Journal of Insect Conservation

, Volume 16, Issue 2, pp 263–273 | Cite as

Dispersal via stream corridors structures populations of the endangered St. Francis’ satyr butterfly (Neonympha mitchellii francisci)

  • Laura V. Milko
  • Nick M. Haddad
  • Stacey L. Lance


Habitat fragmentation may reduce gene flow and population viability of rare species. We tested whether riparian corridors enhanced gene flow and if human habitat modification between riparian corridors subsequently reduced dispersal and gene flow of a wetland butterfly, the US federally endangered St. Francis’ satyr butterfly (Neonympha mitchellii francisci). We surveyed nine populations throughout the taxon’s range using five polymorphic microsatellite loci. We found that genetic diversity of N. m. francisci was relatively high despite its restricted distribution, and that there is little evidence of population bottlenecks or extensive inbreeding within populations. We found substantial gene flow and detectable first generation migration, suggesting that N. m. francisci is unlikely to be currently endangered by genetic factors. Pairwise population differentiation and clustering indicate some structuring between populations on different drainages and suggest that dispersal probably occurs mainly via a stepping stone from the closest riparian corridors. However, genetic differentiation between geographically close populations suggests that isolation by distance is not solely responsible for population structure, and that management actions should be targeted at maintaining connectivity of riparian and upland habitats.


Neonympha mitchellii francisci Satyrinae Butterfly Microsatellite STR Corridors 


  1. Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Blackwell Publishing Ltd, OxfordGoogle Scholar
  2. Bartel RA, Haddad NM, Wright JP (2010) Ecosystem engineers maintain a rare species of butterfly and increase plant diversity. Oikos 119:883–890CrossRefGoogle Scholar
  3. Bouzat JL, Johnson JA, Toepfer JE, Simpson SA, Esker TL, Westemeier RL (2008) Beyond the beneficial effects of translocations as an effective tool for the genetic restoration of isolated populations. Conserv Genet 10:191–201CrossRefGoogle Scholar
  4. Chaline N, Ratneiks FLW, Raine NE, Badcock NS, Burke T (2004) Non-lethal sampling of honey bee (Apis mellifera) DNA using wing tips. Apidologies 35:11–18Google Scholar
  5. Cornuet JM, Luikart G (1997) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014Google Scholar
  6. DeWoody AJ, Schupp J, Kenefic L (2004) Universal method for producing ROX-labeled size standards suitable for automated genotyping. BioTechniques 37:348–350PubMedGoogle Scholar
  7. DiRienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Frimer NB (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci 91:3166–3170CrossRefGoogle Scholar
  8. Don RH, Cox PT, Wainwright BJ, Baker K, Mattick JS (1991) ‘Touchdown’ PCR to circumvent spurious priming during gene amplification. Nucleic Acids Res 19:4008PubMedCrossRefGoogle Scholar
  9. Epps CW, Wehausen JD, Bleich VC, Torres SG, Brahares JS (2007) Optimizing dispersal and corridor models using landscape genetics. J Appl Ecol 44:714–724CrossRefGoogle Scholar
  10. 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
  11. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetic data analysis. Evol Bioinf 1:47–50 OnlineGoogle Scholar
  12. Faircloth BC (2008) MSATCOMMANDER: detection of microsatellite repeat arrays and automated, locus-specific primer design. Mol Ecol 8:92–94CrossRefGoogle Scholar
  13. 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
  14. Flanagan SP, Wilson WH, Jones KL, Lance SL (2010) Development and characterization of twelve polymorphic microsatellite loci in the Bog Copper, Lycaena epixanthe. Conserv Genet Resour. doi:10.1007/s12686-010-9206-5
  15. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, CambridgeGoogle Scholar
  16. Glenn TC, Schable NA (2005) Isolating microsatellite DNA loci. Methods Enzymol 395:202–222PubMedCrossRefGoogle Scholar
  17. Goudet J (2002) FSTAT, a program to estimate and test gene diversities and fixation indices version Available from [updated from Goudet (1995)]
  18. Grant EH, Nichols JD, Lowe WH, Fagan WF (2010) Use of multiple dispersal pathways facilitates amphibian persistence in stream networks. Proc Natl Acad Sci USA 107:6936–6940CrossRefGoogle Scholar
  19. Haddad NM (1999) Corridor and distance effects on interpatch movements: a landscape experiment with butterflies. Ecol Appl 9:612–622CrossRefGoogle Scholar
  20. Haddad NM, Baum KA (1999) An experimental test of corridor effects on butterfly densities. Ecol Appl 9:623–633CrossRefGoogle Scholar
  21. Haddad NM, Tewksbury JJ (2006) Impacts of corridors on populations and communities. In: Crooks KR, Sanjayan MA (eds) Connectivity conservation. Cambridge University Press, Cambridge, pp 390–415CrossRefGoogle Scholar
  22. Haddad NM, Kuefler D, Hudgens B (2003) Evaluating population viability, and potential restoration of the St. Francis’ Satyr butterfly. Report to the Endangered Species Branch, Ft. Bragg, NCGoogle Scholar
  23. Haddad NM, Hudgens B, Damiani C, Gross K, Kuefler D, Pollock K (2008a) Determining optimal monitoring for rare butterfly populations. Conserv Biol 22:929–940PubMedCrossRefGoogle Scholar
  24. Haddad N, Vogel L, Wilson J, Bartel R, Hudgens B, Mortell Q (2008b) Research for the conservation and restoration of an endangered butterfly, the St. Francis Satyr. Report to Ft. Bragg Endangered Species Branch Ft. Bragg, NCGoogle Scholar
  25. Hale ML, Lurz PW, Shirley MDF, Rushton S, Fuller RM, Wolff K (2001) Impact of landscape management on the genetic structure of red squirrel populations. Science 293:2246–2248PubMedCrossRefGoogle Scholar
  26. Hall SP (1993) A rangewide status survey of Saint Francis satyr, (Lepidoptera: Nymphalidae). Report to the U.S. Fish and Wildlife Service, Region 6 Endangered Species Office, Asheville, NCGoogle Scholar
  27. Hall SP, Haddad NM (2005) Rearing studies of larval Neonympha mictchellii francisci and N. areolata. Report to the Endangered Species Branch, Ft. Bragg, NCGoogle Scholar
  28. Hall SP, Hoffman EL (1994) Supplement to the rangewide status survey of Saint Francis’ satyr, Neonympha mitchellii francisci, (Lepidoptera: Nymphalidae); 1993 field season. Report to the U.S. Fish and Wildlife Service, Region 6 Endangered Species Office, Asheville, NCGoogle Scholar
  29. Hamm CA, Aggarwal D, Landis DA (2010) Evaluating the impact of non-lethal DNA sampling on two butterflies, Vanessa cardui and Satyrodes eurydice. J Insect Conserv 14:11–18CrossRefGoogle Scholar
  30. Hanski I (1998) Metapopulation dynamics. Nature 396:4149CrossRefGoogle Scholar
  31. Hartl DL, Clark AG (1997) Principles of population genetics, 3rd edn. Sinauer Associates Inc, SunderlandGoogle Scholar
  32. Henningsen, JP, Lance, SL, Jones KL, Hagen C, Laurila J, Cole RA, Perez KE (2010) Development and characterization of 17 polymorphic loci in the faucet snail, Bithynia tentaculata (Gatropoda: Caenogastropoda: Bithyniidae). Conserv Genet Resour. doi:10.1007/s12686-010-9255-9
  33. Hilty J, Lidicker WZ, Merenlender A (2006) Corridor ecology: the science and practice of linking landscapes for biodiversity conservation. Island Press, Washington, DCGoogle Scholar
  34. Huang X, Madan A (1999) CAP3: a DNA sequence assembly program. Genome Res 9:868–877Google Scholar
  35. Jacobsson M, Rosenburg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806CrossRefGoogle Scholar
  36. Keyghobadi N, Roland J, Strobeck C (1999) Influence of landscape on the population genetic structure of the alpine butterfly Parnassius smintheus (Papilonidae). Mol Ecol 8:1481–1495PubMedCrossRefGoogle Scholar
  37. Keyghobadi N, Unger KP, Weintraub JD, Fonseca DM (2006) Remnant populations of the regal fritillary (Speyeria idalia) in Pennsylvania: local genetic structure in a high gene flow species. Conserv Genet 7:309–313CrossRefGoogle Scholar
  38. Kuefler D, Haddad NM, Hall S, Hudgens B, Bartel B, Hoffman E (2008) Distribution, population structure, and habitat use of the endangered St. Francis’ satyr butterfly, Neonympha mitchellii francisci. Am Mid Nat 159:298–320CrossRefGoogle Scholar
  39. Kuefler D, Hudgens B, Haddad NM, Morris WF, Thurgate N (2010) The conflicting role of matrix habitats as conduits and barriers for dispersal. Ecology 91:944–950PubMedCrossRefGoogle Scholar
  40. Lance SL, Light JE, Jones KL, Hagen C, Hafner JC (2010) Isolation and characterization of 17 polymorphic microsatellite loci in the kangaroo mouse, genus Microdipodops (Rodentia: Heteromyidae). Conserv Genet Resour. doi:10.1007/s12686-010-9195-4
  41. Lessig H, Wilson J, Hudgens B, Haddad N (2010) Research for the conservation and restoration of an endangered butterfly, the St. Francis’ satyr. Report to the Endangered Species Branch, Ft. Bragg NCGoogle Scholar
  42. Lushai G, Fjellsted W, Marcovitch O (2000) Application of molecular techniques to non-lethal tissue samples of endangered butterfly populations (Parnassius apollo L.) in Norway for conservation management. Biol Conserv 94:43–50CrossRefGoogle Scholar
  43. Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197CrossRefGoogle Scholar
  44. Mech SG, Hallett JG (2001) Evaluating the effectiveness of corridors: a genetic approach. Conserv Biol 15(2):467–474CrossRefGoogle Scholar
  45. Meglecz E et al (2007) Microsatellite flanking region similarities among different loci within insect species. Insect Mol Biol 16:175–185PubMedCrossRefGoogle Scholar
  46. Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Nat Acad Sci 70:3321–3323PubMedCrossRefGoogle Scholar
  47. New TR (1991) Butterfly conservation. Oxford University Press, OxfordGoogle Scholar
  48. Paetkau D, Slade R, Burden M, Estoup A (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65PubMedCrossRefGoogle Scholar
  49. Peterson MA, Denno RF (1998) The influence of dispersal and diet breadth on patterns of genetic isolation by distance in phytophagous insects. Am Nat 152:428–446Google Scholar
  50. Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GeneClass2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539PubMedCrossRefGoogle Scholar
  51. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  52. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  53. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138CrossRefGoogle Scholar
  54. Rousset F (2008) GENEPOP ‘007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106PubMedCrossRefGoogle Scholar
  55. Saastamoinen M, Hanski I (2008) Genotypic and environmental effects on flight activity and oviposition in the Glanville fritillary butterfly. Am Nat 171:701–712PubMedCrossRefGoogle Scholar
  56. Slatkin M (1985) Rare alleles as indicators of gene flow. Evolution 39:53–65CrossRefGoogle Scholar
  57. Stevens VM, Verkenne C, Vandenwoestijne S, Wesselingh RA, Baguette M (2006) Gene flow and functional connectivity in the natterjack toad. Mol Ecol 15:2333–2344PubMedCrossRefGoogle Scholar
  58. Storfer A (1999) Gene flow and endangered species translocations: a topic revisited. Biol Conserv 87:173–180CrossRefGoogle Scholar
  59. Sutcliffe OL, Thomas CD (1996) Open corridors appear to facilitate dispersal by ringlet butterflies (Aphantopus hyperantus) between woodland clearings. Conserv Biol 10:1359–1365CrossRefGoogle Scholar
  60. Wilcove DS, Rothstein D, Dubow J, Phillips A, Losos E (1998) Quantifying threats to imperiled species in the United States. Bioscience 48:607–615CrossRefGoogle Scholar
  61. Wilkins JF, Wakeley J (2002) The coalescent in a continuous, finite, linear populations. Genetics 161:873–888PubMedGoogle Scholar
  62. Wright S (1951) The genetic structure of populations. Ann Eugen 15:323–354Google Scholar
  63. Zhang D (2004) Lepidopteran microsatellite DNA: redundant but promising. Trends Ecol Evol 19:507–509PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Laura V. Milko
    • 1
  • Nick M. Haddad
    • 1
  • Stacey L. Lance
    • 2
  1. 1.Department of BiologyNorth Carolina State UniversityRaleighUSA
  2. 2.Savannah River Ecology LaboratoryUniversity of GeorgiaAikenUSA

Personalised recommendations