Advertisement

Evolutionary Ecology

, Volume 25, Issue 5, pp 1127–1144 | Cite as

Fine-scale spatial genetic structure and within population male-biased gene-flow in the grasshopper Mioscirtus wagneri

  • Joaquín Ortego
  • Maria Pilar Aguirre
  • Pedro J. Cordero
Original Paper

Abstract

Dispersal is a life history trait that plays a key role in population dynamics, determining gene flow and influencing the size, structure and persistence of populations. For these reasons, the study of the genetic consequences of dispersal can be considered a central topic in both conservation and population genetics. In this study we examine the patterns of fine-scale genetic structure within two populations of the grasshopper Mioscirtus wagneri (Orhoptera: Acrididae). For this purpose, we have used seven species-specific microsatellite markers to type 266 individuals from two populations (Peña Hueca and El Salobral) located in Central Spain. We have found subtle genetic differentiation between some sampling patches and significant kinship structures up to 25 m distance which were particularly patent for females. In Peña Hueca locality, patterns of isolation-by-distance at both the patch scale and the individual level have also revealed an association between genetic differentiation/similarity and geographical distance in females but not in males. Overall, these data suggest a fine-scale spatial genetic substructure in the studied populations which seems to be mainly driven by female philopatry. Such pattern of within population genetic structure together with the inferred restricted dispersal distances is likely to contribute to reduce effective population sizes and inter-population gene flow. This can erode genetic variability and limit the colonization ability of this orthoptera, factors which can ultimately compromise the long-term persistence of their small size and isolated populations.

Keywords

Genetic structure Isolation by distance Microsatellites Mioscirtus wagneri Sex-biased dispersal 

Notes

Acknowledgments

We wish to thank José Miguel Aparicio for advice on some statistical analyses. The Editors from Evolutionary Ecology and two anonymous referees provided useful discussion and valuable comments on an earlier draft of this manuscript. This work received financial support from the projects PCI08-0130 and POII09-0198-8057 (JCCM) and CGL2008-00095/BOS (MICINN). Specimens were captured under license from the Junta de Comunidades de Castilla-La Mancha (JCCM). The study was funded by a post-doctoral JAE-Doc (CSIC) contract (to J.O.) and a research contract from the Junta de Comunidades de Castilla-La Mancha/European Social Fund (to P.A.).

Supplementary material

10682_2011_9462_MOESM1_ESM.doc (180 kb)
Supplementary material 1 (DOC 180 kb)

References

  1. Aguirre MP, Bloor P, Ramírez-Escobar U, Ortego J, Cordero PJ (2010) Isolation and characterization of polymorphic microsatellite markers in the grasshopper Mioscirtus wagneri (Orthoptera: Acrididae). Conserv Genet 11:1119–1121CrossRefGoogle Scholar
  2. Bailey NW, Gwynne DT, Ritchie MG (2007) Dispersal differences predict population genetic structure in Mormon crickets. Mol Ecol 16:2079–2089PubMedCrossRefGoogle Scholar
  3. Broquet T, Petit EJ (2009) Molecular estimation of dispersal for ecology and population genetics. Annu Rev Ecol Evol Syst 40:193–216CrossRefGoogle Scholar
  4. Chapman JR, Nakagawa S, Coltman DW, Slate J, Sheldon BC (2009) A quantitative review of heterozygosity-fitness correlations in animal populations. Mol Ecol 18:2746–2765PubMedCrossRefGoogle Scholar
  5. Chapuis MP, Lecoq M, Michalakis Y, Loiseau A, Sword GA, Piry S, Estoup A (2008) Do outbreaks affect genetic population structure? A worldwide survey in Locusta migratoria, a pest plagued by microsatellite null alleles. Mol Ecol 17:3640–3653PubMedCrossRefGoogle Scholar
  6. Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Ann Rev Ecol Evol Syst 18:237–268CrossRefGoogle Scholar
  7. Clarke AL, Saether BE, Roskaft E (1997) Sex biases in avian dispersal: a reappraisal. Oikos 79:429–438CrossRefGoogle Scholar
  8. Clemencet J, Viginier B, Doums C (2005) Hierarchical analysis of population genetic structure in the monogynous ant Cataglyphis cursor using microsatellite and mitochondrial DNA markers. Mol Ecol 14:3735–3744PubMedCrossRefGoogle Scholar
  9. Clobert J, Danchin E, Dhondt AA, Nichols JD (2001) Dispersal. Oxford University Press, OxfordGoogle Scholar
  10. Coltman DW (2005) Evolutionary genetics—differentiation by dispersal. Nature 433:23–24PubMedCrossRefGoogle Scholar
  11. Coltman DW, Pilkington JG, Pemberton JM (2003) Fine-scale genetic structure in a free-living ungulate population. Mol Ecol 12:733–742PubMedCrossRefGoogle Scholar
  12. Cordero PJ, Llorente V, Aparicio JM (2007) New data on morphometrics, distribution and ecology of Mioscirtus wagneri (Kittary, 1859) (Orthoptera, Acrididae) in Spain: is maghrebi a well defined subspecies? Graellsia 63:3–16CrossRefGoogle Scholar
  13. Dieckmann U, O’Hara B, Weisser W (1999) The evolutionary ecology of dispersal. Trends Ecol Evol 14:88–90CrossRefGoogle Scholar
  14. Dobson FS (1982) Competition for mates and predominant juvenile male dispersal in mammals. Anim Behav 30:1183–1192CrossRefGoogle Scholar
  15. Double MC, Peakall R, Beck NR, Cockburn A (2005) Dispersal, philopatry, and infidelity: Dissecting local genetic structure in superb fairy-wrens (Malurus cyaneus). Evolution 59:625–635PubMedGoogle Scholar
  16. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  17. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50Google Scholar
  18. Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 3rd edn. Longman, HarlowGoogle Scholar
  19. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedGoogle Scholar
  20. Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10:1500–1508CrossRefGoogle Scholar
  21. Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140CrossRefGoogle Scholar
  22. Galarza JA, Carreras-Carbonell J, Macpherson E, Pascual M, Roques S, Turner GF, Rico C (2009) The influence of oceanographic fronts and early-life-history traits on connectivity among littoral fish species. Proc Natl Acad Sci USA 106:1473–1478PubMedCrossRefGoogle Scholar
  23. Garant D, Kruuk LEB, Wilkin TA, McCleery RH, Sheldon BC (2005) Evolution driven by differential dispersal within a wild bird population. Nature 433:60–65PubMedCrossRefGoogle Scholar
  24. Gilpin M (1991) The genetic effective size of a metapopulation. Biol J Linn Soc 42:165–175CrossRefGoogle Scholar
  25. Gómez A, Montero-Pau J, Lunt DH, Serra M, Campillo S (2007) Persistent genetic signatures of colonization in Brachionus manjavacas rotifers in the Iberian Peninsula. Mol Ecol 16:3228–3240PubMedCrossRefGoogle Scholar
  26. Goodisman MAD, Ross KG (1998) A test of queen recruitment models using nuclear and mitochondrial markers in the fire ant Solenopsis invicta. Evolution 52:1416–1422CrossRefGoogle Scholar
  27. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices, version 2.9.3. Lausanne University, LausanneGoogle Scholar
  28. Goudet J, Perrin N, Waser P (2002) Tests for sex-biased dispersal using bi-parentally inherited genetic markers. Mol Ecol 11:1103–1114PubMedCrossRefGoogle Scholar
  29. Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162CrossRefGoogle Scholar
  30. Guo SW, Thompson EA (1992) A monte-carlo method for combined segregation and linkage analysis. Am J Hum Gen 51:1111–1126Google Scholar
  31. Gyllenstrand N, Seppa P (2003) Conservation genetics of the wood ant, Formica lugubris, in a fragmented landscape. Mol Ecol 12:2931–2940PubMedCrossRefGoogle Scholar
  32. Hansson B, Bensch S, Hasselquist D (2003) A new approach to study dispersal: immigration of novel alleles reveals female-biased dispersal in great reed warblers. Mol Ecol 12:631–637PubMedCrossRefGoogle Scholar
  33. Hardy OJ, Vekemans X (2002) SPAGEDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620CrossRefGoogle Scholar
  34. Harrison S, Hastings A (1996) Genetic and evolutionary consequences of metapopulation structure. Trends Ecol Evol 11:180–183PubMedCrossRefGoogle Scholar
  35. Havel JE, Shurin JB (2004) Mechanisms, effects, and scales of dispersal in freshwater zooplankton. Limnol Oceanogr 49:1229–1238CrossRefGoogle Scholar
  36. Hazlitt SL, Eldridge MDB, Goldizen AW (2004) Fine-scale spatial genetic correlation analyses reveal strong female philopatry within a brush-tailed rock-wallaby colony in southeast Queensland. Mol Ecol 13:3621–3632PubMedCrossRefGoogle Scholar
  37. Hedrick PW (1996) Bottleneck(s) or metapopulation in cheetahs. Conserv Biol 10:897–899CrossRefGoogle Scholar
  38. Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332PubMedCrossRefGoogle Scholar
  39. 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
  40. Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Gen 6:13Google Scholar
  41. Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189CrossRefGoogle Scholar
  42. Knight ME, Van Oppen MJH, Smith HL, Rico C, Hewitt GM, Turner GF (1999) Evidence for male-biased dispersal in Lake Malawi cichlids from microsatellites. Mol Ecol 8:1521–1527PubMedCrossRefGoogle Scholar
  43. Lambin X, Aars J, Piertney SB (2001) Dispersal, intraspecific competition, kin competition and kin facilitation: a review of empirical evidence. In: Clobert J, Danchin E, Dhondt AA, Nichols JD (eds) Dispersal. Oxford University Press, Oxford, pp 123–142Google Scholar
  44. Lorch PD, Gwynne DT (2000) Radio-telemetric evidence of migration in the gregarious but not the solitary morph of the Mormon cricket (Anabrus simplex: Orthoptera: Tettigoniidae). Naturwissenschaften 87:370–372PubMedCrossRefGoogle Scholar
  45. Lorch PD, Sword GA, Gwynne DT, Anderson GL (2005) Radiotelemetry reveals differences in individual movement patterns between outbreak and non-outbreak Mormon cricket populations. Ecol Entomol 30:548–555CrossRefGoogle Scholar
  46. Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197CrossRefGoogle Scholar
  47. Moore J, Ali R (1984) Are dispersal and inbreeding avoidance related. Anim Behav 32:94–112CrossRefGoogle Scholar
  48. Nei M (1977) F-statistics and analysis of gene diversity in subdivided populations. Ann Hum Genet 41:225–233PubMedCrossRefGoogle Scholar
  49. Nussey DH, Coltman DW, Coulson T, Kruuk LEB, Donald A, Morris SJ, Clutton-Brocks TH, Pemberton J (2005) Rapidly declining fine-scale spatial genetic structure in female red deer. Mol Ecol 14:3395–3405PubMedCrossRefGoogle Scholar
  50. Ortego J, Aparicio JM, Cordero PJ, Calabuig G (2008a) Individual genetic diversity correlates with the size and spatial isolation of natal colonies in a bird metapopulation. Proc R Soc B 275:2039–2047PubMedCrossRefGoogle Scholar
  51. Ortego J, Calabuig G, Aparicio J, Cordero PJ (2008b) Genetic consequences of natal dispersal in the colonial lesser kestrel. Mol Ecol 17:2051–2059PubMedCrossRefGoogle Scholar
  52. Ortego J, Bonal R, Cordero PJ, Aparicio JM (2009) Phylogeography of the Iberian populations of Mioscirtus wagneri (Orthoptera: Acrididae), a specialized grasshopper inhabiting highly fragmented hypersaline environments. Biol J Linn Soc 97:623–633CrossRefGoogle Scholar
  53. Ortego J, Aguirre MP, Cordero PJ (2010) Population genetics of Mioscirtus wagneri, a grasshopper showing a highly fragmented distribution. Mol Ecol 19:472–483PubMedCrossRefGoogle Scholar
  54. Palo JU, Lesbarreres D, Schmeller DS, Primmer CR, Merila J (2004) Microsatellite marker data suggest sex-biased dispersal in the common frog Rana temporaria. Mol Ecol 13:2865–2869PubMedCrossRefGoogle Scholar
  55. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  56. Peakall R, Smouse PE, Huff DR (1995) Evolutionary implications of allozyme and RAPD variation in diploid populations of dioecious buffalograss Buchloe dactyloides. Mol Ecol 4:135–147CrossRefGoogle Scholar
  57. Peakall R, Ruibal M, Lindenmayer DB (2003) Spatial autocorrelation analysis offers new insights into gene flow in the Australian bush rat, Rattus fuscipes. Evolution 57:1182–1195PubMedGoogle Scholar
  58. Perrin N, Mazalov V (2000) Local competition, inbreeding, and the evolution of sex-biased dispersal. Am Nat 155:116–127PubMedCrossRefGoogle Scholar
  59. Postma E, Van Noordwijk AJ (2005) Gene flow maintains a large genetic difference in clutch size at a small spatial scale. Nature 433:65–68PubMedCrossRefGoogle Scholar
  60. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  61. Prugnolle F, de Meeus T (2002) Inferring sex-biased dispersal from population genetic tools: a review. Heredity 88:161–165PubMedCrossRefGoogle Scholar
  62. Pusey AE (1987) Sex-biased dispersal and inbreeding avoidance in birds and mammals. Trends Ecol Evol 2:295–299PubMedCrossRefGoogle Scholar
  63. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic-markers. Evolution 43:258–275CrossRefGoogle Scholar
  64. Rassmann K, Tautz D, Trillmich F, Gliddon C (1997) The microevolution of the Galapagos marine iguana Amblyrhynchus cristatus assessed by nuclear and mitochondrial genetic analyses. Mol Ecol 6:437–452CrossRefGoogle Scholar
  65. Riegert PW, Fuller RA, Putnam LG (1954) Studies on dispersal of grasshoppers. (Acrididae) tagged with phosphorus-32. Can Entomol 86:223–232CrossRefGoogle Scholar
  66. Robbins RK, Small GB (1981) Wind dispersal of Panamanian hairstreak butterflies (Lepidoptera, Lycaenidae) and its evolutionary significance. Biotropica 13:308–315CrossRefGoogle Scholar
  67. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228PubMedGoogle Scholar
  68. Rousset F (2000) Genetic differentiation between individuals. J Evol Biol 13:58–62CrossRefGoogle Scholar
  69. Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I (1998) Inbreeding and extinction in a butterfly metapopulation. Nature 392:491–494CrossRefGoogle Scholar
  70. Slatkin M (1993) Isolation by distance in equilibrium and nonequilibrium populations. Evolution 47:264–279CrossRefGoogle Scholar
  71. Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573PubMedCrossRefGoogle Scholar
  72. Stow AJ, Sunnucks P, Briscoe DA, Gardner MG (2001) The impact of habitat fragmentation on dispersal of Cunningham’s skink (Egernia cunninghami): evidence from allelic and genotypic analyses of microsatellites. Mol Ecol 10:867–878PubMedCrossRefGoogle Scholar
  73. Sugg DW, Chesser RK, Dobson FS, Hoogland JL (1996) Population genetics meets behavioral ecology. Trends Ecol Evol 11:338–342PubMedCrossRefGoogle Scholar
  74. Suni SS, Gordon DM (2010) Fine-scale genetic structure and dispersal distance in the harvester ant Pogonomyrmex barbatus. Heredity 104:168–173PubMedCrossRefGoogle Scholar
  75. Sword GA, Lorch PD, Gwynne DT (2008) Radiotelemetric analysis of the effects of prevailing wind direction on Mormon cricket migratory band movement. Environ Entomol 37:889–896PubMedCrossRefGoogle Scholar
  76. Temple HJ, Hoffman JI, Amos W (2006) Dispersal, philopatry and intergroup relatedness: fine-scale genetic structure in the white-breasted thrasher, Ramphocinclus brachyurus. Mol Ecol 15:3449–3458PubMedCrossRefGoogle Scholar
  77. Ustinova J, Achmann R, Cremer S, Mayer F (2006) Long repeats in a huge genome: microsatellite loci in the grasshopper Chorthippus biguttulus. J Mol Evol 62:158–167PubMedCrossRefGoogle Scholar
  78. Van de Casteele T, Matthysen E (2006) Natal dispersal and parental escorting predict relatedness between mates in a passerine bird. Mol Ecol 15:2557–2565PubMedCrossRefGoogle Scholar
  79. Vanschoenwinkel B, Gielen S, Seaman M, Brendonck L (2009) Wind mediated dispersal of freshwater invertebrates in a rock pool metacommunity: differences in dispersal capacities and modes. Hydrobiologia 635:363–372CrossRefGoogle Scholar
  80. Vitalis R (2002) Sex-specific genetic differentiation and coalescence times: estimating sex-biased dispersal rates. Mol Ecol 11:125–138PubMedCrossRefGoogle Scholar
  81. Watts PC, Rousset F, Saccheri IJ, Leblois R, Kemp SJ, Thompson DJ (2007) Compatible genetic and ecological estimates of dispersal rates in insect (Coenagrion mercuriale: Odonata : Zygoptera) populations: analysis of ‘neighbourhood size’ using a more precise estimator. Mol Ecol 16:737–751PubMedCrossRefGoogle Scholar
  82. Willi Y, Van Buskirk J, Hoffmann AA (2006) Limits to the adaptive potential of small populations. Ann Rev Ecol Evol Syst 37:433–458CrossRefGoogle Scholar
  83. Wright S (1969) Evolution and the genetics of populations, vol. 2. The theory of gene frequencies. University of Chicago Press, ChicagoGoogle Scholar
  84. Wright S (1978) Evolution and the genetics of populations, vol. 4: variability within and among natural populations. University of Chicago Press, ChicagoGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Joaquín Ortego
    • 1
  • Maria Pilar Aguirre
    • 2
  • Pedro J. Cordero
    • 2
  1. 1.Departamento de Ecología EvolutivaMuseo Nacional de Ciencias Naturales (CSIC)MadridSpain
  2. 2.Grupo de Investigación de la Biodiversidad Genética y Cultural, Instituto de Investigación en Recursos Cinegéticos, IREC (CSIC, UCLM, JCCM)Ciudad RealSpain

Personalised recommendations