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Genomic distinctness despite shared color patterns among threatened populations of a tiger beetle

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Abstract

Conservation biologists have long debated the value of subspecies, which are morphologically and geographically identifiable but not necessarily evolutionarily distinctive. One example of a controversial subspecies is Cicindela formosa gibsoni, a tiger beetle that is nationally listed as threatened in Canada and whose taxonomic status is based primarily on its unique elytral (forewing) color pattern. To determine whether C. f. gibsoni represents one or more genetically distinctive units, we sampled 14 populations within or near this subspecies’ disjunct North American range and assessed their genetic differentiation from neighboring and phenotypically distinctive populations of C. f. formosa and C. f. fletcheri. Instead of clustering by color pattern, analyses of mitochondrial and nuclear markers recovered three geographically structured genetic groupings: a northern cluster from Canada, a southwestern cluster from northwestern Colorado, and a southeastern cluster of US populations east of the Continental Divide. These data, coupled with previously documented differences in larval morphology, suggest that populations of C. formosa in western Canada and northwestern Colorado may have independently evolved similar color patterns. Thus, we consider C. f. gibsoni to be endemic to Canada and describe the novel subspecies C. f. gaumeri ssp. nov. from northwestern Colorado. Both subspecies are evolutionarily significant units, and each deserves consideration for conservation listing. Collectively, our results reveal general congruence between mitochondrial and nuclear genetic data but conflict with color pattern, the conventional basis for subspecies designations in tiger beetles.

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Data availability

COI sequences are available from GenBank under the accession numbers MW663773–MW663837 (5′ region) and MW665391–MW665456 (3′ region). Raw, demultiplexed sequences produced by ddRAD-seq are available from the Sequence Read Archive (SRA) under the accession numbers SAMN18079467–SAMN18079520. VCF files containing filtered SNP data, PopArt Nexus files containing trimmed COI sequences, and STRUCTURE input and output files were deposited in Dryad (https://doi.org/10.5061/dryad.k6djh9w5t). Raw phenotypic data are available as online supplementary tables.

Code availability

The code that we used to process and filter SNP data is available on Dryad (https://doi.org/10.5061/dryad.k6djh9w5t).

References

  • Acorn JH (1992) The historical development of geographic color variation among dune Cicindela in western Canada. In: Noonan GE, Ball GE, Stork NE (eds) The biogeography of ground beetles of mountains and islands. Intercept Press, Andover, p 256

    Google Scholar 

  • Acorn JH (2001) Tiger Beetles of Alberta: Killers on the Clay. University of Alberta Press, Edmonton, Stalkers on the Sand

    Google Scholar 

  • Acorn JH (2004) Grassland tiger beetles in Canada. Arthropods of Canadian Grasslands, Biological Survey of Canada 10:6-13

  • Acorn JH (2011) Sand hill arthropods in grasslands. In: Floate KD (ed) Arthropods of Canadian grasslands (volume 2): inhabitants of a changing landscape. Biological Survey of Canada, Ottawa, pp 25–43

    Google Scholar 

  • Amadon D (1949) The seventy-five per cent rule for subspecies. The Condor 51:250–258

    Article  Google Scholar 

  • Avise JC, Nelson WS (1989) Molecular genetic relationships of the extinct dusky seaside sparrow. Science 243:646–648

    Article  PubMed  CAS  Google Scholar 

  • Bailey NW, Gwynne DT, Ritchie MG (2007) Dispersal differences predict population genetic structure in Mormon crickets. Mol Ecol 16:2079–2089

    Article  PubMed  CAS  Google Scholar 

  • Bedford NL, Hoekstra HE (2015) Peromyscus mice as a model for studying natural variation. eLife 4:e06813. https://doi.org/10.7554/eLife.06813

    Article  PubMed Central  Google Scholar 

  • Bell AJ, Calladine KS, Phillips ID (2019) Distribution, abundance, and ecology of the threatened Gibson’s Big Sand Tiger Beetle (Cicindela formosa gibsoni Brown) in the Elbow Sand Hills of Saskatchewan. J Insect Conserv 23:957–965. https://doi.org/10.1007/s10841-019-00183-5

    Article  Google Scholar 

  • Bolles K, Forman SL, Sweeney M (2017) Eolian processes and heterogenous dust emissivity during the 1930s Dust Bowl Drought and implications for projected 21st-century megadroughts. Holocene 27:1578–1588

    Article  Google Scholar 

  • Braby MF, Eastwood R, Murray N (2012) The subspecies concept in butterflies: has its application in taxonomy and conservation biology outlived its usefulness? Biol J Linn Soc 106:699–716

    Article  Google Scholar 

  • Brown WJ (1940) Some new and poorly known species of Coleoptera. Can Entomol 72:182–187

    Article  Google Scholar 

  • Burbrink FT, Lawson R, Slowinski JB (2000) Mitochondrial DNA phylogeography of the polytypic North American rat snake (Elaphe obsoleta): a critique of the subspecies concept. Evolution 54:2107–2118

    PubMed  CAS  Google Scholar 

  • Campbell EO, Gage EV, Gage RV, Sperling FAH (2020) Single nucleotide polymorphism-based species phylogeny of greater fritillary butterflies (Lepidoptera: Nymphalidae: Speyeria) demonstrates widespread mitonuclear discordance. Syst Entomol 45:269–280

    Article  Google Scholar 

  • Catchen JM, Amores A, Hohenlohe P, Cresko W, Postlethwait JH (2011) Stacks: building and genotyping loci de novo from short-read sequences. 1:171–182. https://doi.org/10.1534/g3.111.000240

  • Coates DJ, Byrne M, Moritz C (2018) Genetic diversity and conservation units: dealing with the species-population continuum in the age of genomics. Front Ecol Evol 6:165. https://doi.org/10.3389/fevo.2018.00165

    Article  Google Scholar 

  • COSEWIC (2012) Committee on the Status of Endangered Wildlife in Canada’s assessment and status report on the Gibson’s Big Sand Tiger Beetle Cicindela formosa gibsoni in Canada. COSEWIC, Ottawa

    Google Scholar 

  • Criddle N (1925) A new Cicindela from the adjacent territory of Montana and Alberta. Can Entomol 57:127–128

    Article  Google Scholar 

  • Danecek P et al (2011) The variant call format and VCFtools. Bioinformatics 27:2156–2158. https://doi.org/10.1093/bioinformatics/btr330

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dice LR (1940) Ecologic and genetic variability within species of Peromyscus. Am Nat 74:212–221

    Article  Google Scholar 

  • Dumbacher JP, Fleischer RC (2001) Phylogenetic evidence for colour pattern convergence in toxic pitohuis: Müllerian mimicry in birds? Proc R Soc B 268:1971–1976

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dupuis JR, Roe AD, Sperling FAH (2012) Multi-locus species delimitation in closely related animals and fungi: one marker is not enough. Mol Ecol 21:4422–4436

    Article  PubMed  Google Scholar 

  • Dupuis JR, Oliver JC, Brunet BMT, Longcore T, Johnson JJ, Sperling FAH (2018) Genomic data indicate ubiquitous evolutionary distinctiveness among populations of California metalmark butterflies. Conserv Genet 19:1097–1108

    Article  Google Scholar 

  • Duran DP, Laroche RA, Gough HM, Gwiazdowski RA, Knisley CB, Herrmann DP, Roman SJ, Egan SP (2020) Geographic life history differences predict genomic divergence better than mitochondrial barcodes or phenotype. Genes 11:1–22

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Foll M, Gaggiotti O (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180:977–993

    Article  PubMed  PubMed Central  Google Scholar 

  • Freitag RP (1999) Catalogue of the tiger beetles of Canada and the United States. National Research Council Research Press, Ottawa

    Google Scholar 

  • Gaumer GC (1977) The variation and taxonomy of Cicindela formosa Say (Coleoptera: Cicindelidae). PhD Dissertation, Texas A & M University, College Station, Texas. 253 pp.

  • de Guia APO, Saitoh T (2007) The gap between the concept and definitions in the evolutionarily significant unit: the need to integrate neutral genetic variation and adaptive variation. Ecol Res 22:604–612. https://doi.org/10.1007/s11284-006-0059-z

    Article  Google Scholar 

  • Hadley NF, Savill A, Schultz TD (1992) Coloration and its thermal consequences in the New Zealand tiger beetle Neocicindela perhispida. J Therm Biol 17:55–61

    Article  Google Scholar 

  • Herweijer C, Seager R, Cook ER (2006) North American droughts of the mid to late nineteenth century: a history, simulation and implication for Mediaeval drought. Holocene 16:159–171

    Article  Google Scholar 

  • Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332

    Article  PubMed  PubMed Central  Google Scholar 

  • The Inkscape Team (2019) Inkscape v0.92. https://inkscape.org/. Accessed 9 Mar 2020

  • Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. https://doi.org/10.1093/bioinformatics/btn129

    Article  PubMed  CAS  Google Scholar 

  • Knisley CB, Kippenhan M, Brzoska D (2014) Conservation status of United States tiger beetles. Terr Arthropod Rev 7:93–145

    Article  Google Scholar 

  • Kopelman NM, Mayzel J, Jakobsson MJ, Rosenberg NA, Mayrose I (2015) CLUMPAK: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Leigh JW, Bryant D (2015) POPART: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116

    Article  Google Scholar 

  • Li Y-L, Liu J-X (2018) StructureSelector: a web-based software to select and visualize the optimal number of clusters using multiple methods. Mol Ecol Resour 18:176–177

    Article  PubMed  Google Scholar 

  • MacDonald ZG, Dupuis JR, Davis CS, Acorn JH, Nielsen SE, Sperling FAH (2020) Gene flow and climate-associated genetic variation in a vagile habitat specialist. Mol Ecol. https://doi.org/https://doi.org/10.1111/MEC.15604

  • Mace GM (2004) The role of taxonomy in species conservation. Philos Trans R Soc B 359:711–719. https://doi.org/10.1098/rstb.2003.1454

    Article  Google Scholar 

  • Martin M (2011) Cutadapt removed adapter sequences from high-throughput sequencing reads. EMBnet J 17:10–12

    Article  Google Scholar 

  • Mayr E (1942) Systematics and the origin of species. Columbia University Press, New York

    Google Scholar 

  • Mayr E (1982) Of what use are subspecies? Auk 99:593–595

    Google Scholar 

  • Mayr E, Ashlock PD (1991) Principles of Systematic Zoology, 2nd edn. McGraw-Hill, New York

    Google Scholar 

  • 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. https://doi.org/10.1111/j.1471-8286.2004.00770.x

    Article  Google Scholar 

  • Miao X, Mason JA, Swinehart JB, Loope DB, Hanson PR, Goble RJ, Liu X (2007) A 10,000 year record of dune activity, dust storms, and severe drought in the central Great Plains. Geology 35:119–122

    Article  Google Scholar 

  • Michie LJ, Mallard F, Majerus MEN, Jiggins FM (2010) Melanic through nature or nurture: genetic polymorphism and phenotypic plasticity in Harmonia axyridis. J Evol Biol 23:1699–1707

    Article  PubMed  CAS  Google Scholar 

  • Morgan M, Knisley CB, Vogler AP (2000) New taxonomic status of the endangered tiger beetle Cicindela limbata albissima (Coleoptera: Cicindelidae): evidence from mtDNA. Ann Entomol Soc Am 93:1108–1115

    Article  CAS  Google Scholar 

  • Nei M (1987) Molecular Evolutionary Genetics. Columbia University Press, New York

    Book  Google Scholar 

  • Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10

    Article  PubMed  Google Scholar 

  • O’Leary SJ, Puritz JB, Willis SC, Hollenbeck CM, Portnoy DS (2018) These aren’t the loci you’re looking for: principles of effective SNP filtering for molecular ecologists. Mol Ecol 27:3193–3206

    Article  Google Scholar 

  • Paris JR, Stevens JR, Catchen JM (2017) Lost in parameter space: a road map for STACKS. Methods Ecol Evol 8:1360–1373

    Article  Google Scholar 

  • Pearson DL, Vogler AP (2001) Tiger Beetles. The Evolution, Ecology, and Diversity of the Cicindelids. Comstock Publishing Associates (Cornell University Press), Ithaca

  • Pearson DL, Knisley CB, Duran DP, Krazilek CJ (2015) A field guide to the tiger beetles of the United States and Canada, 2nd edn. Oxford University Press, New York

    Google Scholar 

  • Pembleton LW, Cogan NOI, Forster JW (2013) StAMPP: an R package for calculation of genetic differentiation and structure of mixed-ploidy level populations. Mol Ecol Resour 13:946–952

    Article  PubMed  CAS  Google Scholar 

  • Phillimore AB, Owens IPF (2006) Are subspecies useful in evolutionary and conservation biology? Proc R Soc B 273:1049–1053

    Article  PubMed  PubMed Central  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Proshek B, Dupuis JR, Engberg A, Davenport K, Opler PA, Powell JA, Sperling FA (2015) Genetic evaluation of the evolutionary distinctness of a federally endangered butterfly Lange’s Metalmark. BMC Evol Biol 15:73. https://doi.org/10.1186/s12862-015-0354-9

    Article  PubMed  PubMed Central  Google Scholar 

  • Puechmaille SJ (2016) The program STRUCTURE does not reliably recover the correct population structure when sampling is uneven: subsampling and new estimators alleviate the problem. Mol Ecol Resour 16:608–627

    Article  PubMed  Google Scholar 

  • R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Ratnasingham S, Hebert PDN (2007) BOLD: the Barcode of Life Data System. Mol Ecol Notes 7:355–364

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Reyes-Velasco J, Adams RH, Boissinot S, Parkinson CL, Campbell JA, Castoe TA, Smith EN (2020) Genome-wide SNPs clarify lineage diversity confused by coloration in coralsnakes of the Micrurus diastema complex (Serpentes: Elapidae). Mol Phylogenet Evol 147:106770. https://doi.org/10.1016/j.ympev.2020.106770

    Article  PubMed  Google Scholar 

  • Rochette NC, Catchen JM (2017) Deriving genotypes from RAD-seq short-read data using Stacks. Nat Protoc 12:2640–2659

    Article  PubMed  CAS  Google Scholar 

  • Rubinoff D (2006) Utility of mitochondrial barcodes in species conservation. Conserv Biol 20:1026–1033

    Article  PubMed  Google Scholar 

  • Ryder OA (1986) Species conservation and systematics: The dilemma of subspecies. Trends Ecol Evol 1:9–10

    Article  Google Scholar 

  • Schultz TD, Hadley NF (1987) Structural colors of tiger beetles and their role in heat transfer through the integument. Physiol Zool 60:737–745

    Article  Google Scholar 

  • Steiner CC, Römpler H, Boettger LM, Schöneberg T, Hoekstra HE (2009) The genetic basis of phenotypic convergence in beach mice: similar pigment patterns but different genes. Mol Biol Evol 26:35–45

    Article  PubMed  CAS  Google Scholar 

  • Torres-Cambas Y, Ferreira S, Cordero-Rivera A, Lorenzo-Carballa M (2017) Identification of evolutionarily significant units in the Cuban endemic damselfly Hypolestes trinitatis (Odonata: Hypolestidae). Conserv Genet 18:1229–1234

    Article  CAS  Google Scholar 

  • Tsuji K, Hori M, Phyu MH, Liang H, Sota T (2016) Colorful patterns indicate common ancestry in diverged tiger beetle taxa: molecular phylogeny, biogeography, and evolution of elytral coloration of the genus Cicindela subgenus Sophiodela and its allies. Mol Phylogenet Evol 95:1–10

    Article  PubMed  Google Scholar 

  • Vogler AP, Desalle R (1994) Diagnosing units of conservation management. Conserv Biol 8:354–363

    Article  Google Scholar 

  • Wallis JB (1961) The Cicindelidae of Canada. University of Toronto Press, Toronto

    Book  Google Scholar 

  • Walsh J, Lovette IJ, Winder V, Elphick CS, Olsen BJ, Shriver G, Kovach AI (2017) Subspecies delineation amid phenotypic, geographic and genetic discordance in a songbird. Mol Ecol 26:1242–1255

    Article  PubMed  CAS  Google Scholar 

  • Wang J (2017) The computer program STRUCTURE for assigning individuals to populations: easy to use but easier to misuse. Mol Ecol Resour 17:981–990

    Article  PubMed  CAS  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    PubMed  CAS  Google Scholar 

  • Wilson EO, Brown WL (1953) The subspecies concept and its taxonomic application. Syst Zool 2:97–111

    Article  Google Scholar 

  • Wolfe SA, Huntley DJ, David PP, Ollerhead J, Sauchyn DJ, MacDonald GM (2001) Late 18th century drought-induced sand dune activity, Great Sand Hills, Saskatchewan. Can J Earth Sci 38:105–117

    Article  Google Scholar 

  • Yamamoto N, Sota T (2020) Evolutionary fine-tuning of background-matching camouflage among geographical populations in the sandy beach tiger beetle. Proc R Soc B 287:20202315

    Article  PubMed  PubMed Central  Google Scholar 

  • Zink RM (2004) The role of subspecies in obscuring avian biological diversity and misleading conservation policy. Proc R Soc B 271:561–564

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank Barry Knisley, Todd Lawton, Mathew Brust, Michael Kippenhan, Michael Ivie, Dave Larson, and Boris Kondratieff for information that assisted in collecting field specimens, Eric Neilson for assistance transporting specimens, Robin Wiggins for access to his property, and Charlene and Brian Donnelly for their hospitality during fieldwork. We also thank Randy Dzenkiw, Ron Huber, David Maddison, Ted McRae, and Cindy Sheppard for generously sharing specimens, data, and insights. Finally, we are grateful to Danny Shpeley for assisting with specimen deposition, Erin Campbell for offering advice on sequencing protocols and bioinformatics, Brittany Wingert and Kyle Snape for sharing R scripts for data visualization, and three anonymous reviewers for comments that improved this manuscript. Saskatchewan populations of Cicindela formosa were sampled under permit 18FW122 from the Saskatchewan Ministry of Environment, as well as permits from Saskatchewan’s Representative Areas Network and the Saskatchewan Ministry of Parks, Culture, and Sport. This work was enabled by Compute Canada Calcul Canada Resources (http://www.computecanada.ca) and the Molecular Biology Services Unit (MBSU) at the University of Alberta. Funding was provided by the Natural Sciences and Engineering Research Council of Canada (NSERC) through a Discovery Grant to F.A.H.S. (RGPIN-2018-04920) and an Undergraduate Student Research Award to R.L.K.F. (USRA-540997-2019).

Funding

This study was funded by a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant to F.A.H.S. (RGPIN-2018-04920) and an NSERC Undergraduate Student Research Award to R.L.K.F. (USRA-540997-2019).

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  1. Rowan L. K. French

    Present address: Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada

Authors and Affiliations

  1. Department of Biological Sciences, University of Alberta, Edmonton, AB, Canada

    Rowan L. K. French & Felix A. H. Sperling

  2. Department of Biology, University of Saskatchewan, Saskatoon, SK, Canada

    Aaron J. Bell & Kiara S. Calladine

  3. Troutreach Saskatchewan, Saskatchewan Wildlife Federation, Moose Jaw, SK, Canada

    Aaron J. Bell & Kiara S. Calladine

  4. Department of Renewable Resources, University of Alberta, Edmonton, AB, Canada

    John H. Acorn

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Correspondence to Rowan L. K. French.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Saskatchewan populations of Cicindela formosa were sampled under permit 18FW122 from the Saskatchewan Ministry of Environment, as well as permits from Saskatchewan’s Representative Areas Network and the Saskatchewan Ministry of Parks, Culture, and Sport.

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French, R.L.K., Bell, A.J., Calladine, K.S. et al. Genomic distinctness despite shared color patterns among threatened populations of a tiger beetle. Conserv Genet 22, 873–888 (2021). https://doi.org/10.1007/s10592-021-01370-1

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