Abstract
There is growing evidence for the decline of cryptic species across the planet as a result of human activities. Accurate data regarding patterns of poorly known or hard-to-find species diversity is essential for the recognition and conservation of threatened species and ecosystems. Casey’s June beetle Dinacoma caseyi is a federally listed endangered species restricted to the Coachella Valley in southern California, where rapid development is leading to habitat fragmentation. This fragmentation may be disproportionately impacting a wide-range of poorly-dispersing, cryptic species, including Casey’s June beetle, which has flightless females. We characterized 1876 single nucleotide polymorphisms from across the genome along with 1480 bp of mitochondrial DNA of all confirmed extant Dinacoma populations. We found that Dinacoma is isolated into three distinct species, including evidence for a previously undescribed species revealed during this study. Each is restricted to a small part of the inland desert region. Our results suggest unappreciated and fine scale diversity, which may be reflected in the other cryptic species of the region. Patterns of diversity in non-vagile species should guide ongoing conservation planning in the region. These results show that genetic exchange within the one remaining island of beetle habitat (Palm Canyon Wash) is not limited. However, non-vagile species, such as Casey’s June beetle, may not colonize suitable but fragmented habitat islands which presents risks to the species due to habitat loss and periodic natural events that may put the single population at risk of extirpation.
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Data availability
Raw ddRAD reads are available on NCBI. BioProject: PRJNA552048; SRA: SRR9646661-SRR9646708. Sanger sequencing data is available on BOLD and GenBank MT324554-MT324591.
References
Alagona PS, Pincetl S (2008) The Coachella valley multiple species habitat conservation plan: a decade of delays. Environ Manag. https://doi.org/10.1007/s00267-007-9018-x
Andersson P, Koffman A, Sjödin NE, Johansson V (2017) Roads may act as barriers to flying insects: species composition of bees and wasps differs on two sides of a large highway. Nat Conserv 18:47
Archer FI, Adams PE, Schneiders BB (2017) stratag: an R package for manipulating, summarizing and analysing population genetic data. Mol Ecol Resour 17:5–11
Avise JC (1989) A role for molecular genetics in the recognition and conservation of endangered species. Trends Ecol Evol 4(9):279–281
Banbury B, Leache A (2014) Phrynomics: an SNP toolkit. R package version 2.0.
Blaisdell FE (1930) Revision of the genus and species of dinacoma with description of a new species (Coleoptera: Scarabaeidae). Pan Pac Entomol 6(4):171–177
Bickford D, Lohman DJ, Sodhi NS, Ng PK, Meier R, Winker K, Ingram KK, Das I (2007) Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22(3):148–155
California Department of Fish and Game (1993) Southern California coastal sage scrub natural communities conservation plan. Scientific review panel conservation guidelines and documentation. California Department of Fish and Game, Sacramento, California
Catchen J, Hohenlohe PA, Bassham S, Amores A, Cresko WA (2013) Stacks: an analysis tool set for population genomics. Mol Ecol 22(11):3124–3140
Clement M, Snell Q, Walker P, Posada D, Crandall K (2002) TCS: estimating gene genealogies. Parallel and distributed processing symposium, international proceedings 2:184
Coachella Valley Association of Governments (2016) Coachella valley multiple species habitat conservation plan. CVMSHCP plan documents. Coachella Valley Association of Governments, Palm Desert, California. https://www.cvmshcp.org
Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA et al (2011) The variant call format and VCFtools. Bioinformatics 27(15):2156–2158
DeAngelis MM, Wang DG, Hawkins TL (1995) Solid-phase reversible immobilization for the isolation of PCR products. Nucleic Acids Res 23(22):4742
Dobson AP, Rodriguez JP, Roberts WM, Wilcove DS (1997) Geographic distribution of endangered species in the United States. Science 275(5299):550–553
Eggers B, Matern A, Drees C, Eggers J, Haerdtle W, Assmann T (2010) Value of semi-open corridors for simultaneously connecting open and wooded habitats: a case study with ground beetles. Conserv Biol 24(1):256–266
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14(8):2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotech 3(5):294–299
Francis RM (2017) Pophelper: an R package and web app to analyse and visualize population structure. Mol Ecol Resour 17(1):27–32. https://doi.org/10.1111/1755-0998.12509
Frankham R (2005) Genetics and extinction. Biol Conserv 126(2):131–140
Griffiths AM, Sims DW, Cotterell SP, El Nagar A, Ellis JR, Lynghammar A, Serra-Pereira B et al (2010) Molecular markers reveal spatially segregated cryptic species in a critically endangered fish, the common skate (Dipturus batis). Proc R Soc Lond B 277(1687):1497–1503
Holland BS, Hadfield MG (2002) Islands within an island: phylogeography and conservation genetics of the endangered Hawaiian tree snail Achatinella mustelina. Mol Ecol 11(3):365–375
Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23(2):254–267. Software available from www.splitstree.org
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(14):1801–1806. https://doi.org/10.1093/bioinformatics/btm233
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S et al (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12):1647–1649
Keogh JS, Edwards DL, Fisher RN, Harlow PS (2008) Molecular and morphological analysis of the critically endangered Fijian iguanas reveals cryptic diversity and a complex biogeographic history. Philos Trans R Soc B 363(1508):3413–3426
Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15(5):1179–1191
Lewis PO (2001) A likelihood approach to estimating phylogeny from discrete morphological character data. Syst Biol 50(6):913–925. https://doi.org/10.1080/106351501753462876
Lischer HE, Excoffier L (2012) PGDSpider: an automated data conversion tool for connecting population genetics and genomics programs. Bioinformatics 28(2):298–299
Lister BC, Garcia A (2018) Climate-driven declines in arthropod abundance restructure a rainforest food web. Proc Natl Acad Sci 115(44):E10397–E10406
Loboda S, Savage J, Buddle CM, Schmidt NM, Høye TT (2018) Declining diversity and abundance of High Arctic fly assemblages over two decades of rapid climate warming. Ecography 41(2):265–277
McKinney ML (1999) High rates of extinction and threat in poorly studied taxa. Conserv Biol 13(6):1273–1281
Meirmans PG, Van Tienderen PH (2004) genotype and genodive: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794
Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Curran Associates, Red Hook, NY, pp 1–8
Mora C, Tittensor DP, Adl S, Simpson AG, Worm B (2011) How many species are there on earth and in the ocean? PLoS Biol 9(8):e1001127
Moritz C (1994) Defining ‘evolutionarily significant units’ for conservation. Trends Ecol Evol 9(10):373–375
Muñoz PT, Torres FP, Megías AG (2015) Effects of roads on insects: a review. Biodivers Conserv 24(3):659–682
Murphy SA, Joseph L, Burbidge AH, Austin J (2011) A cryptic and critically endangered species revealed by mitochondrial DNA analyses: the Western Ground Parrot. Conserv Genet 12(2):595–600
Paradis E (2010) pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26:419–420
Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE (2012) Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS ONE 7(5):e37135
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959
R Core Team (2015) R: a language and environment for statistical computing. Vienna, Austria: R foundation for statistical computing. https://www.R-project.org/
Régnier C, Fontaine B, Bouchet P (2009) Not knowing, not recording, not listing: numerous unnoticed mollusk extinctions. Conserv Biol 23(5):1214–1221
Régnier C, Achaz G, Lambert A, Cowie RH, Bouchet P, Fontaine B (2015) Mass extinction in poorly known taxa. Proc Natl Acad Sci 112(25):7761–7766
Rohland N, Reich D (2012) Cost-effective, high-throughput DNA sequencing libraries for multiplexed target capture. Genome Res 22(5):939–946
Rubinoff D (2001) Evaluating the California gnatcatcher as an umbrella species for conservation of coastal sage scrub. Conserv Biol 15:1374–1383
Rubinoff D (2006) Utility of mitochondrial DNA barcodes in species conservation. Conserv Biol 20(4):1026–1033
Rubinoff D, Sperling FAH (2004) Mitochondrial DNA sequence, morphology and ecology yield contrasting conservation implications for two threatened Buckmoths (Hemileuca: Saturniidae). Biol Conserv 118:341–351
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425
Samways MJ (2007) Insect conservation: a synthetic management approach. Annu Rev Entomol 52:465–487
Sánchez-Bayo F, Wyckhuys KA (2019) Worldwide decline of the entomofauna: a review of its drivers. Biol Conserv 232:8–27
Shaffer H, Fellers GM, Randal Voss S, Oliver JC, Pauly GB (2004) Species boundaries, phylogeography and conservation genetics of the red-legged frog (Rana aurora/draytonii) complex. Mol Ecol 13(9):2667–2677
Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am 87(6):651–701
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Stein BA, Kutner LS, Hammerson GA, Master LL, Morse LE (2000) State of the states: geographic patterns of diversity, rarity, and endemism. Precious heritage: the status of biodiversity in the United States. Oxford University Press, New York, pp 119–158
Trontelj P, Fišer C (2009) Perspectives: cryptic species diversity should not be trivialised. Syst Biodivers 7(1):1–3
Vogel G (2017) Where have all the insects gone? Science 345(6338):576–579
United States Fish and Wildlife Services (2011) Determination of endangered status for Casey’s June beetle and designation of critical habitat; final rule. Fed Reg 76(184):58954–58998
United States Fish and Wildlife Services (2019) Listed species believed to or known to occur in each state. https://ecos.fws.gov/ecp0/reports/species-listed-by-state-totals-report. Accessed 15 Mar 2019
Winter DJ (2012) MMOD: an R library for the calculation of population differentiation statistics. Mol Ecol Res 12:1158–1160
Zhang J, Pei N, Mi X (2012) Phylotools: phylogenetic tools for Ecophylogenetics. R package version 0.1.2. https://CRAN.R-project.org/package=phylotools
Zheng X, Levine D, Shen J, Gogarten S, Laurie C, Wier B (2012) A high-performance computing toolset for relatedness and principal component analysis of SNP data. Bioinformatics 28(24):3326–3328. https://doi.org/10.1093/bioinformatics/bts606
Acknowledgements
We dedicate this paper to the memory of Chris Gregory, USFWS, who tirelessly advocated for the thorough investigation and protection of all threatened species, and without whom this project would have never been completed. Noelle Ronan (USFWS) provided valuable feedback, comments and support. ddRAD library construction was performed with the support of Angela Kauwe (USDA-ARS). HiSeq 4000 sequencing was provided by the Vincent J. Coates Genomics Sequencing Laboratory at UC Berkeley, supported by NIH S10 OD018174 Instrumentation Grant. This research was funded by the United States Fish and Wildlife Service, with additional funding provided by The College of Tropical Agriculture and Human Resources, University of Hawaii at Manoa; USDA Cooperative State Research, Education and Extension (CSREES), Grant/Award Number: HAW00942-H. USDA is an equal opportunity employer. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA.
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Communicated by Anurag Chaurasia.
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Rubinoff, D., Reil, J.B., Osborne, K.H. et al. Phylogenomics reveals conservation challenges and opportunities for cryptic endangered species in a rapidly disappearing desert ecosystem. Biodivers Conserv 29, 2185–2200 (2020). https://doi.org/10.1007/s10531-020-01968-w
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DOI: https://doi.org/10.1007/s10531-020-01968-w