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Development of Eleven Polymorphic Microsatellite Loci for the Sea Snake

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Conservation Genet Resour (2012) 4:11–14 DOI 10.1007/s12686-011-9461-0 TECHNICAL NOTE Development of eleven polymorphic microsatellite loci for the sea snake Emydocephalus annulatus (Elapidae: Hydrophiinae) and cross-species amplification for seven species in the sister genus Aipysurus Vimoksalehi Lukoschek • John C. Avise Received: 21 May 2011 / Accepted: 1 June 2011 / Published online: 23 June 2011 Ó Springer Science+Business Media B.V. 2011 Abstract We developed eleven microsatellite loci for the in marine systems hinder significant progress. High-reso- turtleheaded sea snake, Emydocephalus annulatus, from lution molecular markers, such as nuclear microsatellites, partial genomic DNA libraries using a repeat enrichment provide compelling alternatives for addressing critical protocol. Nine loci had high numbers of alleles (11–32) per questions about population genetic structure, gene flow, locus, while the other two loci had six alleles each. All dispersal, effective population sizes and relatedness. eleven loci amplified successfully and were polymorphic True sea snakes comprise two evolutionary lineages: the in six of seven sea snake species from the sister genus Hydrophis and Aipysurus groups (Lukoschek and Keogh Aipysurus, while ten loci amplified successfully for the 2006). Ten highly polymorphic microsatellite loci were seventh species. Based on these highly successful cross- recently developed for the Hydrophis group (Lukoschek amplifications we expect these loci to be useful markers for and Avise 2011); however, only five microsatellite loci evaluating population genetic structure, gene flow, relat- previously had been developed for an Aipysurus group edness and effective population sizes for all Aipysurus species, (Lukoschek et al. 2005) and large-scale genotyping group sea snakes. revealed relatively low polymorphism at most loci (Luko- schek et al. 2008). In order to better understand how con- Keywords Aipysurus Á Emydocephalus Á Bottleneck Á temporary demographic processes have affected genetic Connectivity Á Effective population size Á Sea snake diversity, effective population sizes and dispersal in the Aipysurus group, we aimed to develop highly polymorphic microsatellite loci for population genetic analyses. We Recently published IUCN Red List Assessments for all true targeted Emydocephalus annulatus because previous phy- sea snake species (Elapidae: Hydrophiinae) listed two of the logenies based on morphology (Voris 1977) and molecules 54 species as Critically Endangered (CR) and a third species (Lukoschek and Keogh 2006) consistently supported its as Endangered (IUCN 2010). All three species are from the basal position in the Aipysurus group. genus Aipysurus and all are endemic to a handful of reefs in We employed a modified version of a hybridization the Ashmore Reef region of the Timor Sea, where they have capture protocol using magnetic streptavidin beads and undergone recent precipitous population declines (Guinea biotinylated probes (Hamilton et al. 1999; Hauswaldt and 2007; Lukoschek Unpublished Data). The reasons for these Glenn 2003) to enrich for microsatellites in a genomic declines are unknown and difficulties of direct observation library for E. annulatus. Our protocol followed Lukoschek and Avise (2011). A total of 101 inserts were sequenced and microsatellite repeat regions detected by eye. Primers pairs V. Lukoschek Á J. C. Avise Department of Ecology and Evolutionary Biology, were designed for all 25 inserts containing microsatellites University of California at Irvine, Irvine, CA 92697, USA using OligoAnalyzer 3.0 (Integrated DNA Technologies) and tested on E. annulatus (n = 48). One primer from each & V. Lukoschek ( ) pair was 50 end labeled with a tag (50-GGAAACAGCT ARC Centre of Excellence for Coral Reef Studies, 0 James Cook University, Townsville, QLD 4811, Australia ATGACCATG-3 ) for tailed PCR with an M13 primer e-mail: [email protected] labeled with a 6-FAM, HEX, or NED (Applied Biosystems) 123 12 Conservation Genet Resour (2012) 4:11–14 fluorophore. Eleven microsatellite loci (Table 1), which disequilibrium (LD). MICRO-CHECKER (van Oosterhout amplified consistently and without multiple peaks, were et al. 2004) was used to test for null alleles. screened further. For E. annulatus, nine microsatellite loci had high Polymerase chain reaction (PCR) amplification of numbers of alleles (11–32) per locus, while the other two microsatellite loci were performed following the reaction loci had six alleles each. Eight loci had expected hetero- conditions and thermal cycling protocols described in zygosities (He) C 0.75 (Table 2). All eleven loci amplified Lukoschek and Avise (2011) using the locus specific successfully in six of the seven Aipysurus species while annealing temperatures (Tm) given in Table 1.We only one locus failed in A. pooleorum (Table 2); however screened 225 adult E. annulatus from five Australian and only two A. pooleorum museum samples were screened two New Caledonian locations. Cross-species amplifica- and the DNA was somewhat degraded. Allele sizes and tions were conducted for all seven species in the sister frequency distributions varied considerably among species genus Aipysurus.ForAipysurus laevis we screened 326 (Table 2). individuals from 11 locations throughout its Australian Genotype frequencies for A. laevis from seven locations range, while sample sizes for the remaining six species with n [ 30 were in HWE at P = 0.05 for 74 of the 77 ranged from 2 to 30 (Table 2), typically from one or tests, and the three significant tests (two loci in three two locations per species. Tissue samples were obtained locations) did not remain significant after Bonferroni cor- from biopsy of live snakes, trawler by-catch and museum rection. Moreover, eleven loci were in HWE for A. fuscus collections. Exact tests implemented in GenePop Web at Ashmore Reef (n = 27). Microchecker did not find Version 4.0.10 (Raymond and Rousset 1995; Rousset evidence for null alleles for A. laevis or A. fuscus. Geno- 2008) were used to evaluate whether genotype frequencies type frequencies for E. annulatus departed from HWE in conformed to Hardy–Weinberg equilibrium (HWE) (Guo nine of 44 tests and one locus (Ea478) departed from HWE and Thompson 1992) and whether loci were in linkage in all four locations tested. Three tests remained significant Table 1 Characteristics of eleven microsatellite loci developed for Emydocephalus annulatus Locus Repeat motif Primer sequence (50–30) (F/R) Tm (°C) Expected GenBank product size accession (bp) no. Ea407 (TAGA)12 M13_TCTAACCACTGCACCACCACAGTT 55 168 JF969261 TGTCCATAGTCTGGTGGGCCAAAT Ea823 (GATA)15 M13_AACGTGTGGACTCCAATTCCCAGA 55 168 JF969262 TAGGACTCCAGCTGTTGAGCTATC Ea462 (GAAGA)11(GGAGA)(GAAGA)9 M13_AGCATTCTGTCAAGTGAGGCTCCA 53 397 JF969263 ACGCCACCTGAAGATACCTCAACA Ea820 (CTTT)16(CTTC)(CTTT)3 M13_ATGCGAGGCAAATGACAGTGGTTG 51 380 JF969264 TGGCTGTTCAACTGTTAGCTGGT Ea475 (CT)2GTCTGT(CT)4(GT)5CTGT(CT)4 M13_TCAGTTATTTCTGTGAACTTTG 51 363 JF969265 GT(CT)6GTCTGT (CT)3(GT)2(CT)2 GTTGCAACATAGCGTACCTC GT(CT)6GT(CT)2GT(CT)4GT(CT)6 Ea804 (TG)9(AG)10 M13_GCAAGTTGATGTCTTATCCTTCTCC 57 201 JF969266 TGGACAACAGCTGCTTAGTACAGCTC Ea886 (CTTT)3(CT)4(TTCT)2(AC)(CTTT)2 M13_ACAGGTAGAACAAGCAGTGTGGTC 47 182 JF969267 (CTTC)(TTCC)2 (ATTCTTT) GAGGACTATGATACATGATTGGACA (CCTTCTTT)2(CCTT)5CCCT(CCTT)4 Ea844 (GATA)17 M13_GAGCATATCAGAAACATGGACTGC 55 267 JF969268 CCTATTATCTTGTAAGCAATTGACA Ea478 (TACTC)18 M13_TTCCCACCACTCCTTATCACCCAT 57 446 JF969269 ACTCCTGAGGAAGTAGACAGGAAC Ea841 (TC)10*int*(CTAT)14*int*(TC)3(TG)3 M13_GTTCTGGTTTGTCCACAGCTTTCAG 53 398 JF969270 (TC)4(TG)2(TC)3*int*(T)8(TCTG)4(TC)6 TTGGGATGAGGAGTGATCTTCGGA Ea879 (TC)4(TG)14(TA)2 M13_CGTTTCAGCAGAATCTCATCTGCC 51 179 JF969271 AGCTATGGTTCCGAGCTCTTCACA 123 Conservation Genet Resour (2012) 4:11–14 13 Table 2 Attributes of eleven microsatellite loci developed for Emydocephalus annulatus and the results of cross-species amplification trials for seven sea snake species in the genus Aipysurus Locus Emydocephalus annulatus (N = 225) Aipysurus laevis (N = 326) Size range (bp) N Na Ho He Size range (bp) N Na Ho He Ea407 174–214 219 11 0.64 0.75 174–218 317 12 0.84 0.85 Ea823 169–205 210 16 0.77 0.79 133–161 317 5 0.25 0.24 Ea462 342–452 212 17 0.81 0.88 372–467 312 17 0.86 0.89 Ea820 369–453 197 18 0.87 0.90 365–433 299 17 0.87 0.89 Ea475 373–421 222 11 0.30 0.57 375–431 310 19 0.89 0.90 Ea804 202–226 225 6 0.23 0.31 198–222 324 12 0.32 0.42 Ea886 160–262 222 19 0.75 0.86 196–294 316 25 0.93 0.93 Ea844 244–300 185 15 0.84 0.84 248–288 254 11 0.72 0.85 Ea478 365–435 197 12 0.52 0.80 355–425 319 12 0.81 0.82 Ea841 405–483 207 32 0.80 0.90 377–463 306 30 0.86 0.91 Ea879 191–203 219 6 0.16 0.20 198–253 307 15 0.81 0.83 Locus Aipysurus fuscus (N = 30) Aipysurus apraefrontalis (N = 2) Size range (bp) N Na Ho He Size range (bp) N Na Ea407 186–206 28 6 0.74 0.75 190 2 1 Ea823 141–149 29 3 0.32 0.33 141 2 1 Ea462 372–427 27 9 0.84 0.85 382 1 1 Ea820 381–421 26 11 0.80 0.82 381, 393, 401 2 3 Ea475 375–427 22 7 0.73 0.75 413, 431 1 2 Ea804 200–214 30 4 0.67 0.68 210, 212 2 2 Ea886 238–282 28 13 0.86 0.87 266 1 1 Ea844 256–276 22 6 0.79 0.81 268 1 1 Ea478 360–395 30 8 0.83 0.85 375, 380 2 2 Ea841 343–411 30 12 0.68 0.69 345, 351 1 2 Ea879 225–241 30 9 0.80 0.81 245 1 1 Locus Aipysurus duboisii (N = 25) Aipysurus eydouxi (N = 10) Size range (bp) N Na Ho He Size range (bp) N Na Ho He Ea407 174–202 23 7 0.78 0.77 186–248 10 5 0.70 0.76 Ea823 133–141 24 3 0.42 0.34 133–189 8 8 0.88 0.80 Ea462 372–427 22 12 0.77 0.89 387–422 8 6 0.75 0.73 Ea820 373–425 22 11 0.82
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    Status of the World’s Sea Snakes IUCN Red List Assessment Final Report August 2009 IUCN Global Red List Assessment of Sea Snakes Workshop: 11‐14th February 2009 Brisbane, Australia Contact: Suzanne R Livingstone, PhD, Global Marine Species Assessment Email: [email protected] OR [email protected] Website: http://www.sci.odu.edu/gmsa/ 1. Contents Page 1. Contents 2 2. Acknowledgments 3 3. Project Rationale 3 4. Background 4 4.1. The Red List of Threatened Species 4 4.2. Global Marine Species Assessment 5 5. Methods 5 5.1. Data collection and IUCN Red List assessment process 5 5.2 IUCN Red List Categories 6 6. Results and Discussion 7 6.1. Sea snakes 7 6.2. Homalopsids 8 7. Conclusions 9 8. Reporting and outcomes 10 8.1. Results on the IUCN Red List of Threatened Species 10 8.2. Peer‐reviewed publications 10 8.3. Nominations for Australia’s EPBC Act 11 8.4. Creation of the IUCN Sea Snake Specialist Group 12 9. References 13 10. Appendices Appendix 1 ‐ workshop participants 14 Appendix 2 ‐ IUCN staff and project partners 15 Appendix 3 ‐ Sea snake species list and Red List Category 16 Appendix 4 ‐ Homalopsid snake species and Red List Category 18 2 2. Acknowledgements We would like to thank Dr Colin Limpus (Australian Government Environmental Protection Agency) and the International Sea Turtle Symposium committee for logistical and organizational support for the workshop. Special thanks to Jenny Chapman (EPA) and Chloe Schauble (ISTS). Thank you also to Dr Gordon Guymer (Chief Botanist – Director of Herbarium) for accommodating us at the Herbarium in the Brisbane Botanical Gardens.
  • Final Rule to List the Dusky Sea Snake and Three

    Final Rule to List the Dusky Sea Snake and Three

    60560 Federal Register / Vol. 80, No. 194 / Wednesday, October 7, 2015 / Rules and Regulations Manufacturer Subject lines Passat. Tiguan. VOLVO ......................................................................................... S60. 1 Granted an exemption from the parts marking requirements beginning with MY 2016. 2 The X1 carline was replaced by the X1 MPV line beginning in MY 2016. According to BMW, production of its X1 carline ceased in MY 2015. 3 Granted an exemption from the parts marking requirements beginning with MY 2015. 4 According to Mercedes-Benz, the CL-Class was renamed the S-Coupe Class beginning with MY 2015. Under authority delegated in 49 CFR part FOR FURTHER INFORMATION CONTACT: whether a group of organisms 1.95. Dwayne Meadows, Ph.D., NMFS, Office constitutes a ‘‘species’’ under the ESA, Raymond R. Posten, of Protected Resources, (301) 427–8403. then whether the status of the species Associate Administrator for Rulemaking. SUPPLEMENTARY INFORMATION: qualifies it for listing as either [FR Doc. 2015–25369 Filed 10–6–15; 8:45 am] threatened or endangered. Section 3 of Background BILLING CODE 4910–59–P the ESA defines a ‘‘species’’ to include On July 15, 2013, we received a ‘‘any subspecies of fish or wildlife or petition from WildEarth Guardians to plants, and any distinct population list 81 marine species as threatened or segment of any species of vertebrate fish DEPARTMENT OF COMMERCE endangered under the Endangered or wildlife which interbreeds when Species Act (ESA). We found that the mature.’’ National Oceanic and Atmospheric petitioned actions may be warranted for Section 3 of the ESA defines an Administration 27 of the 81 species and announced the endangered species as ‘‘any species initiation of status reviews for each of which is in danger of extinction 50 CFR Parts 223 and 224 the 27 species (78 FR 63941, October 25, throughout all or a significant portion of 2013; 78 FR 66675, November 6, 2013; its range’’ and a threatened species as [Docket No.