Skip to main content

Advertisement

SpringerLink
Log in

Genetic diversity of Parides ascanius (Lepidoptera: Papilionidae: Troidini): implications for the conservation of Brazil’s most iconic endangered invertebrate species

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Parides ascanius (Lepidoptera: Papilionidae) is a butterfly endemic to the sand forests (“restingas”) of one of the most populated areas of Brazil (from Rio de Janeiro state to South Espírito Santo state), and was the first invertebrate officially recognized as being threatened in Brazil. Here we present a panel of eight polymorphic microsatellite loci and partial sequences of mitochondrial gene COI aiming to characterize this butterfly’s genetic diversity and understand its distribution among the extant populations. We estimate FST metrics, migration rates, cluster assignment, and spatial structure of genetic diversity. FST and statistics indicate low genetic structure and no evidence for endogamy, with all populations connected by high migration rates. Seven populations have low permanence rates (68–75 %) with increased migration probabilities for all populations. One population displays higher permanence rate (87.7 %), as the metropolitan matrix isolates it. Spatial analysis shows a global structure around the city of Rio de Janeiro and the Guanabara Bay; assignment analysis recovers six clusters evenly spread among sampled populations. These findings are consistent with a natural scenario of metapopulation dynamics for P. ascanius, with low genetic diversity and no endogamy, but progressively isolated by the metropolitan matrix. Conservation efforts should focus in connecting the isolated population, broaden the searches for new populations, and preserve all extant habitat patches where P. ascanius still occurs.

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
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Blackwell Publishing, Oxford

    Google Scholar 

  • Billotte N, Lagoda PJL, Risterucci AM, Baurens FC (1999) Microsatellite-enriched libraries: applied methodology for the development of SSR markers in tropical crops. Fruits 54:277–288

    CAS  Google Scholar 

  • Bogdanowicz SM, Wallner WE, Bell J et al (1993) Asian gypsy moths (Lepidoptera: Lymantriidae) in North America: evidence from molecular data. Ann Entomol Soc Am 86:710–715. doi:10.1093/aesa/86.6.710

    Article  CAS  Google Scholar 

  • Brown KS Jr, Brown GG (1992) Habitat alteration and species loss in Brazilian forests. In: Whitmore TC, Sayer JA (eds) Tropical deforestation and species extinction. Boom Koninklijke Uitgevers, Barneveld

    Google Scholar 

  • Brown KS Jr, Freitas AVL (2002) Butterfly communities of urban forest fragments in Campinas, São Paulo, Brazil: structure, instability, environmental correlates, and conservation. J Insect Conserv 6:217–231. doi:10.1023/A:1024462523826

    Article  Google Scholar 

  • Brown KSJ, Damman AJ, Feeny P (1981) Troidine swallowtails (Lepidoptera: Papilionidae) in southeastern Brazil: natural history and foodplant relationships. J Res Lepid 19:199–226

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Dewoody J, Nason JD, Hipkins VD (2006) Mitigating scoring errors in microsatellite data from wild populations. Mol Ecol Notes 6:951–957. doi:10.1111/j.1471-8286.2006.01449.x

    Article  CAS  Google Scholar 

  • Earl DA, vonHoldt BM (2011) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. doi:10.1007/s12686-011-9548-7

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620. doi:10.1111/j.1365-294X.2005.02553.x

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. doi:10.1111/j.1755-0998.2010.02847.x

    Article  PubMed  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among dna haplotypes—application to human mitochondrial-dna restriction data. Genetics 131:479–491

    CAS  PubMed  PubMed Central  Google Scholar 

  • Folmer O, Black M, Hoeh W et al (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    CAS  PubMed  Google Scholar 

  • Freitas A, Marini-Filho O. J (2011) Plano de açao nacional para conservaçao dos lepidópteros ameaçados de extinçao. Instituto Chico Mendes de Conservação da Biodiversidade

  • Freitas AVL, Ramos RR (2001) Population biology of Parides anchises nephalion (Papilionidae) in a coastal site in Southeast Brazil. Braz J Biol 61:623–630. doi:10.1590/S1519-69842001000400011

    Article  CAS  PubMed  Google Scholar 

  • Gimenez Dixon M (1996) The IUCN red list of threatened species. IUCN, Gland

    Google Scholar 

  • Goudet J (2005) hierfstat, a package for r to compute and test hierarchical F-statistics. Mol Ecol Notes 5:184–186. doi:10.1111/j.1471-8286.2004.00828.x

    Article  Google Scholar 

  • Habel JC, Schmitt T, Meyer M et al (2010) Biogeography meets conservation: the genetic structure of the endangered lycaenid butterfly Lycaena helle (Denis & Schiffermüller, 1775). Biol J Linn Soc 101:155–168. doi:10.1111/j.1095-8312.2010.01471.x

    Article  Google Scholar 

  • Herkenhoff EV, Monteiro RF, Esperanço AP (2013) Population biology of the endangered fluminense swallowtail butterfly Parides ascanius (Papilionidae: Papilioninae: Troidini). J Lepid Soc 67:29–34

    Google Scholar 

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806. doi:10.1093/bioinformatics/btm233

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. doi:10.1093/bioinformatics/btn129

    Article  CAS  PubMed  Google Scholar 

  • Jombart T, Devillard S, Dufour A-B, Pontier D (2008) Revealing cryptic spatial patterns in genetic variability by a new multivariate method. Heredity (Edinb) 101:92–103. doi:10.1038/hdy.2008.34

    Article  CAS  Google Scholar 

  • Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94. doi:10.1186/1471-2156-11-94

    Article  PubMed  PubMed Central  Google Scholar 

  • Kearse M, Moir R, Wilson A et al (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. doi:10.1093/bioinformatics/bts199

    Article  PubMed  PubMed Central  Google Scholar 

  • Leal CG, de Gusmão Câmara I (2003) The Atlantic Forest of South America: biodiversity status, threats, and outlook. Island Press, Washington, DC

    Google Scholar 

  • Marques MCM, Swaine MD, Liebsch D (2011) Diversity distribution and floristic differentiation of the coastal lowland vegetation: implications for the conservation of the Brazilian Atlantic Forest. Biodivers Conserv 20:153–168. doi:10.1007/s10531-010-9952-4

    Article  Google Scholar 

  • Meglécz E, Solignac M (1998) Microsatellite Loci for Parnassius mnemosyne (Lepidoptera). Hereditas 128:179–180. doi:10.1111/j.1601-5223.1998.00179.x

    Article  Google Scholar 

  • Meglécz E, Petenian F, Danchin E et al (2004) High similarity between flanking regions of different microsatellites detected within each of two species of Lepidoptera: Parnassius apollo and Euphydryas aurinia. Mol Ecol 13:1693–1700. doi:10.1111/j.1365-294X.2004.02163.x

    Article  PubMed  Google Scholar 

  • Moran P (1948) The interpretation of statistical maps. J Roy Stat Soc B 10:243–251

    Google Scholar 

  • Moran PAP (1950) Notes on continuous stochastic phenomena. Biometrika 37:17–23. doi:10.1093/biomet/37.1-2.17

    Article  CAS  PubMed  Google Scholar 

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

  • Otero LS, Brown KS Jr (1986) Biology and ecology of Parides ascanius (Cramer, 1775) (Lep., Papilionidae), a primitive butterfly threatened with extinction. Atala 10–12:2–16

    Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research–an update. Bioinformatics 28:2537–2539. doi:10.1093/bioinformatics/bts460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Plummer M, Best N, Cowles K, Vines K (2006) CODA: convergence diagnosis and output analysis for MCMC. R News 6:7–11

    Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pritchard JK, Wen X, Falush D (2010) Documentation for structure software: Version 2.3

  • R Core Team (2014) R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Available at http://cran.r-project.org

  • Rambaut A, Suchard MA, Xie W, Drummond A (2014) Tracer, v1.6

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

    Google Scholar 

  • Ribeiro DB, Freitas AVL (2014) Brazil’s new laws bug collectors. Science 345:1571. doi:10.1126/science

    Article  CAS  PubMed  Google Scholar 

  • Ribeiro MC, Metzger JP, Martensen AC et al (2009) The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv 142:1141–1153. doi:10.1016/j.biocon.2009.02.021

    Article  Google Scholar 

  • Rocha CFD, Bergallo HG, Van Sluys M et al (2007) The remnants of restinga habitats in the brazilian Atlantic Forest of Rio de Janeiro state, Brazil: habitat loss and risk of disappearance. Braz J Biol 67:263–273

    Article  CAS  PubMed  Google Scholar 

  • Rosenberg NA (2004) distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138. doi:10.1046/j.1471-8286.2003.00566.x

    Article  Google Scholar 

  • Rousset F (2008) genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106. doi:10.1111/j.1471-8286.2007.01931.x

    Article  PubMed  Google Scholar 

  • Schoville SD, Lam AW, Roderick GK (2012) A range-wide genetic bottleneck overwhelms contemporary landscape factors and local abundance in shaping genetic patterns of an alpine butterfly (Lepidoptera: Pieridae: Colias behrii). Mol Ecol 21:4242–4256. doi:10.1111/j.1365-294X.2012.05696.x

    Article  PubMed  Google Scholar 

  • Sielezniew M, Rutkowski R (2011) Population isolation rather than ecological variation explains the genetic structure of endangered myrmecophilous butterfly Phengaris (=Maculinea) arion. J Insect Conserv 16:39–50. doi:10.1007/s10841-011-9392-9

    Article  Google Scholar 

  • Sinama M, Dubut V, Costedoat C, Gilles A (2011) Challenges of microsatellite development in Lepidoptera: Euphydryas aurinia (Nymphalidae) as a case study. Eur J Entomol 108:261–266

    Article  Google Scholar 

  • Soares A, Bizarro J, Bastos CB (2011) Preliminary analysis of the diurnal Lepidoptera fauna of the Três Picos State Park, Rio de Janeiro, Brazil, with a note on Parides ascanius (Cramer, 1775). Trop Lepid Res 21:66–79

    Google Scholar 

  • Tay W, Behere GT, Batterham P, Heckel DG (2010) Generation of microsatellite repeat families by RTE retrotransposons in lepidopteran genomes. BMC Evol Biol 10:144–146. doi:10.1186/1471-2148-10-144

    Article  PubMed  PubMed Central  Google Scholar 

  • Tyler HA, Brown KS, Wilson KH (1994) Swallowtail butterflies of the Americas: a study in biological dynam- ics, ecological diversity, biosystematics, and conservation. ScientiÞc Publishers, Gainesville

    Google Scholar 

  • Uehara-Prado M, Fonseca RL (2007) Urbanization and mismatch with protected areas place the conservation of a threatened species at risk. Biotropica 39:264–268. doi:10.1111/j.1744-7429.2006.00260.x

    Article  Google Scholar 

  • Ugelvig LV, Andersen A, Boomsma JJ, Nash DR (2012) Dispersal and gene flow in the rare, parasitic Large Blue butterfly Maculinea arion. Mol Ecol 21:3224–3236. doi:10.1111/j.1365-294X.2012.05592.x

    Article  CAS  PubMed  Google Scholar 

  • Untergasser A, Nijveen H, Rao X et al (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35:W71–W74. doi:10.1093/nar/gkm306

    Article  PubMed  PubMed Central  Google Scholar 

  • van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538. doi:10.1111/j.1471-8286.2004.00684.x

    Article  Google Scholar 

  • Weir BS (1996) Genetic data analysis II: methods for discrete population genetic data (Sinauer. Massachusetts, Sunderland

    Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population-structure. Evolution 38:1358–1370. doi:10.2307/2408641

    Article  Google Scholar 

  • Whitlock MC (2004) Selection and drift in metapopulations. In: Hanski I, Gaggiotti OE (eds) Ecology, genetics, and evolution of metapopulations. Academic Press, San Diego, pp 153–173

    Chapter  Google Scholar 

  • Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191

    PubMed  PubMed Central  Google Scholar 

  • Zhang D-X (2004) Lepidopteran microsatellite DNA: redundant but promising. Trends Ecol Evol 19:507–509. doi:10.1016/j.tree.2004.07.020

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Juan Pablo Torres Florez and Leila Shirai for contributions to the manuscript. NS thanks CNPq scholarship (141254/2013-0) and CAPES (3700/14-3), RFM thanks CNPq, CAPES, FAPESP, INCT, HYMPAR SUDESTE, FAPERJ and Instituto Chico Mendes-ICMBio (38024-3), GSSA thanks Secretaria do Meio Ambiente do Rio de Janeiro, Ministério do Meio Ambiente do Brasil, and the Brazilian Army for authorization for sampling, APS thanks FAPESP (2008/52197-4) and CNPq, AVLF thanks BIOTA/FAPESP (2011/50225-3), CNPq (302585/2011-7) and the National Science Foundation (DEB-1256742). This publication is part of the RedeLep “Rede Nacional de Pesquisa e Conservação de Lepidópteros” SISBIOTA-Brasil/CNPq (563332/2010-7).

Funding

Seraphim, N: Conselho Nacional de Desenvolvimento Científico e Tecnológico, Brazil, Grant Number 141254/2013-0; and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brazil, Grant Number 3700/14-3. Souza, AP: Fundação de Amparo à Pesquisa do Estado de São Paulo, Brazil, Grant Number: 2008/52197-4. Freitas, AVL: Fundação de Amparo à Pesquisa do Estado de São Paulo, Brazil, Grant from BIOTA/FAPESP Number 2011/50225-3.

Author information

Author notes

  1. N. Seraphim

    Present address: Institudo Federal de Educação, Ciência e Tecnologia de São Paulo, Campus Capivari, Avenida Dr Ênio Pires de Camargo, 2971, Capivari, SP, CEP 13360-000, Brazil

Authors and Affiliations

  1. Departamento de Biologia Animal, Instituto de Biologia, Universidade Estadual de Campinas (UNICAMP), Cidade Universitária Zeferino Vaz, Caixa postal 6109, Barão Geraldo, Campinas, SP, 13083-970, Brazil

    N. Seraphim & A. V. L. Freitas

  2. Centro de Biologia Molecular e Engenharia Genética, Universidade Estadual de Campinas (UNICAMP), Cidade Universitária Zeferino Vaz, Barão Geraldo, Campinas, SP, 13083-875, Brazil

    M. A. Barreto & A. P. Souza

  3. Departamento de Biologia Geral, Instituto de Biologia, Universidade Federal Fluminense, Caixa Postal 100.436, CEP: 24020-971, Niterói, RJ, CEP 24020-150, Brazil

    G. S. S. Almeida

  4. Laboratório de Ecologia de Insetos, Departamento Ecologia, Instituto de Biologia, Universidade Federal do Rio de Janeiro, CP68020, Rio de Janeiro, RJ, CEP 21941-590, Brazil

    A. P. Esperanço & R. F. Monteiro

  5. Departamento de Biologia Vegetal, Instituto de Biologia, Universidade Estadual de Campinas (UNICAMP), Cidade Universitária Zeferino Vaz, Caixa postal 6109, Barão Geraldo, Campinas, SP, 13083-970, Brazil

    A. P. Souza

  6. Laboratório de Melhoramento de Plantas, Centro de Energia Nuclear na Agricultura, Universidade de São Paulo, Campus “Luiz de Queiroz”. Av. Centenário, 303, Piracicaba, SP, 13400-970, Brazil

    K. L. Silva-Brandão

Authors
  1. N. Seraphim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. A. Barreto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. G. S. S. Almeida
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. P. Esperanço
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. R. F. Monteiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. A. P. Souza
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. A. V. L. Freitas
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. K. L. Silva-Brandão
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to N. Seraphim.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (EPS 619 kb)

Supplementary material 2 (DOCX 48 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Seraphim, N., Barreto, M.A., Almeida, G.S.S. et al. Genetic diversity of Parides ascanius (Lepidoptera: Papilionidae: Troidini): implications for the conservation of Brazil’s most iconic endangered invertebrate species. Conserv Genet 17, 533–546 (2016). https://doi.org/10.1007/s10592-015-0802-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-015-0802-5

Keywords

Search

Navigation