground-nesting social bee, Lasioglossum malachurum (Hymenoptera: Halictidae), in a Mediterranean semiagricultural landscape. Psyche J Entomol 2010(6745):1–11. doi:10.1155/2010/851947
Potts SG, Willmer PA (1997) Abiotic and biotic factors influencing nest-site selection by Halictus rubicundus, a ground-nesting halictine bee. Ecol Entomol 22(3):319–328. doi:10.1046/j.1365-2311.1997.00071.x
Potts SG, Willmer PA (1998) Compact housing in built-up areas: spatial patterning of nests in aggregations of a ground-nesting bee. Ecol Entomol 23(4):427–432. doi:10.1046/j.1365-2311.1998.00160.x
Pusey AE, Wolf M (1996) Inbreeding avoidance in animals. Trends Ecol Evol 11(5):201–206. doi:10.1016/0169-5347(96)10028-8
Pusey AE (1987) Sex-biased dispersal and inbreeding avoidance in birds and mammals. Trends Ecol Evol 2(10):295–299. doi:10.1016/0169-5347(87)90081-4
QGIS Development Team (2009) QGIS Geographic Information System. Open Source Geospatial Foundation. http://qgis.osgeo.org. Accessed 2014
Queller DC, Goodnight KF (1989) Estimating relatedness using genetic-markers. Evol Int J org Evol 43(2):258–275
R Development Core Team (2008). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86(3):248
Rice WR (1989) Analyzing tables of statistical tests. Evol Int J Org Evol 43(1):223. doi:10.2307/2409177
Richards MH (2000) Evidence for geographic variation in colony social organization in an obligately social sweat bee, Lasioglossum malachurum Kirby (Hymenoptera; Halictidae). Can J Zool 78(7):1259–1266. doi:10.1139/z00-064
Richards MH, French D, Paxton RJ (2005) It’s good to be queen: classically eusocial colony structure and low worker fitness in an obligately social sweat bee. Mol Ecol 14(13):4123–4133. doi:10.1111/j.1365-294X.2005.02724.x
Ronce O (2007) How does it feel to be like a rolling stone? Ten questions about dispersal evolution. Annu Rev Ecol Evol Syst 38(1):231–253. doi:10.1146/annurev.ecolsys.38.091206.095611
Rosenheim JA (1990) Density-dependent parasitism and the evolution of aggregated nesting in the solitary Hymenoptera. Ann Entomol Soc Am 83(3):277
Rousset F (2008) genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8(1):103–106. doi:10.1111/j.1471-8286.2007.01931.x
Sakagami SF, Hoshikawa K, Fukuda H (1984) Overwintering ecology of two social halictine bees, Lasioglossum duplex and L. problematicum. Res Popul Ecol 26(2):363–378. doi:10.1007/BF02515500
Salkind NJ (2007) Encyclopedia of measurement and statistics: Holm’s sequential Bonferroni procedure. Sage, Thousand Oaks
Schuttler SG, Philbrick JA, Jeffery KJ, Eggert LS, Wade C (2014) Fine-scale genetic structure and cryptic associations reveal evidence of kin-based sociality in the African forest elephant. PLoS One 9(2):e88074. doi:10.1371/journal.pone.0088074
Smith BH, Ayasse M (1987) Kin-based male mating preferences in two species of halictine bee. Behav Ecol Sociobiol 20(5):313–318. doi:10.1007/BF00300676
Smith BH, Weller C (1989) Social competition among gynes in halictine bees: the influence of bee size and pheromones on behavior. J Insect Behav 2(3):397–411. doi:10.1007/BF01068064
Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82(5):561–573. doi:10.1038/sj.hdy.6885180
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. Insect Soc 56(1):55–63. doi:10.1007/s00040-008-1037-y
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 Resour 9(1):150–152. doi:10.1111/j.1755-0998.2008.02416.x
Ulrich Y, Perrin N, Chapuisat M (2009) Flexible social organization and high incidence of drifting in the sweat bee, Halictus scabiosae. Mol Ecol 18(8):1791–1800. doi:10.1111/j.1365-294X.2009.04154.x
van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Mocro-Checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4(3):535–538. doi:10.1111/j.1471-8286.2004.00684.x
Vangestel C, Mergeay J, Dawson DA, Vandomme V, Lens LU (2011) Spatial heterogeneity in genetic relatedness among house sparrows along an urban–rural gradient as revealed by individual-based analysis. Mol Ecol 20(22):4643–4653. doi:10.1111/j.1365-294X.2011.05316.x
Waldbauer GP, Sternburg JG (1979) Inbreeding depression and a behavioral mechanism for its avoidance in Hyalophora cecropia. Am Midl Nat 102(1):204. doi:10.2307/2425089
Waldman B, McKinnon J (1993) Inbreeding and outbreeding in fishes, amphibians, and reptiles. The natural history of inbreeding and outbreeding: theoretical and empirical perspectives. University of Chicago Press, Chicago, 250–282
Wcislo WT (1996) Parasitism rates in relation to nest site in bees and wasps (Hymenoptera: Apoidea). J Insect Behav 9(4):643–656. doi:10.1007/BF02213885
Weissel N, Mitesser O, Liebig J, Poethke HJ, Strohm E (2006) The influence of soil temperature on the nesting cycle of the halictid bee Lasioglossum malachurum. Insectes Soc 53(4):390–398
Woxvold IA, Adcock GJ, Mulder RA (2006) Fine-scale genetic structure and dispersal in cooperatively breeding apostlebirds. Mol Ecol 15(11):3139–3146. doi:10.1111/j.1365-294X.2006.03009.x
Yanega D (1990) Philopatry and nest founding in a primitively social bee, Halictus rubicundus. Behav Ecol Sociobiol. doi:10.1007/BF00183311
Zobel MU, Paxton RJ (2007) Is big the best? Queen size, usurpation and nest closure in a primitively eusocial sweat bee (Lasioglossum malachurum). Behav Ecol Sociobiol 61(3):435–447. doi:10.1007/s00265-006-0271-4
Acknowledgements
We thank Claudia Mohra and Martin Fellendorf for collecting bees at Schützingen and Robin Moritz, Petra Leibe, and Michael Lattorff for providing laboratory equipment, technical assistance, and helpful discussion. We also thank the group of General Zoology at Martin-Luther University Halle-Wittenberg for discussion and support, and the two anonymous reviewers and the Editor, Miriam Richards, for constructive comments that helped improve the manuscript. Bees were collected under Permit No. 56-6/8852.15 from the Regierungspräsidium Tübingen to RJP.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Friedel, A., Paxton, R.J. & Soro, A. Spatial patterns of relatedness within nesting aggregations of the primitively eusocial sweat bee Lasioglossum malachurum . Insect. Soc. 64, 465–475 (2017). https://doi.org/10.1007/s00040-017-0559-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00040-017-0559-6