REVIEW
Cryptic diversity begets challenges and opportunities in biodiversity research
Rui CHENG,
Arong LUO,
Michael ORR,
Deyan GE,
Zhong'e HOU,
Yanhua QU,
Baocheng GUO,
Feng ZHANG,
Zhongli SHA,
Zhe ZHAO,
Mingqiang WANG,
Xiaoyu SHI,
Hongxiang HAN,
Qingsong ZHOU,
Yuanning LI,
Xingyue LIU,
Chen SHAO,
Aibing ZHANG,
Xin ZHOU,
Chaodong ZHU,
Rui CHENG
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorArong LUO
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorMichael ORR
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Entomologie, Staatliches Museum für Naturkunde Stuttgart, Stuttgart, Germany
Search for more papers by this authorDeyan GE
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorZhong'e HOU
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorYanhua QU
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorBaocheng GUO
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorFeng ZHANG
College of Plant Protection, Nanjing Agricultural University, Nanjing, China
Search for more papers by this authorZhongli SHA
Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China
Search for more papers by this authorZhe ZHAO
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorMingqiang WANG
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, China
Search for more papers by this authorXiaoyu SHI
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorHongxiang HAN
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorQingsong ZHOU
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorYuanning LI
Institute of Oceanography, Shandong University, Qingdao, China
Search for more papers by this authorXingyue LIU
Department of Entomology, China Agricultural University, Beijing, China
Search for more papers by this authorChen SHAO
College of Life Sciences, Shaanxi Normal University, Xi'an, China
Search for more papers by this authorAibing ZHANG
College of Life Science, Capital Normal University, Beijing, China
Search for more papers by this authorXin ZHOU
Department of Entomology, China Agricultural University, Beijing, China
Search for more papers by this authorCorresponding Author
Chaodong ZHU
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
State Key Laboratory of Integrated Pest Management, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
College of Life Sciences/International College, University of Chinese Academy of Sciences, Beijing, China
Correspondence: Chaodong Zhu, Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China. Email: [email protected]
Search for more papers by this author
Rui CHENG,
Arong LUO,
Michael ORR,
Deyan GE,
Zhong'e HOU,
Yanhua QU,
Baocheng GUO,
Feng ZHANG,
Zhongli SHA,
Zhe ZHAO,
Mingqiang WANG,
Xiaoyu SHI,
Hongxiang HAN,
Qingsong ZHOU,
Yuanning LI,
Xingyue LIU,
Chen SHAO,
Aibing ZHANG,
Xin ZHOU,
Chaodong ZHU,
Rui CHENG
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorArong LUO
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorMichael ORR
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Entomologie, Staatliches Museum für Naturkunde Stuttgart, Stuttgart, Germany
Search for more papers by this authorDeyan GE
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorZhong'e HOU
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorYanhua QU
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorBaocheng GUO
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorFeng ZHANG
College of Plant Protection, Nanjing Agricultural University, Nanjing, China
Search for more papers by this authorZhongli SHA
Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China
Search for more papers by this authorZhe ZHAO
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorMingqiang WANG
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, China
Search for more papers by this authorXiaoyu SHI
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorHongxiang HAN
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorQingsong ZHOU
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorYuanning LI
Institute of Oceanography, Shandong University, Qingdao, China
Search for more papers by this authorXingyue LIU
Department of Entomology, China Agricultural University, Beijing, China
Search for more papers by this authorChen SHAO
College of Life Sciences, Shaanxi Normal University, Xi'an, China
Search for more papers by this authorAibing ZHANG
College of Life Science, Capital Normal University, Beijing, China
Search for more papers by this authorXin ZHOU
Department of Entomology, China Agricultural University, Beijing, China
Search for more papers by this authorCorresponding Author
Chaodong ZHU
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
State Key Laboratory of Integrated Pest Management, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
College of Life Sciences/International College, University of Chinese Academy of Sciences, Beijing, China
Correspondence: Chaodong Zhu, Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China. Email: [email protected]
Search for more papers by this author
First published: 23 January 2024
Abstract
How many species of life are there on Earth? This is a question that we want to know but cannot yet answer. Some scholars speculate that the number of species may reach 2.2 billion when considering cryptic diversity and that each morphology-based insect species may contain an average of 3.1 cryptic species. With nearly two million described species, such high estimates of cryptic diversity would suggest that cryptic species are widespread. The development of molecular species delimitation has led to the discovery of a large number of cryptic species, and cryptic biodiversity has gradually entered our field of vision and attracted more attention. This paper introduces the concept of cryptic species, how they evolve, and methods by which they may be discovered and confirmed, and provides theoretical and methodological guidance for the study of hidden species. A workflow of how to confirm cryptic species is provided. In addition, the importance and reliability of multi-evidence-based integrated taxonomy are reaffirmed as a way to better standardize decision-making processes. Special focus on cryptic diversity and increased funding for taxonomy is needed to ensure that cryptic species in hyperdiverse groups are discoverable and described. An increased focus on cryptic species in the future will naturally arise as more difficult groups are studied, and thereby, we may finally better understand the rules governing the evolution and maintenance of cryptic biodiversity.
CONFLICT OF INTEREST
The authors declare no competing interests.
REFERENCES
- Adams BJ (1998). Species concepts and the evolutionary paradigm in modem nematology. Journal of Nematology 30, 1–21.
- Agnarsson I, Kuntner M (2007). Taxonomy in a changing world: Seeking solutions for a science in crisis. Systematic Biology 56, 531–539.
- Amor MD, Norman MD, Cameron HE, Strugnell JM (2014). Allopatric speciation within a cryptic species complex of Australasian octopuses. PLoS ONE 9, e98982.
- Andersen JJ, Light JE (2012). Phylogeography and subspecies revision of the hispid pocket mouse Chaetodipus hispidus (Rodentia: Heteromyidae). Journal of Mammalogy 93, 1195–1215.
- Andrews KR, Gerritsen A, Rashed A et al. (2020). Wireworm (Coleoptera: Elateridae) genomic analysis reveals putative cryptic species, population structure, and adaptation to pest control. Communications Biology 3, 489.
- Angulo A, Reichle S (2008). Acoustic signals, species diagnosis, and species concepts: the case of a new cryptic species of Leptodactylus (Amphibia, Anura, Leptodactylidae) from the Chapare region, Bolivia. Zoological Journal of the Linnean Society 152, 59–77.
- Ba JW, Lai DY (2009). Diversity of the cave-dwelling spiders and their adaptation to the cave environment in China. Acta Zootaxonomica Sinica 34, 98–105. (In Chinese with English abstract.)
- Barber PH, Erdmann MV, Palumbi SR (2006). Comparative phylogeography of three codistributed stomatopods: origins and timing of regional lineage diversification in the Coral Triangle. Evolution 60, 1825–1839.
- Barreto FS, Watson ET, Lima TG et al. (2018). Genomic signatures of mitonuclear coevolution across populations of Tigriopus californicus. Nature Ecology & Evolution 2, 1250–1257.
- Barton NH, Hewitt GM (1985). Analysis of hybrid zones. Annual Review of Ecology and Systematics 16, 113–148.
- Belyaeva M, Taylor DJ (2009). Cryptic species within the Chydorus sphaericus species complex (Crustacea: Cladocera) revealed by molecular markers and sexual stage morphology. Molecular Phylogenetics and Evolution 50, 534–546.
- Bickford D, Lohman DJ, Sodhi NS et al. (2007). Cryptic species as a window on diversity and conservation. Trends in Ecology Evolution 22, 148–155.
- Blaxter ML (2004). The promise of a DNA taxonomy. Philosophical Transactions of the Royal Society B: Biological Sciences 359, 669–679.
- Bánki O, Roskov Y, Vandepitte L et al. (2021). Catalogue of Life Checklist (Version 2021-08-25). Catalogue of Life. Available from URL: http://www.catalogueoflife.org
- Chai J, Lu CQ, Yi MR et al. (2022). Discovery of a wild, genetically pure Chinese giant salamander creates new conservation opportunities. Zoological Research 43, 469.
- Chattopadhyay B, Garg KM, Kumar AK et al. (2016). Genome-wide data reveal cryptic diversity and genetic introgression in an Oriental cynopterine fruit bat radiation. BMC Evolutionary Biology 16, 41.
- Chen SH (1946). Evolution of the insect larva. Transactions of the Royal Entomological Society of London 97, 381–404.
- Chen W, Bi K, Fu J (2009). Frequent mitochondrial gene introgression among high elevation Tibet megophryid frogs revealed by conflicting gene genealogies. Molecular Ecology 18, 2856–2876.
- Chen W, Ma X, Shen Y, Mao Y, He S (2015). The fish diversity in the upper reaches of the Salween River, Nujiang River, revealed by DNA barcoding. Scientific Reports 5, 17437.
- Cheng R, Jiang N, Xue D, Li X, Ban X, Han H (2016). The evolutionary history of Biston suppressaria (Guenée)(Lepidoptera: Geometridae) related to complex topography and geological history. Systematic Entomology 41, 732–743.
- Cheng R, Xue D, Galsworthy A, Han H (2017). Complete mitochondrial genomes throw light on budding speciation in three Biston species (Lepidoptera, Geometridae). Zoologica Scripta 46, 73–84.
- Chesters D, Wang Y, Yu F et al. (2012). The integrative taxonomic approach reveals host specific species in an Encyrtid parasitoid species complex. PLoS ONE 7, e37655.
- Chimeno C, Hausmann A, Schmidt S et al. (2022). Peering into the darkness: DNA barcoding reveals surprisingly high diversity of unknown species of Diptera (Insecta) in Germany. Insects 13, 82.
- Chornelia A, Lu J, Hughes AC (2022). How to accurately delineate morphologically conserved taxa and diagnose their phenotypic disparities: species delimitation in cryptic Rhinolophidae (Chiroptera). Frontiers in Ecology and Evolution 10, 854509.
- Cicero C (1996). Sibling Species of Titmice in the Parus inornatus complex (Aves: Paridae). University of California Press, Oakland, California, pp. 1–217.
- Collin R, Venera-Pontón DE, Driskell AC et al. (2020). DNA barcoding of echinopluteus larvae uncovers cryptic diversity in neotropical echinoids. Invertebrate Biology 139, e12292.
- Cong Q, Shen J, Borek D et al. (2017). When COI barcodes deceive: Complete genomes reveal introgression in hairstreaks. Proceedings of the Royal Society B: Biological Sciences 284, 20161735.
- Cooke GM, Chao NL, Beheregaray LB (2012). Five cryptic species in the Amazonian catfish Centromochlus existimatus identified based on biogeographic predictions and genetic data. PLoS ONE 7, e48800.
- Costa FO, DeWaard JR, Boutillier J et al. (2007). Biological identifications through DNA barcodes: The case of the Crustacea. Canadian Journal of Fisheries and Aquatic Sciences 64, 272–295.
- Costello MJ, May RM, Stork NE (2013). Response to comments on “Can we name Earth's species before they go extinct?”. Science 341, 237.
- Damm S, Schierwater B, Hadrys H (2010). An integrative approach to species discovery in odonates: From character-based DNA barcoding to ecology. Molecular Ecology 19, 3881–3893.
- Darwell CT, Cook JM (2017). Cryptic diversity in a fig wasp community-morphologically differentiated species are sympatric but cryptic species are parapatric. Molecular Ecology 26, 937–950.
- Dayrat B (2005). Towards integrative taxonomy. Biological Journal of the Linnean Society 85, 407–417.
- de Moya RS, Brown JK, Sweet AD et al. (2019). Nuclear orthologs derived from whole genome sequencing indicate cryptic diversity in the Bemisia tabaci (Insecta: Aleyrodidae) complex of whiteflies. Diversity 11, 151.
- De Queiroz K (2007). Species concepts and species delimitation. Systematic Biology 56, 879–886.
- Delić T, Trontelj P, Rendoš M, Fišer C (2017). The importance of naming cryptic species and the conservation of endemic subterranean amphipods. Scientific Reports 7, 3391.
- Dennis AB, Hellberg ME (2010). Ecological partitioning among parapatric cryptic species. Molecular Ecology 19, 3206–3225.
- Derkarabetian S, Steinmann DB, Hedin M (2010). Repeated and time-correlated morphological convergence in cave-dwelling harvestmen (Opiliones, Laniatores) from montane western North America. PLoS ONE 5, e10388.
- Derycke S, De Meester N, Rigaux A et al. (2016). Coexisting cryptic species of the Litoditis marina complex (Nematoda) show differential resource use and have distinct microbiomes with high intraspecific variability. Molecular Ecology 25, 2093–2110.
- Després L (2019). One, two or more species? Mitonuclear discordance and species delimitation. Molecular Ecology 28, 3845–3847.
- Dinsdale A, Cook L, Riginos C et al. (2010). Refined global analysis of Bemisia tabaci (Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyrodidae) mitochondrial cytochrome oxidase 1 to identify species level genetic boundaries. Annals of the Entomological Society of America 103, 196–208.
- Dyer LA, Singer MS, Lill JT et al. (2007). Host specificity of Lepidoptera in tropical and temperate forests. Nature 448, 696–699.
- Díaz S, Fargione J, Chapin FS III, Tilman D (2006). Biodiversity loss threatens human well-being. PLoS Biology 4, e277.
- Ehrlich PR (1961). Has the biological species concept outlived its usefulness? Systematic Zoology 10, 167–176.
- Erwin TL (1982). Tropical forests: Their richness in Coleoptera and other arthropod species. The Coleopterists Bulletin 36, 74–75.
- Fan X, Yao S, Luo X et al. (2021). Some morphologically distinguishable hypotrich ciliates share identical 18S rRNA gene sequences—Taxonomic insights from a case study on Oxytricha species (Protista, Ciliophora). Zoological Journal of the Linnean Society 193, 356–379.
- Felsenstein J (1985). Phylogenies and the comparative method. The American Naturalist 125, 1–15.
- Fennessy J, Bidon T, Reuss F et al. (2016). Multi-locus analyses reveal four giraffe species instead of one. Current Biology 2, 2543–2549.
- Fernandez-Triana JL (2022). Turbo taxonomy approaches: Lessons from the past and recommendations for the future based on the experience with Braconidae (Hymenoptera) parasitoid wasps. ZooKeys 1087, 199.
- Fišer C, Robinson CT, Malard F (2018). Cryptic species as a window into the paradigm shift of the species concept. Molecular Ecology 27, 613–635.
- Funk DJ, Omland KE (2003). Species-level paraphyly and polyphyly: Frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Review of Ecology, Evolution, and Systematics 34, 397–423.
- Garcia-Robledo C, Kuprewicz EK, Staines CL, Erwin TL, Kress WJ (2016). Limited tolerance by insects to high temperatures across tropical elevational gradients and the implications of global warming for extinction. PNAS 113, 680–685.
- Ge DY, Feijó A, Abramov AV et al. (2021). Molecular phylogeny and morphological diversity of the Niviventer fulvescens species complex with emphasize on species in China. Zoological Journal of the Linnean Society 191, 528–547.
- Ge DY, Lu L, Xia L et al. (2018). Molecular phylogeny, morphological diversity, and systematic revision of a species complex of common wild rat species in China (Rodentia, Murinae). Journal of Mammalogy 99, 1350–1374.
- Geml J, Laursen GA, O'NEILL K, Nusbaum HC, Taylor DL (2006). Beringian origins and cryptic speciation events in the fly agaric (Amanita muscaria). Molecular Ecology 15, 225–239.
- Gong J, Dong J, Liu X, Massana R (2013). Extremely high copy numbers and polymorphisms of the rDNA operon estimated from single cell analysis of oligotrich and peritrich ciliates. Protist 164, 369–379.
- Grundt HH, Kjølner S, Borgen L et al. (2006). High biological species diversity in the arctic flora. PNAS 103, 972–975.
- Han HX, Galsworthy A, Xue DY (2005). A taxonomic revision of Limbatochlamys Rothschild, 1894 with comments on its tribal placement in Geometrinae (Lepidoptera: Geometridae). Zoological Studies-Taipei 44, 191.
- Harrison RG (1991). Molecular changes at speciation. Annual Review of Ecology and Systematics 22, 281–308.
- Harrison RG (1993). Hybrids and hybrid zones: Historical perspective. In: RG Harrison, ed. Hybrid Zones and the Evolutionary Process. Oxford University Press, New York, pp. 3–13.
- Hartop E, Srivathsan A, Ronquist F, Meier R (2022). Towards large-scale integrative taxonomy (LIT): Resolving the data conundrum for dark taxa. Systematic Biology 71, 1404–1422.
- Havermans C (2016). Have we so far only seen the tip of the iceberg? Exploring species diversity and distribution of the giant amphipod Eurythenes. Biodiversity 17, 12–25
10.1080/14888386.2016.1172257 Google Scholar
- Hebert PD, Cywinska A, Ball SL, DeWaard JR (2003b). Biological identifications through DNA barcodes. Proceedings of the Royal Society B: Biological Sciences 270, 313–321.
- Hebert PD, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004). Ten species in one, DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. PNAS 101, 14812–14817.
- Hebert PD, Ratnasingham S, De Waard JR (2003a). Barcoding animal life: Cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society B: Biological Sciences 270, S96–S99.
- Hedin M (2015). High-stakes species delimitation in eyeless cave spiders (Cicurina, Dictynidae, Araneae) from central Texas. Molecular Ecology 24, 346–361.
- Heethoff M (2018). Cryptic species—conceptual or terminological chaos? A response to Struck et al. Trends in Ecology Evolution 33, 310.
- Hendrichs J, Vera MT, De Meyer M et al. (2015). Resolving cryptic species complexes of major tephritid pests. ZooKeys 540, 5.
- Henry CS (1994). Singing and cryptic speciation insects. Trends in Ecology Evolution 9, 388–392.
- Henry CS, Brooks SJ, Duelli P, Johnson JB (2003). A lacewing with the wanderlust: the European song species ‘Maltese’, Chrysoperla agilis sp.n., of the carnea group of Chrysoperla (Neuroptera: Chrysopidae). Systematic Entomology 28, 131–148.
- Henry CS, Wells MLM (2010). Acoustic niche partitioning in two cryptic sibling species of Chrysoperla green lacewings that must duet before mating. Animal Behaviour 80, 991–1003.
- Hinojosa JC, Koubínová D, Szenteczki MA et al. (2019). A mirage of cryptic species: Genomics uncover striking mitonuclear discordance in the butterfly Thymelicus sylvestris. Molecular Ecology 28, 3857–3868.
- Holland BS, Dawson MN, Crow GL, Hofman DK (2004). Global phylogeography of Cassiopea (Scyphozoa: Rhizostomeae): Molecular evidence for cryptic species and multiple invasions of the Hawaiian Islands. Marine Biology 145, 1119–1128.
- Hong D, Zhuang W, Zhu M et al. (2022). Positioning taxonomic research for the future. Zoological Systematics 47, 185–187.
- Hou Z, Jin P, Liu H et al. (2022). Past climate cooling promoted global dispersal amphipods from Tian Shan montane lakes to circumboreal lakes. Global Change Biology 28, 3830–3845.
- Hou Z, Li S (2010). Intraspecific or interspecific variation: Delimitation of species boundaries within the genus Gammarus (Crustacea, Amphipoda, Gammaridae), with description of four new species. Zoological Journal of the Linnean Society 160, 215–253.
- Huang J, Miao X, Wang Q et al. (2022). Metabarcoding reveals massive species diversity of Diptera in a subtropical ecosystem. Ecology and Evolution 12, e8535.
- Hupało K, Copilaș-Ciocianu D, Leese F, Weiss M (2023). Morphology, nuclear SNPs and mate selection reveal that COI barcoding overestimates species diversity in a Mediterranean freshwater amphipod by an order of magnitude. Cladistics 39, 129–143.
- Janzen DH, Burns JM, Cong Q et al. (2017). Nuclear genomes distinguish cryptic species suggested by their DNA barcodes and ecology. PNAS 114, 8313–8318.
- Janzen DH, Hajibabaei M, Burns JM et al. (2005). Wedding biodiversity inventory of a large and complex Lepidoptera fauna with DNA barcoding. Philosophical Transactions of the Royal Society B: Biological Sciences 360, 1835–1845.
- Jiang N, Liu SX, Xue DY, Tang MJ, Xiao Q, Han HX (2014). External morphology and molecular identification of two tea Geometrid moth from southern China. Chinese Journal of Applied Entomology 51, 987–1002. (In Chinese with English abstract.)
- Jiang N, Xue DY, Han HX, Cheng R (2021). Estimating hybridization as a consequence of climatic fluctuations: A case study of two geometridae species. Molecular Phylogenetics and Evolution 161, 107168.
- Johnston EC, Wyatt AS, Leichter JJ, Burgess SC (2022). Niche differences in co-occurring cryptic coral species (Pocillopora spp.). Coral Reefs 41, 767–778.
- Jones G, Barlow KE (2003). Cryptic species of echolocating bats. In: JA Thomas, C Moss, M Vater, eds. Echolocation in Bats and Dolphins. University of Chicago Press, Chicago, IL, pp. 345–349.
- Kaleka A, Kaur N, Bali G (2020). Larval development and molting. Edible Insects 560, 17.
- Kergoat GJ, Toussaint EF, Capdevielle-Dulac C et al. (2015). Integrative taxonomy reveals six new species related to the Mediterranean corn stalk borer Sesamia nonagrioides (Lefèbvre) (Lepidoptera, Noctuidae, Sesamiina). Zoological Journal of the Linnean Society 175, 244–270.
- Knowlton N (1993). Sibling species in the sea. Annual Review of Ecology and Systematics 24, 189–216.
10.1146/annurev.es.24.110193.001201 Google Scholar
- Korshunova T, Martynov A, Bakken T, Picton B (2017). External diversity is restrained by internal conservatism: New nudibranch mollusc contributes to the cryptic species problem. Zoologica Scripta 46, 683–692.
- Kress WJ, Garcia-Robledo C, Uriarte M, Erickson DL (2015). DNA barcodes for ecology, evolution, and conservation. Trends in Ecology Evolution 30, 25–35.
- Kruckenhauser L, Duda M, Bartel D et al. (2014). Paraphyly and budding speciation in the hairy snail (Pulmonata, Hygromiidae). Zoologica Scripta 43, 273–288.
- Laurance WF (2013). The race to name Earth's species. Science 339, 1275–1275.
- Lee T, Ó Foighil D (2004). Hidden Floridian biodiversity: mitochondrial and nuclear gene trees reveal four cryptic species within the scorched mussel, Brachidontes exustus, species complex. Molecular Ecology 13, 3527–3542.
- Lefébure T, Douady C J, Gouy M et al. (2006). Phylogeography of a subterranean amphipod reveals cryptic diversity and dynamic evolution in extreme environments. Molecular Ecology 15, 1797–1806.
- Lei FM, Payne RB (2002). Territorial songs of the Drongo Cuckoo complex (Surniculus lugubris & S. velotinus). The Raffles Bulletin of Zoology 50, 205–213.
- Lei FM, Zhao HF, Wang G, Payne RB (2003). Vocalizations and species limits of the plaintive cuckoo (Cacomantis merulinus) and the brush cuckoo (C. variolosus). Folia Zoology 52, 399–412.
- Li X, Wiens JJ (2023). Estimating global biodiversity: The role of cryptic insect species. Systematic Biology 72, 391–403.
- Liu J, Li Q, Kong LF, Zheng XD (2011). Cryptic diversity in the pen shell Atrina pectinata (Bivalvia: Pinnidae): High divergence and hybridization revealed by molecular and morphological data. Molecular Ecology 20, 4332–4345.
- Liu JQ (2016). “The integrative species concept” and “species on the speciation way”. Biodiversity science 24, 1004–1008.
10.17520/biods.2016222 Google Scholar
- Liu M, Liu Y, Zhang T et al. (2022). Integrative studies on the taxonomy and molecular phylogeny of four new Pleuronema species (Protozoa, Ciliophora, Scuticociliatia). Marine Life Science Technology 4, 179–200.
- Liu Y, Song Y, Li XY (2010). Application of DNA barcoding technology based on mitochondrial COI gene in insect molecular identification. Plant Quarantine 24, 46–50. (In Chinese with English abstract.)
- Luo C, Yao Y, Wang RJ, Yan FM, Hu DX, Zhang ZL (2002). The use of mitochondrial cytochrome oxidase I (Mt COI) gene sequences for the identification of biotypes of Bemisia tabaci (Gennadius) in China. Acta Entomologica Sinica 45, 759–763. (In Chinese with English abstract.)
- Mallet J (2005). Hybridization as an invasion of the genome. Trends in Ecology and Evolution 20, 229–237.
- Marshall DC, Cooley JR (2000). Reproductive character displacement and speciation in periodical cicadas, with description of a new species, 13-year Magicicada neotredecim. Evolution 54, 1313–1325.
- Martinet B, Lecocq T, Brasero N et al. (2019). Integrative taxonomy of an arctic bumblebee species complex highlights a new cryptic species (Apidae: Bombus). Zoological Journal of the Linnean Society 187, 599–621.
- Mata VA, Ferreira S, Campos RM et al. (2021). Efficient assessment of nocturnal flying insect communities by combining automatic light traps and DNA metabarcoding. Environmental DNA 3, 398–408.
10.1002/edn3.125 Google Scholar
- Mayr AV, Keller A, Peters MK et al. (2021). Cryptic species and hidden ecological interactions of halictine bees along an elevational gradient. Ecology and Evolution 11, 7700–7712.
- Mayr E (1963). Animal Species and Evolution. The Belknap Press, Cambridge, MA.
10.1111/j.0022-1112.2004.00433.x Google Scholar
- Mayr E (1982). Of what use are subspecies? The Auk 99, 593–595.
- Meier R, Blaimer BB, Buenaventura E et al. (2022). A re-analysis of the data in Sharkey et al.’s 2021 minimalist revision reveals that BINs do not deserve names, but BOLD Systems needs a stronger commitment to open science. Cladistics 38, 264–275.
- Michener CD (2007). The Bees of the World. Johns Hopkins University Press, Baltimore, MD, USA.
10.56021/9780801885730 Google Scholar
- Moen DS, Irschick DJ, Wiens JJ (2013). Evolutionary conservatism and convergence both lead to striking similarity in ecology, morphology and performance across continents in frogs. Proceedings of the Royal Society B: Biological Sciences 280, 20132156.
- Mora C, Tittensor DP, Adl S et al. (2011). How many species are there on Earth and Murray in the ocean? PLoS Biology 9, e1001127.
- Ge D, Feijó A, Wen Z et al. (2022). Ancient introgression underlying the unusual mito-nuclear discordance and coat phenotypic variation in the Mouping pika. Diversity and Distributions 28, 2593–2609.
- Murray TE, Fitzpatrick U, Brown MJ, Paxton RJ (2008). Cryptic species diversity in a widespread bumble bee complex revealed using mitochondrial DNA RFLPs. Conservation Genetics 9, 653–666.
- Nair A, Gopalan S V, George S et al. (2012). High cryptic diversity of endemic Indirana frogs in the Western Ghats biodiversity hotspot. Animal Conservation 15, 489–498.
- Narins PM (1983). Divergence of acoustic communication systems of two sibling species of eleutherodactylid frogs. Copeia 4, 1089–1090.
10.2307/1445115 Google Scholar
- Nevo E (2001). Evolution of genome-phenome diversity under environmental stress. PNAS 98, 6233–6240.
- Niemiller ML, Graening GO, Fenolio DB et al. (2013). Doomed before they are described? The need for conservation assessments of cryptic species complexes using an amblyopsid cavefish (Amblyopsidae: Typhlichthys) as a case study. Biodiversity and Conservation 22, 1799–1820.
- Orr MC, Ascher JS, Bai M, Chesters D, Zhu CD (2020). Three questions: How can taxonomists survive and thrive worldwide? Megataxa 1, 19–27.
10.11646/megataxa.1.1.4 Google Scholar
- Orr MC, Feijó A, Chesters D, Vogler AP, Bossert S et al. (2022). Six steps for building a technological knowledge base for future taxonomic work. National Science Review 9, nwac284.
- Ottenburghs J (2020). Ghost introgression: Spooky gene flow in the distant past. Bioessays 42, e2000012.
- Padial JM, Miralles A, De la Riva I, Vences M (2010). The integrative future of taxonomy. Frontiers in Zoology 7, 16.
- Pearce T (2011). Convergence and parallelism in evolution: A neo-Gouldian account. The British Journal for the Philosophy of Science 63, 429–448.
- Pekár S (2014). Comparative analysis of passive defences in spiders (Araneae). Journal of Animal Ecology 83, 779–790.
- Peng JL, Wang XZ, He SP (2008). The progress and application of DNA barcoding. Acta Hydrobiologica Sinica 32, 916–919. (In Chinese with English abstract.)
- Pfenninger M, Schwenk K (2007). Cryptic animal species are homogeneously distributed among taxa and biogeographical regions. BMC Evolutionary Biology 7, 121.
- Pfingstl T, Lienhard A, Baumann J, Koblmüller S (2021). A taxonomist's nightmare–Cryptic diversity in Caribbean intertidal arthropods (Arachnida, Acari, Oribatida). Molecular Phylogenetics and Evolution 163, 107240.
- Ritter CD, Häggqvist S, Karlsson D et al. (2019). Biodiversity assessments in the 21st century: The potential of insect traps to complement environmental samples for estimating eukaryotic and prokaryotic diversity using high-throughput DNA metabarcoding. Genome 62, 147–159.
- Rothschild LJ, Mancinelli RL (2001). Life in extreme environments. Nature 409, 1092–1101.
- Rowe KC, Aplin KP, Baverstock PR, Moritz C (2011). Recent and rapid speciation with limited morphological disparity in the genus Rattus. Systematic Biology 60, 188–203.
- Ruppert KM, Kline RJ, Rahman MS (2019). Past, present, and future perspectives of environmental DNA (eDNA) metabarcoding: A systematic review in methods, monitoring, and applications of global eDNA. Global Ecology and Conservation 17, e00547.
- Ruxton GD (2009). Non-visual crypsis: A review of the empirical evidence for camouflage to senses other than vision. Philosophical Transactions of the Royal Society B: Biological Sciences 364, 549–557.
- Schönrogge K, Barr B, Wardlaw JC et al. (2002). When rare species become endangered: cryptic speciation in myrmecophilous hoverflies. Biological Journal of the Linnean Society 75, 291–300.
- Scriven JJ, Whitehorn PR, Goulson D, Tinsley MC (2016). Niche partitioning in a sympatric cryptic species complex. Ecology and Evolution 6, 1328–1339.
- Shao C, Hu C, Fan Y, Warren A, Lin X (2019). Morphology, morphogenesis and molecular phylogeny of a fresh water ciliate, Monomicrocaryon euglenivorum euglenivorum (Ciliophora, Oxytrichidae). European Journal of Protistology 68, 25–36.
- Sharkey MJ, Janzen DH, Hallwachs W et al. (2021). Minimalist revision and description of 403 new species in 11 subfamilies of Costa Rican braconid parasitoid wasps, including host records for 219 species. ZooKeys 1013, 1–665.
- Shen Y, Hubert N, Huang Y et al. (2019). DNA barcoding the ichthyofauna of the Yangtze River: Insights from the molecular inventory of a mega-diverse temperate fauna. Molecular Ecology Resources 19, 1278–1291.
- Simmons RB, Scheffer SJ (2004). Evidence of cryptic species within the pest Copitarsia decolora (Guenée) (Lepidoptera: Noctuidae). Annals of the Entomological Society of America 97, 675–680.
- Sokal RR, Crovello TJ (1970). The biological species concept: A critical evaluation. The American Naturalist 104, 127–153.
- Stamos DN (2003). The Species Problem: Biological Species, Ontology, and the Metaphysics of Biology. Lexington Books, Lanham, MA.
- Steane DA, Potts BM, McLean E et al. (2015). Genome-wide scans reveal cryptic population structure in a dry-adapted eucalypt. Tree Genetics & Genomes 11, 33.
- Stork NE (2018). How many species of insects and other terrestrial arthropods are there on Earth? Annual Review of Entomology 63, 31–45.
- Struck TH, Cerca J (2019). Cryptic species and their evolutionary significance. In: Encyclopedia of Life Sciences. Wiley, New York, pp. 1–9. https://doi.org/10.1002/9780470015902.a0028292
10.1002/9780470015902.a0028292 Google Scholar
- Struck TH, Feder JL, Bendiksby M et al. (2018). Finding evolutionary processes hidden in cryptic species. Trends in Ecology Evolution 33, 153–163.
- Suh KI, Hwang JM, Bae YJ, Kang JH (2019). Comprehensive DNA barcodes for species identification and discovery of cryptic diversity in mayfly larvae from South Korea: Implications for freshwater ecosystem biomonitoring. Entomological Research 49, 46–54.
- Swift HF, Daglio LG, Dawson MN (2016). Three routes to crypsis: stasis, convergence, and Sun parallelism in the Mastigias species complex (Scyphozoa, Rhizostomeae). Molecular Phylogenetics and Evolution 99, 103–115.
- Tang M, Hardman CJ, Ji Y et al. (2015). High-throughput monitoring of wild bee diversity and abundance via mitogenomics. Methods in Ecology and Evolution 6, 1034–1043.
- Tattersall I (2007). Madagascar's lemurs: cryptic diversity or taxonomic inflation? Evolutionary Anthropology 16, 12–23.
- Tautz D, Arctander P, Minelli A, Thomas RH, Vogler AP (2002). DNA points the way ahead in taxonomy. Nature 418, 479.
- Tautz D, Arctander P, Minelli A, Thomas RH, Vogler AP (2003). A plea for DNA taxonomy. Trends in Ecology & Evolution 18, 70–74.
- Trontelj P, Douady CJ, Fišer C et al. (2009). A molecular test for cryptic diversity in ground water: How large are the ranges of macro-stygobionts? Freshwater Biology 54, 727–744.
- Tyagi K, Kumar V, Singha D et al. (2017). DNA Barcoding studies on Thrips in India: Cryptic species and species complexes. Scientific Reports 7, 4898.
- Utsunomiya YT, Pérez O'Brien AM, Sonstegard TS et al. (2013). Detecting loci under recent positive selection in dairy and beef cattle by combining different genome-wide scan methods. PLoS ONE 8, e64280.
- Van Campenhout J, Derycke S, Moens T, Vanreusel A (2014). Differences in life-histories refute ecological equivalence of cryptic species and provide clues to the origin of bathyal Halomonhystera (Nematoda). PLoS ONE 9, e111889.
- Vodă R, Dapporto L, Dincă V, Vila R (2015a). Cryptic matters: Overlooked species generate most butterfly beta-diversity. Ecography 38, 405–409.
- Vodă R, Dapporto L, Dincă V, Vila R (2015b). Why do cryptic species tend not to co-occur? A case study on two cryptic pairs of butterflies. PLoS ONE 10, e0117802.
- Vrijenhoek RC, Schutz SJ, Gustafson RG et al. (1994). Cryptic species of deep-sea clams (Mollusca: Bivalvia: Vesicomyidae) from hydrothermal vent and cold-water seep environments. Deep Sea Research Part I: Oceanographic Research Papers 41, 1171–1189.
- Wang T, Zhang YP, Yang ZY, Liu Z, Du YY (2020). DNA barcoding reveals cryptic diversity in the underestimated genus Triplophysa (Cypriniformes: Cobitidae, Nemacheilinae) from the northeastern Qinghai-Tibet Plateau. BMC Evolutionary Biology 20, 151.
- Wang W, Dai C, Alström P et al. (2014). Past hybridization between two East Asian long-tailed tits (Aegithalos bonvaloti and A. fuliginosus). Frontiers in Zoology 11, 40.
- Weigand H, Weiss M, Cai H et al. (2017). Deciphering the origin of mito-nuclear discordance in two sibling caddisfly species. Molecular Ecology 26, 5705–5715.
- Weisbecker V, Archer M (2008). Parallel evolution of hand anatomy in kangaroos and vombatiform marsupials: Functional and evolutionary implications. Palaeontology 51, 321–338.
- Westwood J0 (1833). On the probable number of species of insects in the creation; together with descriptions of several minute Hymenoptera. The Magazine of Natural History and Journal of Zoology, Botany, Mineralogy, Geology, and Meteorology 6, 116–123.
- Wilkins JS (2006). The concept and causes of microbial species. History and Philosophy of the Life Sciences 28, 389–407.
- Wilkins JS (2009). Defining Species: A Sourcebook from Antiquity to Today, vol. 203. Peter Lang, New York.
- Williams PH, Brown MJ, Carolan JC et al. (2012). Unveiling cryptic species of the bumblebee subgenus Bombus s. str. worldwide with COI barcodes (Hymenoptera: Apidae). Systematics and Biodiversity 10, 21–56.
- Willig MR, Kaufman DM, Stevens RD (2003). Latitudinal gradients of biodiversity: Pattern, process, scale, and synthesis. Annual Review of Ecology, Evolution, and Systematics 34, 273–309.
- Winker K (2005). Sibling species were first recognized by William Derham (1718). Auk 122, 706–707.
- Witt JDS, Threloff DL, Hebert PDN (2006). DNA barcoding reveals extraordinary cryptic diversity in an amphipod genus: Implications for desert spring conservation. Molecular Ecology 15, 3073–3082.
- Wu HC, Lin RC, Hung HY et al. (2011). Molecular and morphological evidences revealed the cryptic species in the vinaceous rosefinch Carpodacus vinaceus (Fringillidae; Aves). Zoologica Scripta 40, 468–478.
- Xiao JH, Xiao H, Huang DW (2004). DNA barcoding: New approach of biological taxonomy. Acta Zoologica Sinica 50, 852–855. (In Chinese with English abstract.)
- Xiong F, Shu L, Gan X, Zeng H, He S, Peng Z (2022). Methodology for fish biodiversity monitoring with environmental DNA metabarcoding: the primers, databases and bioinformatic pipelines. Water Biology and Security 1, 100007.
10.1016/j.watbs.2022.100007 Google Scholar
- Xu W, Che J (2019). From cryptic species to biodiversity conservation in China: Status and prospects. Scientia Sinica Vitae 49, 519–530. (In Chinese with English abstract.)
10.1360/N052018-00229 Google Scholar
- Yamamoto S, Sota T (2007). Phylogeny of the Geometridae and the evolution of winter moths inferred from a simultaneous analysis of mitochondrial and nuclear genes. Molecular Phylogenetics and Evolution 44, 711–723.
- Yan F, Lü J, Zhang B et al. (2018). The Chinese giant salamander exemplifies the hidden extinction of cryptic species. Current Biology 28, R590–R592.
- Yang XJ, Lei FM (2008). Song structure and its microgeographic variation in the Chinese bulbul Pycnonotus sinensis. Acta Zoologica Sinica 54, 630–639. (In Chinese with English abstract.)
- Yu HJ, Wang Q (2021). Application of DNA barcoding for species identification in aquatic animal. Anhui Agricultural Sciences 49, 1–3. (In Chinese with English abstract.)
- Zakharov EV, Lobo NF, Nowak C, Hellmann JJ (2009). Introgression as a likely cause of mtDNA paraphyly in two allopatric skippers (Lepidoptera: Hesperiidae). Heredity (Edinb) 102, 590–599.
- Zenker MM, Specht A, Fonseca VG (2020). Assessing insect biodiversity with automatic light traps in Brazil: Pearls and pitfalls of metabarcoding samples in preservative ethanol. Ecology and Evolution 10, 2352–2366.
- Zhang DY, Lin K, Hanski I (2004). Coexistence of cryptic species. Ecology Letters 7, 165–169.
- Zhang Y, Li S (2014). A spider species complex revealed high cryptic diversity in South China caves. Molecular Phylogenetics and Evolution 79, 353–358.
- Zhou QS, Polaszek A, Qin YG et al. (2017). Parasitoid–host associations of the genus Coccophagus (Hymenoptera: Aphelinidae) in China. Zoological Journal of the Linnean Society 182, 38–49.
- Zhou X, Guang X, Sun D et al. (2018). Population genomics of finless porpoises reveal an incipient cetacean species adapted to freshwater. Nature Communications 9, 1276.
- Zhou X, Li Y, Liu S et al. (2013). Ultra-deep sequencing enables high-fidelity recovery of biodiversity for bulk arthropod samples without PCR amplification. GigaScience 2, 4.
- Zhu C, Luo A, Bai M et al. (2022). A joint call for actions to advance taxonomy in China. Zoological Systematics 47, 188–197.
