Non-invasive genetic monitoring for the threatened valley elderberry longhorn beetle


Autoři: Raman P. Nagarajan aff001;  Alisha Goodbla aff001;  Emily Graves aff002;  Melinda Baerwald aff001;  Marcel Holyoak aff002;  Andrea Schreier aff001
Působiště autorů: Department of Animal Science, University of California Davis, Davis, CA, United States of America aff001;  Department of Environmental Science and Policy, University of California Davis, Davis, CA, United States of America aff002
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: 10.1371/journal.pone.0227333

Souhrn

The valley elderberry longhorn beetle (VELB), Desmocerus californicus dimorphus (Coleoptera: Cerambycidae), is a federally threatened subspecies endemic to the Central Valley of California. The VELB range partially overlaps with that of its morphologically similar sister taxon, the California elderberry longhorn beetle (CELB), Desmocerus californicus californicus (Coleoptera: Cerambycidae). Current surveying methods are limited to visual identification of larval exit holes in the VELB/CELB host plant, elderberry (Sambucus spp.), into which larvae bore and excavate feeding galleries. Unbiased genetic approaches could provide a much-needed complementary approach that has more precision than relying on visual inspection of exit holes. In this study we developed a DNA sequencing-based method for indirect detection of VELB/CELB from frass (insect fecal matter), which can be easily and non-invasively collected from exit holes. Frass samples were collected from 37 locations and the 12S and 16S mitochondrial genes were partially sequenced using nested PCR amplification. Three frass-derived sequences showed 100% sequence identity to VELB/CELB barcode references from museum specimens sequenced for this study. Database queries of frass-derived sequences also revealed high similarity to common occupants of old VELB feeding galleries, including earwigs, flies, and other beetles. Overall, this non-invasive approach is a first step towards a genetic assay that could augment existing VELB monitoring and accurately discriminate between VELB, CELB, and other insects. Furthermore, a phylogenetic analysis of 12S and 16S data from museum specimens revealed evidence for the existence of a previously unrecognized, genetically distinct CELB subpopulation in southern California.

Klíčová slova:

Beetles – DNA extraction – Insects – Museum collections – Phylogenetic analysis – Polymerase chain reaction – Sequence databases – Valleys


Zdroje

1. Fisher WS. A New Cerambycid Beetle from California. Proc Entomol Soc Washingt. 1921;23: 206–208.

2. Talley TS, Wright D, Holyoak M. Assistance with the 5-Year Review of the Valley elderberry longhorn beetle (Desmocerus californicus dimorphus). Rep to US Fish Wildl Serv Sacramento Fish Wildl Off Sacramento, Calif. 2006.

3. Holyoak M, Talley TS, Hogle SE. The effectiveness of US mitigation and monitoring practices for the threatened Valley elderberry longhorn beetle. J Insect Conserv. 2010. doi: 10.1007/s10841-009-9223-4

4. Collinge SK, Holyoak M, Barr CB, Marty JT. Riparian habitat fragmentation and population persistence of the threatened valley elderberry longhorn beetle in central California. Biol Conserv. 2001. doi: 10.1016/S0006-3207(00)00211–1

5. Barr C. The Distribution, Habitat, and Status of the Valley Elderberry Longhorn Beetle Desmocerus californicus dimorphus Fisher (Insecta: Coleoptera: Cerambycidae). Sacramento; 1991.

6. Burke HE. Biological notes on Desmocerus, a genus of roundhead borers, the species of which infest various elders. J Econ Entomol. 1921;14: 450–452.

7. Lang FJ, Jokerst JD, Sutter GE. HABITAT AND POPULATIONS OF THE VALLEY ELDERBERRY LONGHORN BEETLE ALONG THE SACRAMENTO RIVER 1.

8. Fish US and Service Wildlife. Framework for Assessing Impacts to the Valley Elderberry Longhorn Beetle (Desmocerus californicus dimorphus). 2017.

9. Fish US and Service Wildlife. Listing the Valley Elderberry Longhorn Beetle as a Threatened Species with Critical Habitat. Fed Regist. 1980;45.

10. Katibah EF, Dummer KJ, Nedeff NE. Current Condition of Riparian Resources in the Central Valley of California. California Riparian Systems: Ecology, Conservation, and Productive Management. 1984.

11. Fish US and Service Wildlife. Endangered and Threatened Wildlife and Plants; Withdrawal of the Proposed Rule To Remove the Valley Elderberry Longhorn Beetle From the Federal List of Endangered and Threatened Wildlife; Proposed Rule. Fed Regist. 2014;79.

12. Fish US and Service Wildlife. Endangered and Threatened Wildlife and Plants; Removal of the Valley Elderberry Longhorn Beetle From the Federal List of Endangered and Threatened Wildlife; Proposed Rule E:\FR\FM\02OCP4. Fed Regist. 2012;77.

13. USFWS. Withdrawal of the Proposal to Delist the Valley Elderberry Longhorn Beetle (VELB) Questions and Answers. 2014.

14. USFWS. Framework for Assessing Impacts to the Valley Elderberry Longhorn Beetle. 2017.

15. Talley T, Fleishman E, Holyoak M, Murphy D, Ballard a. Rethinking a rare-species conservation strategy in an urban landscape: The case of the valley elderberry longhorn beetle. Biol Conserv. 2007;135: 21–32. doi: 10.1016/j.biocon.2006.09.022

16. Fish US and Service Wildlife. Valley Elderberry Longhorn Beetle (Desmocerus californicus dimorphus) 5-Year Review: Summary and Evaluation. 2006.

17. Linsley EG, Chemsak JA. Cerambycidae of North America. Part VI, No. 1. Taxonomy and classification of the subfamily Lepturinae. Univ Calif Publ Entomol. 1972;69: 1–138.

18. Chemsak JA. Illustrated revision of the Cerambycidae of North America (Vol II. Lepturinae). Wolfsgarden Books, Chino.; 2005.

19. US Fish and Wildlife Service. Recovery plan for the valley elderberry longhorn beetle. Portland, OR; 1984.

20. Halstead JA, Oldham J. Revision of the nearctic Desmocerus Audinet-Serville with emphasis on the federally threatened valley elderberry longhorn beetle (Coleoptera: Cerambycidae). Fresno, CA; 1990.

21. Ahrens D, Monaghan MT, Vogler AP. DNA-based taxonomy for associating adults and larvae in multi-species assemblages of chafers (Coleoptera: Scarabaeidae). Mol Phylogenet Evol. 2007. doi: 10.1016/j.ympev.2007.02.024 17420144

22. Raupach MJ, Astrin JJ, Hannig K, Peters MK, Stoeckle MY, Wägele JW. Molecular species identification of Central European ground beetles (Coleoptera: Carabidae) using nuclear rDNA expansion segments and DNA barcodes. Front Zool. 2010. doi: 10.1186/1742-9994-7-26 20836845

23. Briski E, Cristescu ME, Bailey SA, MacIsaac HJ. Use of DNA barcoding to detect invertebrate invasive species from diapausing eggs. Biol Invasions. 2011. doi: 10.1007/s10530-010-9892-7

24. Jackson JK, Battle JM, White BP, Pilgrim EM, Stein ED, Miller PE, et al. Cryptic biodiversity in streams: a comparison of macroinvertebrate communities based on morphological and DNA barcode identifications. Freshw Sci. 2014. doi: 10.1086/674430

25. Taberlet P, Prud’Homme SM, Campione E, Roy J, Miquel C, Shehzad W, et al. Soil sampling and isolation of extracellular DNA from large amount of starting material suitable for metabarcoding studies. Mol Ecol. 2012. doi: 10.1111/j.1365-294X.2011.05317.x 22300434

26. Rougerie R, Smith MA, Fernandez-Triana J, Lopez-Vaamonde C, Ratnasingham S, Hebert PDN. Molecular analysis of parasitoid linkages (MAPL): Gut contents of adult parasitoid wasps reveal larval host. Mol Ecol. 2011. doi: 10.1111/j.1365-294X.2010.04918.x 21083857

27. Brandl S, Schumer G, Schreier BM, Conrad JL, May B, Baerwald MR. Ten real-time PCR assays for detection of fish predation at the community level in the San Francisco Estuary-Delta. Mol Ecol Resour. 2015. doi: 10.1111/1755-0998.12305 25042458

28. Zeale MRK, Butlin RK, Barker GLA, Lees DC, Jones G. Taxon-specific PCR for DNA barcoding arthropod prey in bat faeces. Mol Ecol Resour. 2011. doi: 10.1111/j.1755-0998.2010.02920.x 21429129

29. Feinstein J. DNA sequence from butterfly frass and exuviae. Conserv Genet. 2004. doi: 10.1023/B:COGE.0000014058.34840.94

30. Lefort MC, Boyer S, Worner SP, Armstrong K. Noninvasive molecular methods to identify live scarab larvae: An example of sympatric pest and nonpest species in New Zealand. Mol Ecol Resour. 2012. doi: 10.1111/j.1755-0998.2011.03103.x 22189059

31. Scriven JJ, Woodall LC, Goulson D. Nondestructive DNA sampling from bumblebee faeces. Mol Ecol Resour. 2013. doi: 10.1111/1755-0998.12036 23190789

32. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol. 2016;33: 1870–1874. doi: 10.1093/molbev/msw054 27004904

33. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4: 406–25. doi: 10.1093/oxfordjournals.molbev.a040454 3447015

34. Tamura K. Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. Mol Biol Evol. 1992;9: 678–87. doi: 10.1093/oxfordjournals.molbev.a040752 1630306

35. Felsenstein J. CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP. Evolution (N Y). 1985;39: 783–791. doi: 10.1111/j.1558-5646.1985.tb00420.x 28561359

36. Thomsen PF, Elias S, Gilbert MTP, Haile J, Munch K, Kuzmina S, et al. Non-destructive sampling of ancient insect DNA. PLoS One. 2009. doi: 10.1371/journal.pone.0005048 19337382

37. Nagarajan R, Schreier A, Baerwald M, Goodbla A, Graves E, Holyoak M. Using fecal DNA survey protocols to optimize traditional exit hole surveys and increase detection rates for VELB. Final Report to USFWS. 2018.

38. Roy K, Ewing CP, Hughes MA, Keith L, Bennett GM. Presence and viability of Ceratocystis lukuohia in ambrosia beetle frass from Rapid ʻŌhiʻa Death-affected Metrosideros polymorpha trees on Hawaiʻi Island. For Pathol. 2019. doi: 10.1111/efp.12484

39. Kamenova S, Mayer R, Rubbmark OR, Coissac E, Plantegenest M, Traugott M. Comparing three types of dietary samples for prey DNA decay in an insect generalist predator. Mol Ecol Resour. 2018. doi: 10.1111/1755-0998.12775 29509995

40. Ali B, Zhou Y, Zhang Q, Niu C, Zhu Z. Development of an easy and cost-effective method for non-invasive genotyping of insects. Kalendar R, editor. PLoS One. 2019;14: e0216998. doi: 10.1371/journal.pone.0216998 31158235

41. Ide T, Kanzaki N, Ohmura W, Okabe K. Molecular identification of an invasive wood-boring insect Lyctus brunneus (Coleoptera: Bostrichidae: Lyctinae) using Frass by loop-mediated isothermal amplification and nested PCR assays. J Econ Entomol. 2016. doi: 10.1093/jee/tow030 27018442

42. Schrader C, Schielke A, Ellerbroek L, Johne R. PCR inhibitors—occurrence, properties and removal. Journal of Applied Microbiology. 2012. doi: 10.1111/j.1365-2672.2012.05384.x 22747964

43. Lee AB, Cooper TA. Improved direct PCR screen for bacterial colonies: Wooden toothpicks inhibit PCR amplification. Biotechniques. 1995.

44. Schapker PA. A Review of the Lepturinae (Coleoptera: Cerambycidae) of the Pacific Northwest, with Special Attention to the Elderberry Longhorn Beetle, Desmocerus Dejean. Oregon State. 2014.

45. Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, Lewis ZA, et al. Rapid SNP Discovery and Genetic Mapping Using Sequenced RAD Markers. Fay JC, editor. PLoS One. 2008;3: e3376. doi: 10.1371/journal.pone.0003376 18852878

46. Ray AM, Swift IP, McElfresh JS, Alten RL, Millar JG. (R)-Desmolactone, A Female-produced Sex Pheromone Component of the Cerambycid Beetle Desmocerus californicus californicus (subfamily Lepturinae). J Chem Ecol. 2012. doi: 10.1007/s10886-012-0070-5 22350519

47. Ray AM, Arnold RA, Swift I, Schapker PA, McCann S, Marshall CJ, et al. (R)-desmolactone is a sex pheromone or sex attractant for the endangered valley elderberry longhorn beetle Desmocerus californicus dimorphus and several congeners (Cerambycidae: Lepturinae). PLoS One. 2014;9: 1–18. doi: 10.1371/journal.pone.0115498 25521293


Článek vyšel v časopise

PLOS One


2020 Číslo 1