Marine Biology

, 167:1 | Cite as

Insights into reproductive isolation within the pelagic copepod Pleuromamma abdominalis with high genetic diversity using genome-wide SNP data

  • Junya HiraiEmail author
Short Note


Species complexes with multiple genetic clades are frequently observed using mitochondrial DNA (mtDNA) markers in pelagic copepods. However, reproductive isolation among clades is not fully understood because of low sequence variations in common nuclear markers. In the present study, genome-wide single nucleotide polymorphisms (SNPs) were obtained for copepod, Pleuromamma abdominalis, with high genetic diversity and sympatric mtDNA clades using multiplexed inter-simple sequence repeat genotyping by sequencing (MIG-seq). Sequences of mitochondrial cytochrome oxidase subunit I (mtCOI) were classified into six clades in 31 P. abdominalis that co-existed in the western subtropical North Pacific. Four mtCOI clades with genetic distances ≥ 0.082 were monophyletic according to the phylogenetic analyses based on SNPs in MIG-seq. The other two mtCOI clades with mean 0.082 genetic distance were not separated in the MIG-seq phylogenetic tree. The results from our phylogenetic analysis of MIG-seq agreed with those from other genome-wide methods of double digest restriction site-associated DNA sequencing, and reproductive isolation and interbreeding between mtCOI clades were also supported by Bayesian clustering analysis. The two mtCOI clades that had possibly interbred exhibited different distribution patterns, suggesting secondary contact without reproductive isolation in the sampling area. The genome-wide SNP data supported the high cryptic species diversity in P. abdominalis, which was inferred from mitochondrial genes. Further genome-wide studies, especially those that use PCR-based approaches including MIG-seq for small copepods, can lead to appropriate measurements of pelagic species diversity in the ocean.



I thank the captain, crew, and all scientists during KH-16-7 cruise on RV Hakuho-maru for assistance of the field sampling. I also thank Dr. Minoru Ijichi for providing the opportunity for ddRAD-seq.


This study was funded by JSPS KAKENHI (Grant number 18K14519).

Compliance with ethical standards

Conflict of interest

The author declares that there are no conflict of interest.


  1. Andrews KR, Norton EL, Fernandez-Silva I, Portner E, Goetze E (2014) Multilocus evidence for globally distributed cryptic species and distinct populations across ocean gyres in a mesopelagic copepod. Mol Ecol 23:5462–5479CrossRefGoogle Scholar
  2. Andrews KR, Good JM, Miller MR, Luikart G, Hohenlohe PA (2016) Harnessing the power of RADseq for ecological and evolutionary genomics. Nat Rev Genet 17:81–92CrossRefGoogle Scholar
  3. Avise JC (1986) Mitochondrial DNA and the evolutionary genetics of higher animals. Philos Trans R Soc Lond B Biol Sci 312:325–3423CrossRefGoogle Scholar
  4. Beaugrand G, Brander KM, Lindley JA, Souissi S, Reid PC (2003) Plankton effect on cod recruitment in the North Sea. Nature 426:661–664CrossRefGoogle Scholar
  5. Blanco-Bercial L, Bucklin A (2016) New view of population genetics of zooplankton: RAD-seq analysis reveals population structure of the North Atlantic planktonic copepod Centropages typicus. Mol Ecol 25:1566–1580CrossRefGoogle Scholar
  6. Blanco-Bercial L, Cornils A, Copley N, Bucklin A (2014) DNA barcoding of marine copepods: assessment of analytical approaches to species identification. PLoS Curr 6Google Scholar
  7. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120CrossRefGoogle Scholar
  8. Bucklin A, Frost BW, Bradford-Grieve J, Allen LD, Copley NJ (2003) Molecular systematic and phylogenetic assessment of 34 calanoid copepod species of the Calanidae and Clausocalanidae. Mar Biol 142:333–343CrossRefGoogle Scholar
  9. Bucklin A, Nishida S, Schnack-Schiel S, Wiebe PH, Lindsay D, Machida RJ, Nancy JC (2010a) A census of zooplankton of the global ocean. In: McIntyre AD (ed) Life in the world’s oceans: diversity, distribution and abundance. Blackwell Publishing Ltd, Oxford, pp 247–265CrossRefGoogle Scholar
  10. Bucklin A, Ortman BD, Jennings RM, Nigro LM, Sweetman CJ, Copley NJ, Sutton T, Wiebe PH (2010b) A “Rosetta Stone” for metazoan zooplankton: DNA barcode analysis of species diversity of the Sargasso Sea (Northwest Atlantic Ocean). Deep-Sea Res Part II 57:2234–2247CrossRefGoogle Scholar
  11. Bucklin A, Steinke D, Blanco-Bercial L (2011) DNA barcoding of marine metazoa. Ann Rev Mar Sci 3:471–508CrossRefGoogle Scholar
  12. Catchen J, Hohenlohe PA, Bassham S, Amores A, Cresko WA (2013) Stacks: an analysis tool set for population genomics. Mol Ecol 22:3124–3140CrossRefGoogle Scholar
  13. Chihara M, Murano M (1997) An illustrated guide to marine plankton in Japan. Tokai University Press, TokyoGoogle Scholar
  14. Cornils A, Held C (2014) Evidence of cryptic and pseudocryptic speciation in the Paracalanus parvus species complex (Crustacea, Copepoda, Calanoida). Front Zool 11:19CrossRefGoogle Scholar
  15. Cornils A, Wend-Heckmann B, Held C (2017) Global phylogeography of Oithona similis s.l. (Crustacea, Copepoda, Oithonidae)—a cosmopolitan plankton species or a complex of cryptic lineages? Mol Phylogenet Evol 107:473–485CrossRefGoogle Scholar
  16. Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML (2011) Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat Rev Genet 12:499–510CrossRefGoogle Scholar
  17. De Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56:879–886CrossRefGoogle Scholar
  18. Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361CrossRefGoogle Scholar
  19. Goetze E (2003) Cryptic speciation on the high seas; global phylogenetics of the copepod family Eucalanidae. Proc Biol Sci 270:2321–2331CrossRefGoogle Scholar
  20. Hirai J, Shimode S, Tsuda A (2013) Evaluation of ITS2-28S as a molecular marker for identification of calanoid copepods in the subtropical western North Pacific. J Plankton Res 35:644–656CrossRefGoogle Scholar
  21. Hirai J, Tsuda A, Goetze E (2015) Extensive genetic diversity and endemism across the global range of the oceanic copepod Pleuromamma abdominalis. Prog Oceanogr 138A:77–90CrossRefGoogle Scholar
  22. Hohenlohe PA, Bassham S, Etter PD, Stiffler N, Johnson EA, Cresko WA (2010) Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet 6:e1000862CrossRefGoogle Scholar
  23. Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806CrossRefGoogle Scholar
  24. Kuriyama M, Nishida S (2006) Species diversity and niche-partitioning in the pelagic copepods of the family Scolecitrichidae (Calanoida). Crustaceana 79:293–317CrossRefGoogle Scholar
  25. Machida RJ, Tsuda A (2010) Dissimilarity of species and forms of planktonic Neocalanus copepods using mitochondrial COI, 12S, nuclear ITS, and 28S gene sequences. PLoS One 5:e10278CrossRefGoogle Scholar
  26. Palumbi SR (1994) Genetic-divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572CrossRefGoogle Scholar
  27. Paris JR, Stevens JR, Catchen JM (2017) Lost in parameter space: a road map for stacks. Methods Ecol Evol 188:799–814Google Scholar
  28. Park JS, Takayama K, Suyama Y, Choi BH (2019) Distinct phylogeographic structure of the halophyte Suaeda Malacosperma (Chenopodiaceae/Amaranthaceae), endemic to Korea-Japan region, influenced by historical range shift dynamics. Plant Syst Evol 305:193–203CrossRefGoogle Scholar
  29. Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE (2012) Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One 7:e37135CrossRefGoogle Scholar
  30. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  31. Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138CrossRefGoogle Scholar
  32. Sano M, Maki K, Nishibe Y, Nagata T, Nishida S (2013) Feeding habits of mesopelagic copepods in Sagami Bay: insights from integrative analysis. Prog Oceanogr 110:11–26CrossRefGoogle Scholar
  33. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313CrossRefGoogle Scholar
  34. Suyama Y, Matsuki Y (2015) MIG-seq: an effective PCR-based method for genome-wide single-nucleotide polymorphism genotyping using the next-generation sequencing platform. Sci Rep 5:16963CrossRefGoogle Scholar
  35. Tamaki I, Yoichi W, Matsuki Y, Suyama Y, Mizuno M (2017) Inconsistency between morphological traits and ancestry of individuals in the hybrid zone between two Rhododendron japonoheptamerum varieties revealed by a genotyping-by-sequencing approach. Tree Genet Genomes 13:4CrossRefGoogle Scholar
  36. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefGoogle Scholar
  37. Turner JT (2004) The importance of small planktonic copepods and their roles in pelagic marine food webs. Zool Stud 43:255–266Google Scholar
  38. Wagner CE, Keller I, Wittwer S, Selz OM, Mwaiko S, Greuter L, Seehausen O (2013) Genome-wide RAD sequence data provide unprecedented resolution of species boundaries and relationships in the Lake Victoria cichlid adaptive radiation. Mol Ecol 22:787–798CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Atmosphere and Ocean Research InstituteThe University of TokyoKashiwa-ShiJapan

Personalised recommendations