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Conservation Genetics and Species Status of an Endangered Australian Dragon, Tympanocryptis Pinguicolla (Reptilia: Agamidae)

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Conservation Genetics and Species Status of an Endangered Australian Dragon, Tympanocryptis Pinguicolla (Reptilia: Agamidae) Conserv Genet (2007) 8:185–195 DOI 10.1007/s10592-006-9161-6 ORIGINAL PAPER Conservation genetics and species status of an endangered Australian dragon, Tympanocryptis pinguicolla (Reptilia: Agamidae) Jane Melville Æ Stephanie Goebel Æ Carly Starr Æ J. Scott Keogh Æ Jeremy J. Austin Received: 2 November 2005 / Accepted: 19 April 2006 / Published online: 28 September 2006 Ó Springer Science+Business Media B.V. 2006 Abstract We present a phylogenetic and morpho- and eight tRNA genes. We incorporated specialized logical study of the grassland earless dragon, Tym- degraded-DNA techniques to amplify DNA from his- panocryptis pinguicolla, an endangered habitat torical museum specimens, as no extant tissue was specialist that occurs in a few isolated populations in available for Victorian populations. Our results, which eastern Australia. Tympanocryptis pinguicolla oc- include morphological analysis, provide convincing curred historically in Victoria in south-eastern Aus- evidence that populations currently identified as tralia, but has not been seen since 1990, and current T. pinguicolla do not comprise a monophyletic species, populations are known in New South Wales and as the populations from the Darling Downs are more Canberra in south-eastern Australia. Recently, new closely related to T. tetraporophora than to T. pingui- populations identified as T. pinguicolla were discov- colla. In addition, we find that there is a significant ered on the Darling Downs, Queensland. Transloca- level of haplotype divergence between populations of tion of individuals between these populations has been T. pinguicolla, indicating that these lineages separated suggested as a conservation management strategy to at least 1.5 mya. Our results suggest translocation may maintain genetic diversity. To address this issue, we not be an appropriate management strategy and our undertook a phylogenetic study of all major popula- findings that Darling Downs populations are not tions of T. pinguicolla using a 1838 bp region of T. pinguicolla will significantly influence the conser- mitochondrial DNA, incorporating ND1, ND2, COI vation management of this species in Queensland. Keywords Agamidae Æ Genetic diversity Æ Haplotype J. Melville (&) Æ J. J. Austin divergence Æ Historical biogeography Æ Reptiles Department of Sciences, Museum Victoria, Melbourne, VIC 3000, Australia e-mail: [email protected] Introduction S. Goebel School of Natural and Rural Systems Management, Prior to European settlement in the late 1700’s, there University of Queensland, Gatton, QLD 4343, Australia were extensive areas of native grasslands in south- C. Starr eastern Australia (Fig. 1) but in the last two centuries School of Animal Studies, University of Queensland, they have diminished significantly due to agriculture Gatton, QLD 4343, Australia and urbanization (Driscoll and Hardy 2005). Areas of J. S. Keogh remnant native grasslands are found around eastern School of Botany and Zoology, The Australian National Australia’s largest cities but are highly modified and University, Canberra, ACT 2000, Australia fragmented. For example, west of Melbourne the Western Plains Grassland is recognized as one of the J. J. Austin School of Earth and Environmental Sciences, University of most endangered vegetation communities in the state Adelaide, Adelaide, SA 5005, Australia of Victoria (Stuwe 1986; Frood and Calder 1987). 123 186 Conserv Genet (2007) 8:185–195 Fig. 1 Map of Australia’s eastern states: Queensland (QLD); New South Wales (NSW); and Victoria (Vic). Estimated distribution of temperate lowland grasslands prior to European settlement (circa. 1770) are indicated by stippled areas enclosed by dotted lines (Lunt 1995). Distribution of current ()) and historical (n) populations of Tympanocryptis pinguicolla are provided (Robertson and Cooper 2000) Many of the vertebrate species that occur in Australia’s population genetic structure of a species is essential temperate grasslands, such as legless lizards, small prior to the initiation of any translocation conservation marsupials and grassland birds, are habitat specialists program. We investigate these concepts with a small and restricted to grasslands (Stuwe 1986). This spe- earless dragon, Tympanocryptis pinguicolla, from the cialization means that as grasslands become increas- temperate grasslands of south-eastern Australia. ingly fragmented, many populations will become Tympanocryptis pinguicolla is a habitat specialist, isolated, diminish in size and be at increased risk of occurring only in grasslands and using spider burrows as localized extinction. retreat sites (Smith et al. 1999; Scott and Keogh 2000). Translocation of individuals between fragmented The dramatic reduction in native grasslands has meant populations in species that once had more continuous that suitable habitat for T. pinguicolla has greatly distributions is a commonly cited method to counteract diminished and the species is now formally listed as the deleterious effects of habitat and population frag- endangered throughout its range (Robertson and mentation (Frankham et al. 2002). However, without Cooper 2000). In Victoria, five sightings believed to be prior knowledge of the genetic structure of species, this species were reported between 1988 and 1990 but there is a risk of drastically altering the genetic struc- none since, while approximately 500 kms north in New ture of populations and potentially altering the evolu- South Wales (NSW) and Canberra the species survives tionary course of a species (Moritz 2002). Thus, in only a few locations (Fig. 1). In 2001 an individual detailed knowledge of the phylogeography and identified as T. pinguicolla was captured on the Darling 123 Conserv Genet (2007) 8:185–195 187 Downs, Queensland (QLD), which is more than Of three specimens sampled from Museum Victoria, 1000 km north of the populations in Canberra and NSW. one yielded viable DNA using specialized techniques Since then a number of new populations have been lo- described below. All other samples of T. pinguicolla cated in the Darling Downs (QLD) region (Hobson used in this study were tail tips or toe clips collected 2002; Starr and Leung 2005). Due to the highly frag- during field surveys. Our analyses also included 16 mented nature of these remaining populations, which previously published sequences (Appendix 1: Melville precludes gene flow among them, it has been suggested et al. 2001; Schulte et al. 2003). that translocation of individuals may be a viable option Animals used for the morphological analysis were to avoid inbreeding and loss of genetic diversity (Rob- processed at the Queensland Museum. A total of 18 ertson and Cooper 2000). However, a preliminary specimens of T. pinguicolla from museum collections molecular study (Scott and Keogh 2000) of the NSW and were used: seven from the Darling Downs, QLD and Canberra populations suggested a significant level of eleven from Canberra/NSW (Appendix 1). In addition, genetic divergence (>5%) over relatively small geo- 13 live specimens were collected from private property graphic scales, which pre-dates European settlement from known populations of T. pinguicolla at Bongeen and subsequent habitat reductions. on the Darling Downs, QLD. We undertook a phylogenetic study of all known populations of Tympanocryptis pinguicolla to deter- Morphological measurements and data analysis mine the extent of genetic divergence, with particular emphasis on the recently discovered populations from Eighteen morphological measurements and meristic the Darling Downs (QLD) and extirpated populations counts were collected for all specimens using 0– in Victoria. An additional seven species of Tympano- 200 mm Digital Vernier calipers (Scientific Instrument cryptis and two outgroup taxa are included in the and Optical sales). Morphological measurements in- analysis. Sequences reported include a 1838 base-pair cluded: snout-vent length (SVL), tail length (TL), head (bp) segment of the mitochondrial genome spanning length (HL), head width (HW), head depth (HD), the ND1, ND2 and COI genes and intervening tRNA axilla – groin length (AG), fore limb length (FLL), genes. As no extant tissue samples were available for hind limb length (HLL), width of enlarged dorsal spi- Victorian populations of T. pinguicolla, we use spe- nous scales (SSW), length of enlarged dorsal spinous cialized degraded-DNA techniques on spirit-preserved scales (SSL), number of inter-nasals (IN), number of museum specimens to provide a 331 bp section of the infralabials (IL), number of supralabials (SL), number ND2 protein-coding gene for analysis. We also incor- of scales between nasal and supralabial (NL), number porated a morphological analysis of populations from of spinous scales between axilla and groin (AXG), the Darling Downs in Queensland and Canberra/NSW number of enlarged dorsal spinous scales (DSS), to determine whether phylogenetic divergences are number of preanal pores (PP), and number of femoral supported by distinguishable morphological characters. pores (FP). In addition, we test hypotheses concerning the phylo- The differences between populations were analyzed genetic relationships and species status of T. pingui- using an analysis of variance (ANOVA). Due to the colla populations. unbalanced nature of the data (due to unequal num- bers of animals in each population/location) a general linear regression approach was used. Pair-wise com- Materials and methods parisons were used to identify significant terms using a t-test. The relationship between morphological
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