Conservation Genetics

, Volume 17, Issue 4, pp 761–774 | Cite as

How many conservation units are there for the endangered grassland earless dragons?

  • Emma Carlson
  • Anna J. MacDonald
  • Aaron Adamack
  • Tim McGrath
  • Lisa I. Doucette
  • William S. Osborne
  • Bernd Gruber
  • Stephen D. Sarre
Research Article

Abstract

Species are the most commonly recognised unit for conservation management, yet significant variation can exist below the level of taxonomic recognition and there is a lack of consensus around how a species might be defined. This definition has particular relevance when species designations are used to apportion conservation effort and when definitions might be made through legislation. Here, we use microsatellite DNA analyses to test the proposition that the last remaining populations of the endangered grassland earless dragon (Tympanocryptis pinguicolla) harbour substantial cryptic genetic variation. Our study provides strong evidence that long historical isolation and the recent impacts of urbanization, have led to genetic differentiation in microsatellite DNA allele frequencies and high numbers of private alleles among three genetic clusters. This differentiation is partially concordant with previous mitochondrial DNA analyses, which show the two regions (Canberra and Monaro) where this species exists, to be reciprocally monophyletic, but differs through the identification of a third genetic cluster that splits a northern Canberra cluster from that of southern Canberra. Our data also identify a stark contrast in population genetic structure between clusters such that high levels of genetic structure are evident in the highly urbanised Canberra region but not in the largely rural Monaro region. We conclude that this species, like many reptiles, harbours considerable cryptic variation and currently comprises three distinct and discrete units. These units could be classified as separate species for the purpose of conservation under the relevant Australian and international Acts drawing management appropriate to that status.

Keywords

Conservation units Evolutionary significant units Microsatellite DNA Temperate grasslands 

Supplementary material

10592_2016_819_MOESM1_ESM.pdf (342 kb)
Supplementary material 1 (PDF 341 kb) Supplementary Fig. 1: Estimates of average pairwise relatedness within Canberra and Monaro sampling sites for T. pinguicolla. Sites with 2 individuals or less are not included. A value of 0.5 indicates a parent-sibling or full sibling relationship, 0.25 indicates half-siblings and below 0.125 indicates unrelated individuals (Queller and Goodnight 1989). Supplementary Fig. 2: STRUCTURE analysis pathway for the admixed with popinfo STRUCTURE runs. The initial data set consisted of 190 individuals. Following each STRUCTURE run, STRUCTURE harvester was run on the results to identify the number of likely clusters. We then examined plots of individual cluster assignments for consistency across the 20 replicate runs and spatial plots of cluster assignments for genographic consistency. Once the number of clusters had been determined, individuals were placed into sub-cluster and the analysis was repeated for the sub-cluster until no further sub-clustering was detected. QNR/Pop. = Queanbeyan Nature Reserve/. Supplementary Fig. 3: STRUCTURE analysis pathway for the no admixture without popinfo STRUCTURE runs. The initial data set consisted of 190 individuals. Following each STRUCTURE run, STRUCTURE harvester was run on the results to identify the number of likely clusters. We then examined plots of individual cluster assignments for consistency across the 20 replicate runs and spatial plots of cluster assignments for genographic consistency. Once the number of clusters had been determined, individuals were placed into sub-cluster and the analysis was repeated for the sub-cluster until no further sub-clustering was detected
10592_2016_819_MOESM2_ESM.pdf (15 kb)
Supplementary material 2 (PDF 14 kb) Supplementary Fig. 4: Supplemental Figure XXX Deviance information criterion (DIC) plot for each replicate of K (replicates = 20) for K = 2 to 10 (grey points). Durand et al. (2009) recommend examining the DIC values of the lowest 10 to 20 % of replicate values for each K in order to identify the ideal number of clusters as the K value at which DIC values plateau. The average value of the lowest 20 % of DIC values for each K is indicated using red points

References

  1. Adamack AT, Gruber B (2014) Pop gen report : simplifying basic population genetic analyses in R. Methods Ecol Evol 5:384–387. doi:10.1111/2041-210X.12158 CrossRefGoogle Scholar
  2. Anon (2015) EPBC Act list of threatened fauna. In: species profile threat. Database. http://www.environment.gov.au/cgi-bin/sprat/public/publicthreatenedlist.pl?wanted=fauna. Accessed 29 Oct 2015
  3. Benson J (1994) The native grasslands of the Monaro region: Southern Tablelands of NSW. Cunninghamia 3:609–650Google Scholar
  4. Berry O, Tocher MD, Gleeson DM, Sarre SD (2005) Effect of vegetation matrix on animal dispersal: genetic evidence from a study of endangered skinks. Conserv Biol 19:1–10CrossRefGoogle Scholar
  5. Blair C, Weigel DE, Balazik M et al (2012) A simulation-based evaluation of methods for inferring linear barriers to gene flow. Mol Ecol Resour 12:822–833. doi:10.1111/j.1755-0998.2012.03151.x CrossRefPubMedGoogle Scholar
  6. Chen C, Durand E, Forbes F, François O (2007) Bayesian clustering algorithms ascertaining spatial population structure: a new computer program and a comparison study. Mol Ecol Notes 7:747–756. doi:10.1111/j.1471-8286.2007.01769.x CrossRefGoogle Scholar
  7. de Queiroz K (2005) Different species problems and their resolution. BioEssays 27:1263–1269. doi:10.1002/bies.20325 CrossRefPubMedGoogle Scholar
  8. Dimond WJ, Osborne WIS, Evans MC et al (2012) Back to the brink: population decline of the endangered grassland earless dragon (Tympanocryptis pinguicolla) following its rediscovery. Conserv Genet 7:132–149Google Scholar
  9. Driscoll DA, Hardy CM (2005) Dispersal and phylogeography of the agamid lizard Amphibolurus nobbi in fragmented and continuous habitat. Mol Ecol 14:1613–1629. doi:10.1111/j.1365-294X.2005.02509.x CrossRefPubMedGoogle Scholar
  10. Durand E, Chen C, Francois O (2009) TESS version 2.3—reference manual. http://membrestimc.imag.fr/Olivier.Francois/tess.html
  11. Earl DA, VonHoldt BM (2012) 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 CrossRefGoogle Scholar
  12. 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 CrossRefPubMedGoogle Scholar
  13. Frankham R (2010) Challenges and opportunities of genetic approaches to biological conservation. Biol Conserv 143:1919–1927. doi:10.1016/j.biocon.2010.05.011 CrossRefGoogle Scholar
  14. Hayward MW (2009) The need to rationalize and prioritize threatening processes used to determine threat status in the IUCN Red List. Conserv Biol 23:1568–1576. doi:10.1111/j.1523-1739.2009.01260.x CrossRefPubMedGoogle Scholar
  15. Hoehn M, Sarre SD, Henle K (2007) The tales of two geckos: does dispersal prevent extinction in recently fragmented populations? Mol Ecol 16:3299–3312. doi:10.1111/j.1365-294X.2007.03352.x CrossRefPubMedGoogle Scholar
  16. Hoehn M, Osborne WS, Aitken NA, Sarre SD (2010) Isolation and characterization of 10 tetranucleotide microsatellites in the Grassland Earless Dragon (Tympanocryptis pinguicolla). Conserv Genet Resour 2:372–375. doi:10.1007/s12686-010-9259-5 CrossRefGoogle Scholar
  17. Hoehn M, Dimond W, Osborne W, Sarre SD (2013) Genetic analysis reveals the costs of peri-urban development for the endangered grassland earless dragon. Conserv Genet 14:1269–1278. doi:10.1007/s10592-013-0515-6 CrossRefGoogle Scholar
  18. Hurston H, Voith L, Bonanno J et al (2009) Effects of fragmentation on genetic diversity in island populations of the Aegean wall lizard Podarcis erhardii (Lacertidae, Reptilia). Mol Phylogenet Evol 52:395–405. doi:10.1016/j.ympev.2009.03.028 CrossRefPubMedGoogle Scholar
  19. IUCN (2014) The IUCN Red List of Threatened Species. In: IUCN Red List Threat. Species. Version 2014.1. http://www.iucnredlist.org
  20. Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405CrossRefPubMedGoogle Scholar
  21. Jombart T, Collins C (2015) A tutorial for discriminant analysis of principal components (DAPC) using adegenet 2.0.0. http://adegenet.r-forge.r-project.org/files/tutorial-dapc.pdf published 23 June 2015
  22. Jombart T, Pontier D, Dufour A-B (2009) Genetic markers in the playground of multivariate analysis. Heredity 102:330–341CrossRefPubMedGoogle Scholar
  23. Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal component: a new method for the analysis of genetically structured populations. BMC Genet 11:94. doi:10.1186/1471-2156-11-94 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Kosman E, Leonard KJ (2005) Similarity coefficients for molecular markers in studies of genetic relationships between individuals for haploid, diploid, and polyploid species. Mol Ecol 14:415–424. doi:10.1111/j.1365-294X.2005.02416.x CrossRefPubMedGoogle Scholar
  25. Macdonald AJ, Sarre SD, Fitzsimmons NN, Aitken N (2011) Determining microsatellite genotyping reliability and mutation detection ability: an approach using small-pool PCR from sperm DNA. Mol Genet Genomics 285:1–18. doi:10.1007/s00438-010-0577-9 CrossRefPubMedGoogle Scholar
  26. McGrath T, Gurutzeta G, Lahoz-Monfortb JJ et al (2015) Accounting for detectability when surveying for rare or declining reptiles: turning over rocks to find the Grassland Earless Dragon in Australia. Biol Conserv 182:53–62CrossRefGoogle Scholar
  27. Melville J, Goebel S, Starr C et al (2007) Conservation genetics and species status of an endangered Australian dragon, Tympanocryptis pinguicolla (Reptilia: Agamidae). Conserv Genet 8:185–195. doi:10.1007/s10592-006-9161-6 CrossRefGoogle Scholar
  28. Melville J, Smith K, Hobson R et al (2014) The role of integrative taxonomy in the conservation management of cryptic species: the taxonomic status of endangered earless dragons (agamidae: Tympanocryptis) in the grasslands of Queensland, Australia. PLoS One. doi:10.1371/journal.pone.0101847 Google Scholar
  29. Moritz C (1994) Defining “evolutionarily significant units” for conservation. Trends Ecol Evol 9:373–375CrossRefPubMedGoogle Scholar
  30. Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10CrossRefGoogle Scholar
  31. Padial JM, Miralles A, De la Riva I, Vences M (2010) The integrative future of taxonomy: review. Front Zool 7:16CrossRefPubMedPubMedCentralGoogle Scholar
  32. 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
  33. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  35. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275CrossRefGoogle Scholar
  36. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  37. Robertson P, Evans MC (2009) National recovery plan for the Grassland Earless Dragon (Tympanocryptis pinguicolla)—as varied October 2012. ACT Government, Department of Territory and Municipal Services, CanberraGoogle Scholar
  38. 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 CrossRefPubMedGoogle Scholar
  39. Row JR, Blouin-Demers G, Lougheed SC (2010) Habitat distribution influences dispersal and fine-scale genetic population structure of eastern foxsnakes (Mintonius gloydi) across a fragmented landscape. Mol Ecol 19:5157–5171. doi:10.1111/j.1365-294X.2010.04872.x CrossRefPubMedGoogle Scholar
  40. Ryder OA (1986) Species conservation and systematics: the dilemma of subspecies. Trends Ecol Evol 1:9–10. doi:10.1016/0169-5347(86)90059-5 CrossRefGoogle Scholar
  41. Sarre S (1995) Mitochondrial DNA variation among populations of Oedura reticulata (Gekkonidae) in remnant vegetation: implications for metapopulation structure and population decline. Mol Ecol 4:395–405CrossRefGoogle Scholar
  42. Scott IAW, Keogh JS (2000) Conservation genetics of the endangered grassland earless dragon Tympanocryptis pinguicolla (Reptilia : Agamidae) in Southeastern Australia. Conserv Genet 1:357–363CrossRefGoogle Scholar
  43. Smith W, Osborne WS, Donnellan SC, Cooper PD (1999) The systematic status of earless dragon lizards, Tympanocryptis (Reptilia: Agamidae), in south-eastern Australia. Aust J Zool 47:551–564CrossRefGoogle Scholar
  44. 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 10:867–878CrossRefPubMedGoogle Scholar
  45. Torstrom SM, Pangle KL, Swanson BJ (2014) Shedding subspecies: the influence of genetics on reptile subspecies taxonomy. Mol Phylogenet Evol 76:134–143. doi:10.1016/j.ympev.2014.03.011 CrossRefPubMedGoogle Scholar
  46. 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 CrossRefGoogle Scholar
  47. Waples RS, Nammack M, Cochrane JF, Hutchings JA (2013) A tale of two acts: endangered species listing practices in Canada and the United States. Bioscience 63:723–734. doi:10.1525/bio.2013.63.9.8 CrossRefGoogle Scholar
  48. Winter D (2012) MMOD: an R library for the calculation of population differentiation statistics. Mol Ecol Resour 12:1158–1160CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Institute for Applied EcologyUniversity of CanberraBruceAustralia

Personalised recommendations