Skip to main content
SpringerLink
Log in

Male-biased dispersal promotes large scale gene flow in a subterranean army ant, Dorylus (Typhlopone) fulvus

  • Original article
  • Published:
Population Ecology

Abstract

Sex-biased dispersal is a widespread phenomenon in the animal kingdom, which strongly influences gene flow and population structure. Particularly army ants, important key-stone predators in tropical ecosystems, are prone to population fragmentation and isolation due to their extraordinary mating system: queens are permanently wingless, propagate via colony fission, and only the males disperse in mating flights. Here we report on sex-biased dispersal and the genetic population structure of an African subterranean army ant, Dorylus (Typhlopone) fulvus. Using maternally inherited mtDNA markers and bi-parentally inherited nuclear microsatellites we found strong geographical structuring of mtDNA haplotypes, whereas the nuclear genetic population structure was less pronounced. Strong mtDNA (Φ ST = 0.85), but significantly lower nuclear (F ST = 0.23) genetic differentiation translated into a more than an order of magnitude larger male migration rate compared to that of queens, reflecting the low motility of queens and strong, promiscuous dispersal by males. Thus, the well flying D. fulvus males appear to be the sex to promote large scale gene flow, and D. fulvus is indeed a species in which sex specific dispersal patterns and the mating system profoundly affect the population structure and phylogeography.

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

Similar content being viewed by others

References

  • Berg LM, Lascoux M, Pamilo P (1998) The infinite island model with sex-differentiated gene flow. Heredity 81:63–68

    Article  Google Scholar 

  • Berghoff SM, Maschwitz U, Linsenmair KE (2003) Influence of the hypogaeic army ant Dorylus (Dichthadia) laevigatus on tropical arthropod communities. Oecologia 135:149–157

    PubMed  Google Scholar 

  • Berghoff SM, Kronauer DJC, Edwards KJ, Franks NR (2008) Dispersal and population structure of a new world predator, the army ant Eciton burchellii. J Evol Biol 21:1125–1132

    Article  PubMed  CAS  Google Scholar 

  • Bolton B (1995) A new general catalogue of the ants of the world. Harvard University Press, Cambridge

    Google Scholar 

  • Bourke AFG, Heinze J (1994) The ecology of communal breeding—the case of multiple-queen Leptothoracine ants. Philos Trans R Soc B-Biol Sci 345:359–372

    Article  Google Scholar 

  • Bowler DE, Benton TG (2005) Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol Rev 80:205–225

    Article  PubMed  Google Scholar 

  • Brady SG, Gadau J, Ward PS (2000) Systematics of the ant genus Camponotus (Hymenoptera: Formicidae): a preliminary analysis using data from the mitochondrial gene cytochrome oxidase I. In: Austin AD, Dowton M (eds) Hymenoptera: evolution, biodiversity and biological control. CSIRO, Collingwood, pp 131–139

    Google Scholar 

  • Brandt M, Fischer-Blass B, Heinze J, Foitzik S (2007) Population structure and the co-evolution between social parasites and their hosts. Mol Ecol 16:2063–2078

    Article  PubMed  CAS  Google Scholar 

  • Bulmer MG (1983) Sex-ratio theory in social insects with swarming. J Theor Biol 100:329–339

    Article  Google Scholar 

  • Chapman RE, Bourke AFG (2001) The influence of sociality on the conservation biology of social insects. Ecol Lett 4:650–662

    Article  Google Scholar 

  • Chesser RK, Baker RJ (1996) Effective sizes and dynamics of uniparentally and diparentally inherited genes. Genetics 144:1225–1235

    PubMed  CAS  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Article  PubMed  CAS  Google Scholar 

  • Clobert J (2001) Dispersal. Oxford University Press, Oxford

    Google Scholar 

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

    Article  Google Scholar 

  • Darlington JPEC (1985) Attacks by Doryline ants and termite nest defenses (Hymenoptera: Formicidae, Isoptera: Termitidae). Sociobiology 11:189–200

    Google Scholar 

  • Doums C, Cabrera H, Peeters C (2002) Population genetic structure and male-biased dispersal in the queenless ant Diacamma cyaneiventre. Mol Ecol 11:2251–2264

    Article  PubMed  CAS  Google Scholar 

  • Ennos RA (1994) Estimating the relative rates of pollen and seed migration among plant-populations. Heredity 72:250–259

    Article  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50

    CAS  Google Scholar 

  • Goropashnaya AV, Fedorov VB, Seifert B, Pamilo P (2007) Phylogeography and population structure in the ant Formica exsecta (Hymenoptera: Formicidae) across Eurasia as reflected by mitochondrial DNA variation and microsatellites. Ann Zool Fenn 44:462–474

    Google Scholar 

  • Gotwald WH Jr (1995) Army ants: the biology of social predation. Comstock, Ithaca

    Google Scholar 

  • Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Gros A, Hovestadt T, Poethke HJ (2008) Evolution of sex-biased dispersal: the role of sex-specific dispersal costs, demographic stochasticity, and inbreeding. Ecol Model 219:226–233

    Article  Google Scholar 

  • Haddow AJ, Yarrow IHH, Lancaste GA, Corbet PS (1966) Nocturnal flight cycle in the males of African Doryline ants (Hymenoptera: Formicidae). Proc R Entomol Soc A 41:103–106

    Google Scholar 

  • Hedrick PW (1999) Perspective: highly variable loci and their interpretation in evolution and conservation. Evolution 53:313–318

    Article  Google Scholar 

  • Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638

    PubMed  CAS  Google Scholar 

  • Hölldobler B, Wilson EO (1990) The ants. Belknap Press of Harvard University Press, Cambridge

    Book  Google Scholar 

  • Jaffé R, Kronauer DJC, Kraus FB, Boomsma JJ, Moritz RFA (2007) Worker caste determination in the army ant Eciton burchellii. Biol Lett 3:513–516

    Article  PubMed  Google Scholar 

  • Jaffé R, Moritz RFA, Kraus FB (2009) Gene flow is maintained by polyandry and male dispersal in the army ant Eciton burchellii. Popul Ecol 51:227–236

    Article  Google Scholar 

  • Jarne P, Lagoda PJL (1996) Microsatellites, from molecules to populations and back. Trends Ecol Evol 11:424–429

    Article  PubMed  CAS  Google Scholar 

  • Kaspari M, Powell S, Lattke J, O’Donnell S (2011) Predation and patchiness in the tropical litter: do swarm-raiding army ants skim the cream or drain the bottle? J Anim Ecol 80:818–823

    Article  PubMed  Google Scholar 

  • Knowles LL, Maddison WP (2002) Statistical phylogeography. Mol Ecol 11:2623–2635

    Article  PubMed  Google Scholar 

  • Kraus FB, Koeniger N, Tingek S, Moritz RFA (2005) Using drones for estimating colony number by microsatellite DNA analyses of haploid males in Apis. Apidologie 36:223–229

    Article  CAS  Google Scholar 

  • Kraus FB, Wolf S, Moritz RFA (2009) Male flight distance and population substructure in the bumblebee Bombus terrestris. J Anim Ecol 78:247–252

    Article  PubMed  CAS  Google Scholar 

  • Kronauer DJC (2009) Recent advances in army ant biology (Hymenoptera: Formicidae). Myrmecol News 12:51–65

    Google Scholar 

  • Kronauer DJC, Boomsma JJ, Gadau J (2004) Microsatellite markers for the driver ant Dorylus (Anomma) molestus. Mol Ecol Notes 4:289–290

    Article  CAS  Google Scholar 

  • Kronauer DJC, Johnson RA, Boomsma JJ (2007a) The evolution of multiple mating in army ants. Evolution 61:413–422

    Article  PubMed  Google Scholar 

  • Kronauer DJC, Schöning C, Vilhelmsen LB, Boomsma JJ (2007b) A molecular phylogeny of Dorylus army ants provides evidence for multiple evolutionary transitions in foraging niche. BMC Evol Biol 7:1–11

    Article  Google Scholar 

  • Kronauer DJC, Peters MK, Schöning C, Boomsma JJ (2011) Hybridization in East African swarm-raiding army ants. Front Zool 8:1–13

    Article  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  PubMed  CAS  Google Scholar 

  • Lepais O, Darvill B, O’Connor S, Osborne JL, Sanderson RA, Cussans J, Goffe L, Goulson D (2010) Estimation of bumblebee queen dispersal distances using sibship reconstruction method. Mol Ecol 19:819–831

    Article  PubMed  CAS  Google Scholar 

  • Leroux J (1979) Sur quelques modalites de disparition des colonies d’Anomma nigricans Illiger (Formicidæ: Dorylinæ) dans la region de Lamto (Cote-d’Ivoire). Insect Soc 26:93–100 (in French with English abstract)

    Article  Google Scholar 

  • Leston D (1979) Dispersal by male Doryline ants in West Africa. Psyche 86:63–77

    Article  Google Scholar 

  • Liautard C, Keller L (2001) Restricted effective queen dispersal at a microgeographic scale in polygynous populations of the ant Formica exsecta. Evolution 55:2484–2492

    PubMed  CAS  Google Scholar 

  • Meisel JE (2006) Thermal ecology of the neotropical army ant Eciton burchellii. Ecol Appl 16:913–922

    Article  PubMed  Google Scholar 

  • Moritz RFA, Dietemann V, Crewe R (2008) Determining colony densities in wild honeybee populations (Apis mellifera) with linked microsatellite DNA markers. J Insect Conserv 12:455–459

    Article  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Panchal M, Beaumont MA (2007) The automation and evaluation of nested clade phylogeographic analysis. Evolution 61:1466–1480

    Article  PubMed  Google Scholar 

  • Peeters C, Ito F (2001) Colony dispersal and the evolution of queen morphology in social Hymenoptera. Annu Rev Entomol 46:601–630

    Article  PubMed  CAS  Google Scholar 

  • Perrin N, Mazalov V (2000) Local competition, inbreeding, and the evolution of sex-biased dispersal. Am Nat 155:116–127

    Article  PubMed  Google Scholar 

  • Peters MK, Fischer G, Schaab G, Kraemer M (2009) Species compensation maintains abundance and raid rates of African swarm-raiding army ants in rainforest fragments. Biol Conserv 142:668–675

    Article  Google Scholar 

  • Posada D, Crandall KA, Templeton AR (2000) GeoDis: a program for the cladistic nested analysis of the geographical distribution of genetic haplotypes. Mol Ecol 9:487–488

    Article  PubMed  CAS  Google Scholar 

  • Prugnolle F, de Meeus T (2002) Inferring sex-biased dispersal from population genetic tools: a review. Heredity 88:161–165

    Article  PubMed  CAS  Google Scholar 

  • Pusey AE (1987) Sex-biased dispersal and inbreeding avoidance in birds and mammals. Trends Ecol Evol 2:295–299

    Article  PubMed  CAS  Google Scholar 

  • Raigner A, Van Boven JKA (1955) Étude taxonomique, biologique et biométrique des Dorylus du sous-genre Anomma (Hymenoptera: Formicidae). Annales Musée Royal du Congo Belge Nouvelle Série in Quarto Sciences Zoologiques 2:1–359 (in French)

    Google Scholar 

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

    Google Scholar 

  • Ritchie EG, Johnson CN (2009) Predator interactions, mesopredator release and biodiversity conservation. Ecol Lett 12:982–998

    Article  PubMed  Google Scholar 

  • Ross KG, Krieger MJB, Shoemaker DD, Vargo EL, Keller L (1997) Hierarchical analysis of genetic structure in native fire ant populations: results from three classes of molecular markers. Genetics 147:643–655

    PubMed  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Sanetra M, Crozier RH (2003) Patterns of population subdivision and gene flow in the ant Nothomyrmecia macrops reflected in microsatellite and mitochondrial DNA markers. Mol Ecol 12:2281–2295

    Article  PubMed  CAS  Google Scholar 

  • Santschi F (1931) La reine du Dorylus fulvus Westw. Bulletin de la Société d’Histoire Naturelle de l’Afrique du Nord 22:401–408 (in French)

    Google Scholar 

  • Schöning C, Moffett MW (2007) Driver ants invading a termite nest: why do the most catholic predators of all seldom take this abundant prey? Biotropica 39:663–667

    Article  Google Scholar 

  • Schöning C, Njagi WM, Franks NR (2005) Temporal and spatial patterns in the emigrations of the army ant Dorylus (Anomma) molestus in the montane forest of Mt Kenya. Ecol Entomol 30:532–540

    Article  Google Scholar 

  • Schöning C, Kinuthia W, Boomsma JJ (2006) Does the afrotropical army ant Dorylus (Anomma) molestus go extinct in fragmented forests? J East Afr Nat Hist 95:163–179

    Article  Google Scholar 

  • Schöning C, Csuzdi C, Kinuthia W, Ogutu JO (2010) Influence of driver ant swarm raids on earthworm prey densities in the Mount Kenya forest: implications for prey population dynamics and colony migrations. Insect Soc 57:73–82

    Article  Google Scholar 

  • Seppä P, Gyllenstrand M, Corander J, Pamilo P (2004) Coexistence of the social types: genetic population structure in the ant Formica exsecta. Evolution 58:2462–2471

    PubMed  Google Scholar 

  • Seppä P, Fernandez-Escudero I, Gyllenstrand N, Pamilo P (2006) Obligatory female philopatry affects genetic population structure in the ant Proformica longiseta. Insect Soc 53:362–368

    Article  Google Scholar 

  • Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene-sequences and a compilation of conserved polymerase chain-reaction primers. Ann Entomol Soc Am 87:651–701

    CAS  Google Scholar 

  • Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792

    Article  PubMed  CAS  Google Scholar 

  • Sundström L, Seppä P, Pamilo P (2005) Genetic population structure and dispersal patterns in Formica ants—a review. Ann Zool Fenn 42:163–177

    Google Scholar 

  • Templeton AR (2004) Statistical phylogeography: methods of evaluating and minimizing inference errors. Mol Ecol 13:789–809

    Article  PubMed  Google Scholar 

  • Templeton AR (2008) Nested clade analysis: an extensively validated method for strong phylogeographic inference. Mol Ecol 17:1877–1880

    Article  PubMed  Google Scholar 

  • Templeton AR, Routman E, Phillips CA (1995) Separating population structure from population history: a cladistic analysis of the geographical distribution of mitochondrial DNA haplotypes in the tiger salamander, Ambystoma Tigrinum. Genetics 140:767–782

    PubMed  CAS  Google Scholar 

  • Wade MJ, McKnight ML, Shaffer HB (1994) The effects of kin-structured colonization on nuclear and cytoplasmic genetic diversity. Evolution 48:1114–1120

    Article  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

    PubMed  CAS  Google Scholar 

  • Wang JL (2004) Sibship reconstruction from genetic data with typing errors. Genetics 166:1963–1979

    Article  PubMed  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Whitlock MC, McCauley DE (1999) Indirect measures of gene flow and migration: F ST ≠ 1/(4Nm + 1). Heredity 82:117–125

    Article  PubMed  Google Scholar 

  • Wolf S, Toev T, Moritz RLV, Moritz RFA (2012) Spatial and temporal dynamics of the male effective population size in bumblebees (Hymenoptera: Apidae). Popul Ecol 54:115–124

    Article  Google Scholar 

  • Wright S (1969) Evolution and the genetics of populations. vol. 2: the theory of gene frequencies. University of Chicago Press, Chicago

Download references

Acknowledgments

We wish to thank Vincent Dietemann and Eckart Stolle for providing samples and Christoph Eller for valuable help with the laboratory work. We are further grateful for technical assistance by Denise Kleber and Petra Leibe. The comments of two anonymous reviewers significantly improved an earlier draft of the manuscript. Financial support was granted by the Postgraduate Scholarship of Saxony-Anhalt, Germany.

Author information

Authors and Affiliations

  1. Department of Biology, Martin-Luther-University Halle-Wittenberg, Hoher Weg 4, 06099, Halle (Saale), Germany

    Matthias Benjamin Barth, Robin Frederik Alexander Moritz & Frank Bernhard Kraus

  2. Department of Zoology and Entomology, University of Pretoria, Pretoria, 0002, South Africa

    Robin Frederik Alexander Moritz & Christian Walter Werner Pirk

  3. Department of Laboratory Medicine, University Hospital Halle, Ernst Grube Str. 40, 06120, Halle (Saale), Germany

    Frank Bernhard Kraus

Authors
  1. Matthias Benjamin Barth
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robin Frederik Alexander Moritz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christian Walter Werner Pirk
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Frank Bernhard Kraus
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Matthias Benjamin Barth.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 60 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barth, M.B., Moritz, R.F.A., Pirk, C.W.W. et al. Male-biased dispersal promotes large scale gene flow in a subterranean army ant, Dorylus (Typhlopone) fulvus . Popul Ecol 55, 523–533 (2013). https://doi.org/10.1007/s10144-013-0383-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10144-013-0383-4

Keywords

Search

Navigation