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9 - Guerrilla Taxonomy and Discriminating Cryptic Species

Is Quick Also Dirty?

Published online by Cambridge University Press:  01 September 2022

Alexandre K. Monro
Affiliation:
Royal Botanic Gardens, Kew
Simon J. Mayo
Affiliation:
Royal Botanic Gardens, Kew
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Summary

Our grasp of biodiversity is fine-tuned through revisionary taxonomy. If species exist in nature and can be discovered with available techniques, revisions should converge on broadly shared interpretations of species.Here species are recognised using integrative assessment, focussing on whether there is corroboration between evidence from coalescents in the COI gene and evidence from morphological divergences. Retrospective analysis of progress between 2011‒2019 in global analyses of bumblebees in two contrasting groups examines convergence on stable solutions within each group as samples were accumulated.Results show that convergence was slow to be achieved because of initial under-representation of rare species despite directed sampling to increase evenness.Filtering out short sequences with ambiguous data had limited value for improving convergence. Filtering to retain only unique alleles was more successful in reducing the over-sampling effects that can promote acceptance of false cryptic species.In addition, results for discriminating polytypic and cryptic species when using UAF are better supported by patterns in genetic divergence with geographical distance . Consequently, the UAF approach was better able to clarify the distinction for long-problematic cases of cryptic bumblebee species. In summary, these results show that reliable taxonomic revision may be difficult to achieve quickly.

Type
Chapter
Information
Cryptic Species
Morphological Stasis, Circumscription, and Hidden Diversity
, pp. 213 - 241
Publisher: Cambridge University Press
Print publication year: 2022

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References

Almeida, E. A. B., Packer, L., Melo, G. A. R. et al. (2018) The diversification of neopasiphaeine bees during the Cenozoic (Hymenoptera: Colletidae). Zoologica Scripta 12333: 117. https://doi.org/10.1111/zsc.12333Google Scholar
An, J.-D., Huang, J.-X., Shao, Y.-Q. et al. (2014) The bumblebees of North China (Apidae, Bombus Latreille). Zootaxa 3830: 189. https://doi.org/10.11646/zootaxa.3830.1.1Google Scholar
Baum, D. and Smith, S. (2012) Tree Thinking: An Introduction to Phylogenetic Biology. Roberts and Company, Greenwood Village.Google Scholar
Bergsten, J., Bilton, D. T., Fujisawa, T. et al. (2012) The effect of geographical scale of sampling on DNA barcoding. Systematic Biology 61: 851869. https://doi.org/10.1093/sysbio/sys037Google Scholar
Bertsch, A., Schweer, H., Titze, A., and Tanaka, H. (2005) Male labial gland secretions and mitochondrial DNA markers support species status of Bombus cryptarum and B. magnus (Hymenoptera, Apidae). Insectes Sociaux 52: 4554.Google Scholar
Bolton, B. (2007) How to conduct large-scale taxonomic revisions in Formicidae. Memoirs of the American Entomological Institute 80: 5271.Google Scholar
Cameron, S. A., Hines, H. M., and Williams, P. H. (2007) A comprehensive phylogeny of the bumble bees (Bombus). Biological Journal of the Linnean Society 91: 161188.Google Scholar
Cameron, S. A., Lozier, J. D., Strange, J. P. et al. (2011) Patterns of widespread decline in North American bumble bees. Proceedings of the National Academy of Sciences of the United States of America 108: 662667.CrossRefGoogle ScholarPubMed
Campillo, L. C., Barley, A. J., and Thomson, R. C. (2020) Model-based species delimitation: Are coalescent species reproductively isolated? Systematic Biology 69: 708721. https://doi.org/10.1093/sysbio/syz072Google Scholar
de Candolle, A. (1880) La Phytographie ou l’art de décrire les végétaux considérés sous différents points de vue. G. Masson, Paris.Google Scholar
De Queiroz, K. (2007) Species concepts and species delimitation. Systematic Biology 56: 879886. https://doi.org/10.1080/10635150701701083Google Scholar
Dillon, R. T. (1984) Geographic distance, environmental difference, and divergence between isolated populations. Systematic Zoology 33: 6982.Google Scholar
Dray, S. and Dufour, A.-B. (2007) The ade4 package: Implementing the duality diagram for ecologists. Journal of Statistical Software 22: 120.Google Scholar
Drew, L. (2011) Are we losing the science of taxonomy? BioScience 61: 942946. https://doi.org/10.1525/bio.2011.61.12.4Google Scholar
Francoso, E., Zuntini, A. R., Carnaval, A. C., and Arias, M. C. (2016) Comparative phylogeography in the Atlantic forest and Brazilian savannas: Pleistocene fluctuations and dispersal shape spatial patterns in two bumblebees. BMC Evolutionary Biology: 16. https://doi.org/10.1186/s12862–016-0803-0Google Scholar
Fujisawa, T. and Barraclough, T. G. (2013) Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent approach: A revised method and evaluation on simulated data sets. Systematic Biology 62: 707724.Google Scholar
Gaston, K. J. (1994) Rarity. Springer, London.Google Scholar
Goodwin, Z. A., Harris, D. J., Filer, D., Wood, J. R. I., and Scotland, R. W. (2015) Widespread mistaken identity in tropical plant collections. Current Biology 25: R1066–1067. https://doi.org/10.1016/j.cub.2015.10.002Google Scholar
Goulson, D. (2010) Bumblebees, Behaviour, Ecology, and Conservation (2nd ed.). Oxford University Press, Oxford.Google Scholar
Guisan, A., Broennimann, O., Engler, R. et al. (2006) Using niche-based models to improve the sampling of rare species. Conservation Biology 20: 501511. https://doi.org/10.1111/j.1523-1739.2006.00354.xCrossRefGoogle ScholarPubMed
Hebert, P. D. N., Ratnasingham, S., and deWaard, J. R. (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London (B) 270: S96S99. https://doi.org/10.1098/rsbl.2003.0025CrossRefGoogle ScholarPubMed
Hebert, P. D. N., Cywinska, A., Ball, S. L. et al. (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London B, Biological Sciences 270: 313321.CrossRefGoogle ScholarPubMed
Hebert, P. D. N., Penton, E. H., Burns, J. M., Janzen, D. H., and Hallwachs, W. (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Sciences 101: 1481214817. https://doi.org/10.1073/pnas.0406166101CrossRefGoogle ScholarPubMed
Hines, H. M. (2008) Historical biogeography, divergence times, and diversification patterns of bumble bees (Hymenoptera: Apidae: Bombus). Systematic Biology 57: 58-75.Google Scholar
Holland, J. M., Smith, B. M., Storkey, J., Lutman, P. J. W., and Aebischer, N. J. (2015) Managing habitats on English farmland for insect pollinator conservation. Biological Conservation 182: 21222. https://goi.org/10.1016/j.biocon.2014.12.009CrossRefGoogle Scholar
Jackson, J. M., Pimsler, M. L., Oyen, K. J. et al. (2018) Distance, elevation and environment as drivers of diversity and divergence in bumble bees across latitude and altitude. Molecular Ecology 27: 29262942.CrossRefGoogle ScholarPubMed
Kapli, P., Lutteropp, S., Zhang, J. et al. (2017) Multi-rate Poisson tree processes for single-locus species delimitation under maximum likelihood and Markov chain Monte Carlo. Bioinformatics 33: 16301638. https://doi.org/10.1093/bioinformatics/btx025Google Scholar
Koch, J. B., Rodriguez, J., Pitts, J. P., and Strange, J. (2018) Phylogeny and population genetic analyses reveals cryptic speciation in the Bombus fervidus species complex (Hymenoptera: Apidae). PLoS ONE 13. https://doi.org/10.1371/journal.pone.0207080Google Scholar
Lecocq, T., Dellicour, S., Michez, D. et al. (2013) Scent of a break-up: Phylogeography and reproductive trait divergences in the red-tailed bumblebee (Bombus lapidarius). BMC Evolutionary Biology 13: 263. https://doi.org/10.1186/1471-2148-13-263Google Scholar
Lecocq, T., Dellicour, S., Michez, D. (2015) Methods for species delimitation in bumblebees (Hymenoptera, Apidae, Bombus): Towards an integrative approach. Zoologica Scripta 44: 281297. https://doi.org/10.1111/zsc.12107Google Scholar
Lecocq, T., Biella, P., Martinet, B., and Rasmont, P. (2019) Too strict or too loose? Integrative taxonomic assessment of Bombus lapidarius complex (Hymenoptera: Apidae). Zoologica Scripta. https://doi.org/10.1111/zsc.12402CrossRefGoogle Scholar
Lohse, K. (2009) Can mtDNA barcodes be used to delimit species? A response to Pons et al. (2006). Systematic Biology 58: 439442.CrossRefGoogle ScholarPubMed
Lou, M. and Golding, G. B. (2012) The effect of sampling from subdivided populations on species identification with DNA barcodes using a Bayesian statistical approach. Molecular Phylogenetics and Evolution 65: 765773. https://doi.org/10.1016/j.ympev.2012.07.033CrossRefGoogle ScholarPubMed
Luo, A., Lan, H.-Q., Ling, C. et al. (2015) A simulation study of sample size for DNA barcoding. Ecology and Evolution 5: 58695879. https://doi.org/10.1002/ece3.1846Google Scholar
Magnacca, K. N. and Brown, M. J. F. (2010) Mitochondrial heteroplasmy and DNA barcoding in Hawaiian Hylaeus (Nesoprosopis) bees (Hymenoptera: Colletidae). BMC Evolutionary Biology 10: 116. https://doi.org/10.1186/1471-2148-10-174Google Scholar
Mantel, N. (1967) The detection of disease clustering and a generalized regression approach. Cancer Research 27: 209220.Google Scholar
Martinet, B., Brasero, N., Lecocq, T. et al. (2018) Adding attractive semio-chemical trait refines the taxonomy of Alpinobombus (Hymenoptera: Apidae). Apidologie. https://goi.org/10.1007/s13592–018-0611-1Google Scholar
Matz, M. V. and Nielsen, R. (2005) A likelihood ratio test for species membership based on DNA sequence data. Transactions of the Royal Society (Biological Sciences) 360: 19691974.Google Scholar
Meierotto, S., Sharkey, M. J., Janzen, D. H. et al. (2019) A revolutionary protocol to describe understudied hyperdiverse taxa and overcome the taxonomic impediment. Deutsche Entomologische Zeitschrift 66: 119145. https://doi.org/10.3897/dez.66.34683Google Scholar
Meusnier, I., Singer, G. A. C., Landry, J.-F. et al. (2008) A universal DNA mini-barcode for biodiversity analysis. BioMed Central Genomics 9: 214[4 pp.]. https://doi.org/10.1186/1471-2164-9-214Google Scholar
Monaghan, M. T., Balke, M., Gregory, T. R., and Vogler, A. P. (2005) DNA-based species delineation in tropical beetles using mitochondrial and nuclear markers. Philosophical Transactions of the Royal Society (B) 360: 19251933.Google Scholar
Monaghan, M. T., Wild, R., Elliot, M. et al. (2009) Accelerated species inventory on Madagascar using coalescent-based models of species delineation. Systematic Biology 58: 298311.Google Scholar
Neyman, J. (1934) On the two different aspects of the representative method: The method of stratified sampling and the method of purposive sampling. Journal of the Royal Statistical Society 97: 558625.Google Scholar
Packer, L., Sheffield, C. S., Gibbs, J. et al. (2009) The campaign to barcode the bees of the world: Progress, problems, prognosis. In: Yurrita, C. L. (ed.) Memorias: VI Congresso Mesoamericano Sobre Abejas Nativas. Universidad de San Carlos de Guatemala, Centro de Estudios Conservacionistas, Guatemala, pp. 178180.Google Scholar
Padial, J. M., Miralles, A., De La Riva, I., and Vences, M. (2010) The integrative future of taxonomy. Frontiers in Zoology 7: 16. https://doi.org/10.1186/1742-9994-7-16Google Scholar
Paknia, O., Rajaei, H., and Koch, A. (2015) Lack of well-maintained natural history collections and taxonomists in megadiverse developing countries hampers global biodiversity exploration. Organisms Diversity and Evolution 15: 619629. https://doi.org/10.1007/s13127–015-0202-1CrossRefGoogle Scholar
Papadopoulou, A., Bergsten, J., Fujisawa, T. et al. (2008) Speciation and DNA barcodes: Testing the effects of dispersal on the formation of discrete sequence clusters. Philosophical Transactions of the Royal Society (B) 363: 29872996.Google Scholar
Papadopoulou, A., Monaghan, M. T., Barraclough, T. G., and Vogler, A. P. (2009) Sampling error does not invalidate the Yule-coalescent model for species delimitation: A response to Lohse (2009). Systematic Biology 58: 442444.Google Scholar
Phillips, J. D., Gillis, D. J., and Hanner, R. H. (2018) Incomplete estimates of genetic diversity within species: Implications for DNA barcoding. Ecology and Evolution: 115. https://doi.org/10.1002/ece3.4757Google Scholar
Potapov, G. S., Kondakov, A. V., Filippov, B .Y. et al. (2019) Pollinators on the polar edge of the Ecumene: Taxonomy, phylogeography, and ecology of bumble bees from Novaya Zemlya. Zookeys 866: 85115. https://doi.org/10.3897/zookeys.866.355084Google Scholar
Prathapan, K. D., Pethiyagoda, R., Bawa, K. S. et al. (2018) When the cure kills: CBD limits biodiversity research. Science 360(6396): 14051406. https://10.1126/science.aat9844Google Scholar
Rasmont, P. (1984) Les bourdons du genre Bombus Latreille sensu stricto en Europe occidentale et centrale (Hymenoptera, Apidae). Spixiana 7: 135160.Google Scholar
Ratnasingham, S. and Hebert, P. D. N. (2007) BOLD: The Barcode Of Life Data system (www.barcodinglife.org). Molecular Ecology Notes 2007: 110. 10.1111/j.1471-8286.2006.01678.xGoogle Scholar
Ratnasingham, S. and Hebert, P. D. N. (2013) A DNA-based registry for all animal species: The barcode index number (BIN) system. PLoS ONE 8: 116. https://doi.org/10.1371/journal.pone.0066213Google Scholar
Reinig, W. F. (1939) Die Evolutionsmechanismen, erläutert an den Hummeln. Verhandlungen der Deutschen zoologischen Gesellschaft (supplement) 12: 170206.Google Scholar
Ronquist, F. and Huelsenbeck, J. P. (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 15721574.Google Scholar
Schlick-Steiner, B. C., Steiner, F. M., Seifert, B. et al. (2010) Integrative taxonomy: A multisource approach to exploring biodiversity. Annual Review of Entomology 55: 421438. https://doi.org/10.116/annurev-ento-112408-085432Google Scholar
Schmidt, S., Schmid-Egger, C., Morniere, J., Haszprunar, G., and Hebert, P. D. N. (2015) DNA barcoding largely supports 250 years of classical taxonomy: Identifications for Central European bees (Hymenoptera, Apoidea partim). Molecular Ecology Resources 15: 9851000. https://doi.org/10.1111/1755-0998.12363Google Scholar
Strange, J. P., Knoblett, J., and Griswold, T. (2009) DNA amplification from pin-mounted bumble bees (Bombus) in a museum collection: Effects of fragment size and specimen age on successful PCR. Apidologie 40: 134139. https://doi.org/10.1051/apido/2008070Google Scholar
Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 27252729.Google Scholar
Vieites, D. R., Wollenberg, K. C., Andreone, F. et al. (2009) Vast underestimation of Madagascar’s biodiversity evidenced by an integrative amphibian inventory. PNAS 106: 82678272. https://doi.org/10.1073/pnas.0810821106CrossRefGoogle ScholarPubMed
Vogt, O. (1909) Studien über das Artproblem. 1. Mitteilung. Über das Variieren der Hummeln. 1. Teil. Sitzungsberichte der Gesellschaft naturforschender Freunde zu Berlin 1909: 2884.Google Scholar
Vogt, O. (1911) Studien über das Artproblem. 2. Mitteilung. Über das Variieren der Hummeln. 2. Teil. (Schluss). Sitzungsberichte der Gesellschaft naturforschender Freunde zu Berlin 1911: 3174.Google Scholar
Wickham, H. (2011) GGPLOT2. WIREs Computational Statistics 3: 180185. https://doi.org/10.1002/wics.147CrossRefGoogle Scholar
Williams, P. H. (1991) The bumble bees of the Kashmir Himalaya (Hymenoptera: Apidae, Bombini). Bulletin of the British Museum (Natural History) (Entomology) 60: 1204.Google Scholar
Williams, P. H. (1998) An annotated checklist of bumble bees with an analysis of patterns of description (Hymenoptera: Apidae, Bombini). Bulletin of The Natural History Museum (Entomology) 67: 79152 [updated at www.nhm.ac.uk/bombus/ accessed 2015].Google Scholar
Williams, P. H. (2011) Bumblebees collected by the Kyushu University Expeditions to Central Asia (Hymenoptera, Apidae, genus Bombus). Esakia 50: 2736.Google Scholar
Williams, P. H., Altanchimeg, D., Byvaltsev, A. et al. (2020) Widespread polytypic species or complexes of local species? Revising bumblebees of the subgenus Melanobombus world-wide (Hymenoptera, Apidae, Bombus). European Journal of Taxonomy 719: 1120. https://doi.org/10.5852/ejt.2020.719.1107Google Scholar
Williams, P. H., Berezin, M. V., Cannings, S. G. et al. (2019) The arctic and alpine bumblebees of the subgenus Alpinobombus revised from integrative assessment of species’ gene coalescents and morphology (Hymenoptera, Apidae, Bombus). Zootaxa 4625: 168. https://doi.org/10.11646/zootaxa.4625.1.1Google Scholar
Williams, P. H., Brown, M. J. F., Carolan, J. C. et al. (2012) Unveiling cryptic species of the bumblebee subgenus Bombus s. str. world-wide with COI barcodes (Hymenoptera: Apidae). Systematics and Biodiversity 10: 2156. https://doi.org/10.1080/14772000.2012.664574Google Scholar
Williams, P. H., Bystriakova, N., Huang, J.-X. et al. (2015a) Bumblebees, climate and glaciers across the Tibetan plateau (Apidae: Bombus Latreille). Systematics and Biodiversity 13: 164181. https://doi.org/10.1080/14772000.2014.982228Google Scholar
Williams, P. H., Byvaltsev, A. M., Cederberg, B. et al. (2015b) Genes suggest ancestral colour polymorphisms are shared across morphologically cryptic species in arctic bumblebees. PLoS ONE 10: 126. https://doi.org/10.1371/journal.pone.0144544Google Scholar
Williams, P. H., Cannings, S. G., and Sheffield, C. S. (2016) Cryptic subarctic diversity: A new bumblebee species from the Yukon and Alaska (Hymenoptera, Apidae). Journal of Natural History 50: 113. https://doi.org/10.1080/00222933.2016.1214294CrossRefGoogle Scholar
Williams, P. H., Huang, J.-X., and An, J.-D. (2017) Bear wasps of the Middle Kingdom: A decade of discovering China’s bumblebees. Antenna 41: 2124.Google Scholar
Williams, P. H., Huang, J.-X., Rasmont, P. et al. (2016) Early-diverging bumblebees from across the roof of the world: The high-mountain subgenus Mendacibombus revised from species’ gene coalescents and morphology (Hymenoptera, Apidae). Zootaxa 4204: 172. https://doi.org/10.11646/zootaxa.4204.1.1Google Scholar
Williams, P. H., Ito, M., Matsumura, T. et al. (2010) The bumblebees of the Nepal Himalaya (Hymenoptera: Apidae). Insecta Matsumurana 66: 115151.Google Scholar
Williams, P. H., Tang, Y., Yao, J. et al. (2009) The bumblebees of Sichuan (Hymenoptera: Apidae, Bombini). Systematics and Biodiversity 7: 101190. https://doi.org/10.1017/S1477200008002843Google Scholar
Williams, P. H., Thorp, R. W., Richardson, L. L., and Colla, S. R. (2014) Bumble Bees of North America: An Identification Guide. Princeton University Press, Princeton, NJ.Google Scholar
Zayed, A. and Packer, L. (2005) Complementary sex determination substantially increases extinction proneness of haplodiploid populations. Proceedings of the National Academy of Sciences 102: 1074210746.Google Scholar
Zhang, A.-B., He, L. J., Crozier, R. H., Muster, C., and Zhu, C.-D. (2010) Estimating sample sizes for DNA barcoding. Molecular Phylogenetics and Evolution 54: 10351039. https://doi.org/10.1016/.ympev.2009.09.014CrossRefGoogle ScholarPubMed
Zhang, J.-J., Kapli, P., Pavlidis, P., and Stamatakis, A. (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29: 28692876. https://doi.org/10.1093/bioinformatics/btt499Google Scholar

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