Document Type : Original Article

Authors

1 Department of Biology, Faculty of Sciences, Ferdowsi University of Mashhad, Mashhad, Iran

2 Department of Medical Entomology and Vector Control, School of Health, Shiraz University of Medical Sciences, Shiraz, Iran

3 Department of Crop Productions Technology, Faculty of Agriculture, Higher Educational Complex of Saravan, Saravan, Iran

Abstract

Background: Morphological and allozyme studies are not remarkably efficient in identification of cryptic and unknown species; therefore, the differences between intra-and interspecific genetic variation (DNA barcoding) have been applied in recent decades. Applying molecular markers has been common for identification of taxa, so that suitable marker choice representing high divergence is a crucial issue to reveal taxonomic status of the taxa in this approach.
Methods: In this analytical study, the performance of two mitochondrial markers including cytochrome c oxidase subunit I (COI) and cytochrome b (cyt b)was compared with nuclear recombination activating protein I locus(RAGI), and their efficiency in identification of mammal taxa as the host of zoonotic diseases was evaluated. The COI, cyt b, and RAGI sequences were retrieved from GenBank. Intra-and interspecific genetic distances were estimated and compared at the species level. The variances in genetic divergence were also calculated and compared between the markers.
 Results: Our results showed a wide gap between intra-and interspecific genetic distances for both COI and cyt b markers and less apparent gap for RAGI, indicating that this nuclear marker is less proper for species delimitation in DNA barcoding.
Conclusion: We concluded that in the case of multiple sequences available COI, contributes to accurate differentiation at the species level, showing a significant gap between intra-and interspecific genetic distances and may play an important role as DNA barcoding marker.

Keywords

1        Avise JC. Molecular Markers, Natural History, and Evolution. 2nd. Sunderland (MA): Sinauer; 2004.
2        Roe AD, Sperling FAH. Patterns of evolution of mitochondrial cytochrome c oxidase I and II DNA and implications for DNA barcoding. Molecular Phylogenetics and Evolution. 2007; 44: 325–345.
3        Ranwez V, Delsuc F, Ranwez S, Belkhir K, Tilak MK, Douzery EJ. OrthoMaM: a database of orthologous genomic markers for placental mammal phylogenetics. BMC Evolutionary Biology. 2007; 7: 241.
4        Mohammadi Z, Darvish J, Aliabadian M, Yazdani Moghaddam F, Lissovsky AA, Olsson U. Pleistocene diversification of Afghan pikas Ochotona rufescens (Gray, 1842) (Lagomorpha; Ochotonidae) in Western Asia. Mammalian Biology. 2018; 91: 10–22.
5        Regier JC, Shultz JW, Kambic RE. Pancrustacean phylogeny: hexapods are terrestrial crustaceans and maxillopods are not monophyletic. Proceedings of the Royal Society of London series B, Biological sciences. 2005; 272: 395–401.
6        Blair JE, Hedges SB. Molecular phylogeny and divergence times of deuterostome animals. Molecular Biology and Evolution. 2005; 22: 2275–2284.
7        Bowen WD. Role of marine mammals in aquatic ecosystems. Marine Ecology Progress Series. 1997; 158: 267–274.
8        Woodruff DS. Non-invasive genotyping and field studies of free-ranging non-human primates. In: Chapais B, Berman C. (eds.) Kinship and behavior in primates. Oxford, UK: Oxford University Press; 2003. pp. 46–68.
9        Eizirik E, Murphy WJ, O'Brien SJ. Molecular dating and biogeography of the early placental mammal radiation. Journal of Heredity. 2001; 92: 212–219.
10    Wan XF, Xu D, Kleinhofs A, Zhou J. Quantitative relationship between synonymous codon usage bias and GC composition across unicellular genomes. BMC Evolutionary Biology. 2004; 4: 19.
11    González S, Duarte JMB. Noninvasive methods for genetic analysis applied to ecological and behavioral studies in Latino-America. Revista Brasileira de Zootecnia. 2007; 36: 89–92.
12    Eaton MJ, Meyers GL, Kolokotronis S-O, Leslie MS, Martin AP, Amato G. Barcoding bushmeat: molecular identification of Central African and South American harvested vertebrates. Conservation Genetics. 2010; 11(4): 1389–1404.
13    Hajibabaei M, Singer GAC, Hebert PDN, Hickey DA. DNA barcoding: how it complements taxonomy, molecular phylogenetics and population genetics. Trends in Genetics. 2007; 23: 167–172.
14    Parker PG, Snow AA, Schug MD, Booton GC, Fuerst PA. What molecules can tell us about populations: choosing and using a molecular marker. Ecology. 1998; 79: 361–382.
15    Thomson RC, Wang IJ, Johnson JR. Genome-enabled development of DNA markers for ecology, evolution and conservation. Molecular Ecology. 2010; 19: 2184–2195.
16    Pfenninger M, Schwenk K. Cryptic animal species are homogeneously distributed among taxa and biogeographical regions. BMC Evolutionary Biology. 2007; 7: 121.
17    Hulva P, Horáček I, Benda P. Molecules, morphometrics and new fossils provide an integrated view of the evolutionary history of Rhinopomatidae (Mammalia: Chiroptera). BMC Evolutionary Biology. 2007; 7: 165.
18    Furman A, Postawa T, Öztunç T, Çoraman E. Cryptic diversity of the bent-wing bat, Miniopterus schreibersii (Chiroptera: Vespertilionidae), in Asia Minor. BMC Evolutionary Biology. 2010; 10: 121.
19    Yazbeck GM, Brandão RL, Cunha HM, Paglia AP. Detection of two morphologically cryptic species from the cursor complex (Akodon spp; Rodentia, Cricetidae) through the use of RAPD markers. Genetics and Molecular Research. 2011; 10(4): 2881-2892.
20    Salicini I, Ibáñez C, Juste J. Deep differentiation between and within Mediterranean glacial refugia in a flying mammal, the Myotis nattereri bat complex. Journal of Biogeography. 2013; 40: 1182-1193.
21    Balloux F, Lugon-Moulin N. The estimation of population differentiation with microsatellite markers. Molecular Ecology. 2002; 11(2): 155-65.
22    Zhang DX, Hewitt GM. Nuclear DNA analyses in genetic studies of populations: practice, problems and prospects. Molecular Ecology. 2003; 12: 563–584.
23    Parsons KM, Durban JW, Claridge DE, Herzing DL, KC Balcomb I, Noble LR. Population genetic structure of coastal bottlenose dolphins (Tursiops truncatus) in the northern Bahamas. Marine Mammal Science. 2006; 22: 276–298.
24    Meyer CP, Paulay G. DNA Barcoding: Error Rates Based on Comprehensive Sampling. PLOS Biology. 2005; 3(12): e422.
25    Rivière-Dobigny T, Herbreteau V, Khamsavath K, Douangboupha B, Morand S, Michaux JR, Hugot JP. Preliminary assessment of the genetic population structure of the enigmatic species Laonastes aenigmamus (Rodentia: Diatomyidae). Journal of Mammalogy. 2011; 92(3): 620–628.
26    Barton HD, Wisely SM. Phylogeography of striped skunks (Mephitis mephitis) in North America: Pleistocene dispersal and contemporary population structure. Journal of Mammalogy. 2012; 93: 38–51.
27    Lohse K. Can mtDNA Barcodes Be Used to Delim it Species? A Response to Pons et al. (2006). Systematic Biology. 2009; 58(4): 439–442.
28    Linacre A, Tobe SS. An overview to the investigative approach to species testing in wildlife forensic science. Investigative Genetics. 2011; 2: 2.
29    Lim BK. Preliminary assessment of Neotropical mammal DNA barcodes: an underestimation of biodiversity. The Open Zoology Journal. 2012; 5: 10–17.
30    Ebach MC, Holdrege C. DNA barcoding is no substitute for taxonomy. Nature. 2005; 434: 697.
31    Rubinoff D, Cameron S, Will K. Are plant DNA barcodes a search for the Holy Grail? Trends in Ecology and Evolution. 2006; 21: 1-2.
32    Waugh J. DNA barcoding in animal species: progress, potential and pitfalls. Bioessays. 2007; 29: 188–197.
33    Shen YY, Chen X, Murphy RW. Assessing DNA barcoding as a tool for species identification and data quality control. PLoS One. 2013; 8: e57125.
34    Galimbertia A, Sandionigia A, Brunoa A, Bellatib A, Casiraghia M. DNA barcoding in mammals: what’s new and where next? Hystrix, the Italian Journal of Mammalogy. 2015; 26(1): 13–24.
35    Wörheide G, Solé-Cava A, Hooper JNA. Biodiversity, Molecular Ecology and Phylogeography of Marine Sponges: Patterns, Implications and Outlooks. Integrative and Comparative Biology. 2005; 45(2): 377-385.
36    Pfrender ME, Hawkins CP, Bagley MC, Courtney GW, Creutzburg BR, Epler JH, Fend SV, Schindel D, Ferrington LC, Hartzell PL, Jackson SH, Larsen DP, Levesque AJ, Morse JC, Petersen MJ, Ruiter DD, Whiting M. Assessing macroinvertebrate biodiversity in freshwater ecosystems: advances and challenges in DNA-based approaches. The Quarterly review of biology. 2010; 85(3): 319-340.
37    Andújar C, Arribas P, Gray C, Bruce C, Woodward G, Yu DW, Vogler AP. Metabarcoding of freshwater invertebrates to detect the effects of a pesticide spill. Molecular Ecology. 2018; 27(1): 146-166.
38    Galimberti A, Martinoli A, Russo D, Mucedda M, Casiraghi M. Molecular identification of Italian Mouse-eared bats (genus Myotis). In: Nimis PL, Vignes Lebbe R (eds.) Tools for identifying biodiversity: Progress and problems. Edizioni: Università di Trieste; 2010. pp.289–294.
39    Luo A, Zhang A, Ho SYW, Xu W, Zhang Y, Shi W, Cameron SL, Zhu C. Potential efficacy of mitochondrial genes for animal DNA barcoding: A case study using eutherian mammals. BMC Genomics. 2011; 12: 84.
40    Ferreira PB, Torres RA, Garcia JE. Single nucleotide polymorphisms from cytochrome b gene as a useful protocol in forensic genetics against the illegal hunting of manatees: Trichechus manatus, Trichechus inunguis, Trichechus senegalensis, and Dugong dugon (Eutheria: Sirenia). Zoologia. 2011; 28(1): 133-138.
41    Agrizzi J, Loss AC, Farro APC, Duda R, Costa LP, Leite YL. Molecular diagnosis of Atlantic forest mammals using mitochondrial DNA sequences: didelphid marsupials. The Open Zoology Journal. 2012; 5: 2–9.
42    Bijukumar A, Jijith SS, Kumar US, George S. DNA barcoding of the Bryde's Whale Balaenoptera edeni Anderson (Cetacea: Balaenopteridae) washed ashore along Kerala coast, India. Journal of Threatened Taxa. 2012; 4(3): 2436-2443.
43    Alfonsi E, Méheust E, Fuchs S, Carpentier F-G, Quillivic Y, Viricel A, Hassani S, Jung J-L. The use of DNA barcoding to monitor the marine mammal biodiversity along the French Atlantic coast. In: Nagy ZT, Backeljau T, De Meyer M, Jordaens K (eds.) DNA barcoding: a practical tool for fundamental and applied biodiversity research. ZooKeys. 2013; 365: 5–24.
44    Waddell PJ, Shelley S. Evaluating placental inter-ordinal phylogenies with novel sequences including RAGI, gamma-fibrinogen, ND6, and mt-tRNA, plus MCMC-driven nucleotideamino acid, and codon models. Molecular Phylogenetics and Evolution. 2003; 28: 197–224.
45    Jumawan JC, Vallejo BM, Herrera A, Buerano CC, Fontanilla IKC. DNA barcodes of the suckermouth sailfin catfish. Philippine science letters. 2011; 4: 103–113.
46    Crottini A, Gehring P-S, Glaw F, Harris DJ, Lima A, Vences M. Deciphering the cryptic species diversity of dull-coloured day geckos Phelsuma (Squamata: Gekkonidae) from Madagascar, with description of a new species. Zootaxa. 2011; 2982: 40-48.
47    Fabre P, Hautier L, Dimitrov D, Douzery EJP. A glimpse on the pattern of rodent diversification: a phylogenetic approach. BMC Evolutionary Biology. 2012; 12:1–19.
48    Nijman V, Aliabadian M. DNA barcoding as a tool for elucidating species delineation in wide-ranging species as illustrated by owls (Tytonidae and Strigidae). Zoological Science. 2013; 30(11): 1005-1009.
49    Shahabi S, Aliabadian M, Darvish J, Kilpatrick CW. Molecular phylogeny of brush-tailed mice of the genus Calomyscus (Rodentia: Calomyscidae) inferred from mitochondrial DNA sequences (Cox1 gene). Mammalia. 2013; 77(4): 425-431.
50    Hebert PDN, Cywinska A, Ball SL, deWaard JR. Biological identifications through DNA barcodes. Proceedings of the Royal Society of London series B. 2003; 270: 313–321.
51    Hebert PDN, Stoeckle MY, Zemlak TS, Francis CM. Identification of birds throug DNA barcodes. PLOS Biology. 2004; 2: e312.
52    Barrett RDH, Hebert PDN. Identifying spiders through DNA barcodes. Canadian Journal of Zoology. 2005; 83: 481-491.
53    Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research. 2002; 30: 3059-3066.
54    Librado P, Rozas J. DnaSp v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009; 25: 1451–1452.
55    Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution. 2011; 28: 2731–2739.
56    Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution. 1980; 15: 111–120.
57    Nijman V, Aliabadian M. Performance of distance-based DNA barcoding in the molecular identification of Primates. Comptes Rendus Biologies. 2010; 333: 11–16.
58    Hebert PDN, Ratnasingham S, deWaard JR. Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London. Series B. 2003; 270: S96–S99.
59    Willa KW, Rubinoff D. Myth of the molecule: DNA barcodes for species cannot replace morphology for identification and classification. Cladistics. 2004; 20: 47–55.
60    Aliabadian M, Beentjes KK, Roselaar CS, van Brandwijk H, Nijman V, Vonk R. DNA barcoding of Dutch birds. Zookeys. 2013; 365: 25–48.
61    Mabragaña E, Díaz de Astarloa JM, Hanner R, Zhang J, González Castro M. DNA Barcoding Identifies Argentine Fishes from Marine and Brackish Waters. PLoS One. 2011; 6(12); e28655.
62    Agrizzi J, Loss AC, Farro APC, Duda R, Costa LP, Leite YLR. Molecular Diagnosis of Atlantic Forest Mammals Using Mitochondrial DNA Sequences: Didelphid Marsupials. The Open Zoology Journal. 2012; 5: 2-9.
63    Borisenko AV, Lim BK, Ivanova NV, Hanner RH, Hebert PDN. DNA barcoding in surveys of small mammal communities: a field study in Suriname. Molecular Ecology Resources. 2008; 8: 471-9.
64    Clare EL, Lim BK, Engstrom MD, Eger JL, Hebert PDN. DNA barcoding of Neotropical bats: species identification and discovery within Guyana. Molecular Ecology Notes. 2007; 7: 184-90.
65    Liu J, Jiang J, Song S, Tornabene L, Chabarria R, Naylor GJP, Li C. Multilocus DNA barcoding – Species Identification with Multilocus Data. Scientific Reports. 2017; 7: 16601.
66    Zardoya R, Meyer A. Phylogenetic performance of mitochondrial protein-codinggenes in resolving relationships among vertebrates. Molecular Biology and Evolution. 1996; 13(7): 933-942.
67    Dasmahapatra K, Elias M, Hill R, Hoffman J, Mallet J. Mitochondrial DNA barcoding detects some species that are real, and some that are not. Molecular Ecology Resources. 2010; 10: 264–273.
68    Steppan SJ, Storz BL, Hoffmann RS. Nuclear DNA phylogeny of the squirrels (Mammalia: Rodentia) and the evolution of arboreality from c-myc and RAGI. Molecular Phylogenetics and Evolution. 2004; 30: 703–719.
69    Clare EL, Lim BK, Engstrom MD, Eger JL, Hebert PDN. DNA Barcoding of neotropical bats: Species identification and discovery within Guyana. Molecular Ecology. 2006; 7: 184–190.
70    Nicolas V, Schaeffer B, Missoup AD, Kennis J, Colyn M, et al. Assessment of Three Mitochondrial Genes (16S, Cytb, CO1) for Identifying Species in the Praomyini Tribe (Rodentia: Muridae). PLoS ONE. 2012; 7(5): e36586.
71    Zinner D, Groeneveld LF, Keller C, Roos C. Mitochondrial phylogeography of baboons (Papio spp.) - Indication for introgressive hybridization? BMC Evolutionary Biology. 2009; 9: 83.
72    Tsytsulina K, Dick MH, Maeda K, Masuda R. Systematics and phylogeography of the steppe whiskered bat Myotis aurascens Kuzyakin, 1935 (Chiroptera, Vespertilionidae). Russian Journal of Theriology. 2012; 11: 1–20.
73    Jiang, T, Sun K, Chou C, Zhang Z, Feng J. First record of Myotis flavus (Chiroptera: Vespertilionidae) from mainland China and a reassessment of its taxonomic status. Zootaxa. 2010; 2414: 41–51.
74    Esselstyn JA, Timm RM, Brown R M. Do geological or climatic processes drive speciation in dynamic archipelagos? The tempo and mode of diversification in Southeast Asian shrews. Evolution. 2009; 63: 2595–2610.
75    Soule´ M. Allozyme variation: its determinants in space and time. In: Ayala FJ (eds.) Molecular evolution. Sunderland, Massachusetts: Sinauer and Associates Inc., Publishers; 1976. pp. 60–77.
76    Scotland RW, Olmstead RG, Bennett JR. Phylogeny reconstruction: The role of morphology. Systematic Biology. 2003; 52(4): 539–548.
77    Rubinoff D. Utility of mitochondrial DNA barcodes in species conservation. Conservation Biology. 2006; 20 (4): 1026–1033.
78    Naylor G, Brown WM. Structural biology and phylogenetic estimation. Nature. 1997; 388: 527–528.
79    Moritz C, Cicero C. DNA barcoding: Promise and pitfalls. PLOS Biology. 2004; 2(10): e354.
80    Fujisawa T, Barraclough T. Delimiting Species Using Single-Locus Data and the Generalized Mixed Yule Coalescent Approach: A Revised Method and Evaluation on Simulated Data Sets. Systematic Biology. 2013; 62(5):707–724.
81    Awadalla P, Eyre-Walker A, Smith JM. Linkage disequilibrium and recombination in hominid mitochondrial DNA. Science. 1999; 286: 2524-2525.
82    Rokas A, Ladoukakis E, Zouros E. Animal mitochondrial DNA recombination revisited. Trends in Ecology and Evolution. 2003; 18: 411-417.
83    Hebert PDN, Gregory TR. The promise of DNA barcoding for taxonomy. Systematic Biology. 2005; 54: 852-859.
84    Ondrejicka DA, Locke SA, Morey K, Borisenko AV, Hanner RH. Status and prospects of DNA barcoding in medically important parasites and vectors. Trends in Parasitology. 2014; 30(12): 582-591.
85    Alcaide M, Rico C, Ruiz S, Soriguer R, Muñoz J, Figuerola J. Disentangling Vector-Borne Transmission Networks: A Universal DNA Barcoding Method to Identify Vertebrate Hosts from Arthropod Bloodmeals. PLoS One. 2009; 4(9): e7092.
86    Léger E, Liu X, Masseglia S, Noël V, Vourc’h G, Bonnet S, McCoy KD. Reliability of molecular host-identification methods for ticks: an experimental in vitro study with Ixodes ricinus. Parasites Vectors. 2015; 8:433.
87    Huggins LG, Koehler AV, Ng-Nguyen D, Wilcox S, Schunack B, Inpankaew T, Traub RJ. Assessment of a metabarcoding approach for the characterisation of vector-borne bacteria in canines from Bangkok, Thailand. Parasites Vectors. 2019; 12: 394.