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The Korean Society of Phycology (한국조류학회(藻類))
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Splitting blades: why genera need to be more carefully defined; the case for Pyropia (Bangiales, Rhodophyta)

  • Zuccarello, Giuseppe C. (School of Biological Sciences, Victoria University of Wellington) ;
  • Wen, Xinging (Department of Biological Sciences, Kongju National University) ;
  • Kim, Gwang Hoon (Department of Biological Sciences, Kongju National University)
  • Received : 2022.06.27
  • Accepted : 2022.09.11
  • Published : 2022.09.15
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Abstract

The trend in naming genera based almost exclusively on molecular data, and not on morphological diagnostic characters, is increasing. In bifurcating phylogenetic trees generic cut-offs are arbitrary, but at the bare minimum nomenclatural changes should be supported by multiple phylogenetic methodologies using appropriate models for all the various gene partitions, strong support with all branch support methods, and should also result in adding to our knowledge of the interrelationships of taxa. We believe that a recent taxonomic treatment of the genus Pyropia (Yang et al. 2020) into several genera is unwarranted. We reanalysed the data presented in the recent article, using additional phylogenetic methods. Our results show that many of the newly established genera are not well supported by all methods, and the new circumscription of the genus Pyropia renders it unsupported. We also tested additional outgroups, which were previously suggested as sister to Pyropia, but this did not substantially change our conclusions. These generic nomenclatural changes of the previously strongly supported genus Pyropia, do not shed light on the evolution of this group and have serious consequences in these commercially important algae, that are also governed by a plethora of regulation and by-laws that now need to be amended. We suggest that the over-splitting of groups based only on poorly produced and modestly supported phylogenies should not be accepted and that the genus Pyropia sensu Sutherland et al. (2011) be restored.

Keywords

Acknowledgement

This research was supported by Development of Technology for Biomaterialization of Marine Fisheries byproducts of Korea Institute of Marine Science & Technology Promotion (KIMST) funded by the Ministry of Oceans and Fisheries (KIMST-20220128), and by the National Marine Biodiversity Institute of Korea (2022M01100) and by the National Research Foundation of Korea (NRF) grant (2019M3C1B7025093). We thank Mike Wynne and all anonymous reviewers for comments on this manuscript.

References

  1. Agardh, J. G. 1899. Analecta algologica, Continuatio V. Lunds Universitets Ars-Skrift, Andra Afdelningen, Kongl. Fysiogr. Sallsk. Lund Handl. 35:1-160.
  2. Badis, Y., Han, J. W., Klochkova, T. A., Gachon, C. M. M. & Kim, G. H. 2020. The gene repertoire of Pythium porphyrae (Oomycota) suggests an adapted plant pathogen tackling red algae. Algae 35:133-144. https://doi.org/10.4490/algae.2020.35.6.4
  3. Chernomor, A., von Haeseler, A. & Minh, B. Q. 2016. Terrace aware data structure for phylogenomic inference from supermatrices. System. Biol. 65:997-1008. https://doi.org/10.1093/sysbio/syw037
  4. Clayton, W. D. 1983. The genus concept in practice. Kew Bull. 38:149-153. https://doi.org/10.2307/4108098
  5. Dai, Y.-L., Kim, G. H., Kang, M.-C. & Jeon, Y.-J. 2020. Protective effects of extracts from six local strains of Pyropia yezoensis against oxidative damage in vitro and in zebrafish model. Algae 35:189-200. https://doi.org/10.4490/algae.2020.35.5.14
  6. De Queiroz, K. 1998. The general lineage concept of species: species criteria and the process of speciation. In Howard, D. J. & Berlocher, S. H. (Eds.) Endless Forms: Species and Speciation. Oxford University Press, Oxford, pp. 57-75.
  7. Diaz-Tapia, P., Maggs, C. A., West, J. A. & Verbruggen, H. 2017. Analysis of chloroplast genomes and a supermatrix inform reclassification of the Rhodomelaceae (Rhodophyta). J. Phycol. 53:920-937. https://doi.org/10.1111/jpy.12553
  8. Diaz-Tapia, P., Munoz-Luque, L., Pineiro-Corbeira, C. & Maggs, C. A. 2021. Phylogenetic analyses of Macaronesian turf-forming species reveal cryptic diversity and resolve Stichothamnion in the Vertebrata clade (Rhodomelaceae, Rhodophyta). Eur. J. Phycol. 56:444-454. https://doi.org/10.1080/09670262.2021.1871969
  9. Douady, C. J., Delsuc, F., Boucher, Y., Doolittle, W. F. & Douzery, E. J. P. 2003. Comparison of Bayesian and maximum likelihood bootstrap measures of phylogenetic reliability. Mol. Biol. Evol. 20:248-254. https://doi.org/10.1093/molbev/msg042
  10. Entwisle, T. J. & Weston, P. H. 2005. Majority rules, when systematists disagree. Aust. Syst. Bot. 18:1-6. https://doi.org/10.1071/SB04013
  11. Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783-791. https://doi.org/10.2307/2408678
  12. Fiser, C., Robinson, C. T. & Malard, F. 2018. Cryptic species as a window into the paradigm shift of the species concept. Mol. Ecol. 27:613-635. https://doi.org/10.1111/mec.14486
  13. Garnock-Jones, P., Albach, D. & Briggs, B. G. 2007. Botanical names in southern hemisphere Veronica (Plantaginaceae): sect. Detzneria, sect. Hebe, and sect. Labiatoides. Taxon 56:571-582. https://doi.org/10.1002/tax.562028
  14. Guindon, S., Dufayard, J.-F., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. 2010. New algorithms and methods to estimate maximum-likelyhood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59:307-321. https://doi.org/10.1093/sysbio/syq010
  15. Gurgel, C. F. D., Norris, J. N., Schmidt, W. E., Le, H. N. & Fredericq, S. 2018. Systematics of the Gracilariales (Rhodophyta) including new subfamilies, tribes, subgenera, and two new genera, Agarophyton gen. nov. and Crassa gen. nov. Phytotaxa 374:1-23. https://doi.org/10.11646/phytotaxa.374.1.1
  16. Hey, J., Waples, R. S., Arnold, M. L., Butlin, R. K. & Harrison, R. G. 2003. Understanding and confronting species uncertainty in biology and conservation. Trends Ecol. Evol. 18:597-603. https://doi.org/10.1016/j.tree.2003.08.014
  17. Hoang, D. T., Vinh, L. S., Flouri, T., Stamatakis, A., von Haeseler, A. & Minh, B. Q. 2018. MPBoot: fast phylogenetic maximum parsimony tree inference and bootstrap approximation. BMC Evol. Biol. https://doi.org/10.1186/s12862-018-1131-3.
  18. Humphreys, A. M. & Linder, H. P. 2009. Concept versus data in delimitation of plant genera. Taxon 58:1054-1074. https://doi.org/10.1002/tax.584002
  19. Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., Von Haeseler, A. & Jermiin, L. S. 2017. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat. Methods 14:587-589. https://doi.org/10.1038/nmeth.4285
  20. Kim, G. H., Moon, K.-H., Kim, J.-Y., Shim, J. & Klochkova, T. A. 2014. A revaluation of algal diseases in Korean Pyropia (Porphyra) sea farms and their economic impact. Algae 29:249-265. https://doi.org/10.4490/algae.2014.29.4.249
  21. Kylin, H. 1956. Die Gattungen der Rhodophyceen. C.W.K. Gleerups Press, Lund, 673 pp.
  22. Lee, J.-H., Ahn, G., Ko, J.-Y., Kang, N., Jung, K., Han, E.-J., Kim, G.-H., Kim, H. J., Choi, C. S. & Jeon, Y.-J. 2021. Liposoluble portion of the red alga Pyropia yezoensis protects alcohol induced liver injury in mice. Algae 36:219-229. https://doi.org/10.4490/algae.2021.36.4.28
  23. Leliaert, F., Verbruggen, H., Vanormelingen, P., Steen, F., Lopez-Bautista, J. M., Zuccarello, G. C. & De Clerck, O. 2014. DNA-based species delimitation in algae. Eur. J. Phycol. 49:179-196. https://doi.org/10.1080/09670262.2014.904524
  24. Lyra, G. D. M., Iha, C., Grassa, C. J., Cai, L., Zhang, H., Lane, C., Blouin, N., Oliveira, M. C., de Castro Nunes, J. M. & Davis, C. C. 2021. Phylogenomics, divergence time estimation and trait evolution provide a new look into the Gracilariales (Rhodophyta). Mol. Phylogenet. Evol. 165:107294. https://doi.org/10.1016/j.ympev.2021.107294
  25. Minh, B. Q., Schmidt, H. A., Chernomor, O., Schrempf, D., Woodhams, M. D., Von Haeseler, A. & Lanfear, R. 2020. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37:1530-1534. https://doi.org/10.1093/molbev/msaa015
  26. Muangmai, N., Preuss, M., West, J. A. & Zuccarello, G. C. 2022. Cryptic diversity and phylogeographic patterns of the Bostrychia intricata species complex (Rhodomelaceae, Rhodophyta) along the coast of southeastern Australia. Phycologia 61:27-36. https://doi.org/10.1080/00318884.2021.1994768
  27. Munoz-Gomez, S. A., Mejia-Franco, F. G., Durnin, K., Colp, M., Grisdale, C. J., Archibald, J. M. & Slamovits, C. H. 2017. The new red algal subphylum Proteorhodophytina comprises the largest and most divergent plastid genomes known. Curr. Biol. 27:1677-1684. https://doi.org/10.1016/j.cub.2017.04.054
  28. Rambaut, A. 2009. FigTree v1.4.4. Available from: http://tree.bio.ed.ac.uk/software/figtree/. Accessed May 10, 2022.
  29. Ronquist, F. & Huelsenbeck, J. P. 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574. https://doi.org/10.1093/bioinformatics/btg180
  30. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Hohna, S., Larget, B., Liu, L., Suchard, M. A. & Huelsenbeck, J. P. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61:539-542. https://doi.org/10.1093/sysbio/sys029
  31. Santianez, W. J. E. & Wynne, M. J. 2020. Proposal of Phycocalidia Santianez & M.J. Wynne nom. nov. to replace Calidia L.-E. Yang & J. Brodie nom. illeg. (Bangiales, Rhodophyta). Not. Algarum 140:1-3.
  32. Santorum, J. M., Darriba, D., Taboada, G. L. & Posada, D. 2014. Jmodeltest.org: selection of nucleotide substitution models on the cloud. Bioinformatics 30:1310-1311. https://doi.org/10.1093/bioinformatics/btu032
  33. Saunders, G. W., Huisman, J. M., Verges, A., Kraft, G. T. & Le Gall, L. 2017. Phylogenetic analyses support recognition of ten new genera, ten new species and 16 new combinations in the family Kallymeniaceae (Gigartinales, Rhodophyta). Cryptogam. Algol. 38:79-132. https://doi.org/10.7872/crya/v38.iss2.2017.79
  34. Schneider, C. W., Quach, P. K. & Lane, C. E. 2017. A case for true morphological crypsis: Pacific Dasya anastomosans and Atlantic D. cryptica sp. nov. (Dasyaceae, Rhodophyta). Phycologia 56:359-368. https://doi.org/10.2216/16-79.1
  35. Schneider, C. W. & Wynne, M. J. 2007. A synoptic review of the classification of red algal genera a half century after Kylin's "Die Gattungen der Rhodophyceen". Bot. Mar. 50:197-249. https://doi.org/10.1515/BOT.2007.025
  36. Schneider, C. W. & Wynne, M. J. 2013. Second addendum to the synoptic review of red algal genera. Bot. Mar. 56:111-118. https://doi.org/10.1515/bot-2012-0235
  37. Schneider, C. W. & Wynne, M. J. 2019. Fourth addendum to the synoptic review of red algal genera. Bot. Mar. 62:355-367. https://doi.org/10.1515/bot-2019-0003
  38. Simmons, M. P., Pickett, K. M. & Miya, M. 2004. How meaningful are Bayesian support values? Mol. Biol. Evol. 21:188-199. https://doi.org/10.1093/molbev/msh014
  39. Simon, C. 2022. An evolving view of phylogenetic support. Syst. Biol. 71:921-928. https://doi.org/10.1093/sysbio/syaa068
  40. Stamatakis, A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312-1313. https://doi.org/10.1093/bioinformatics/btu033
  41. Stevens, P. F. 1985. The genus concept in practice: but for what practice? Kew Bull. 40:457-465. https://doi.org/10.2307/4109605
  42. Sutherland, J. E., Lindstrom, S. C., Nelson, W. A., Brodie, J., Lynch, M. D. J., Hwang, M. S., Choi, H.-G., Miyata, M., Kikuchi, N., Oliveira, M. C., Farr, T., Neefus, C., MolsMortensen, A., Milstein, D. & Muller, K. M. 2011. A new look at an ancient order: generic revision of the Bangiales (Rhodophyta). J. Phycol. 47:1131-1151. https://doi.org/10.1111/j.1529-8817.2011.01052.x
  43. Suzuki, Y., Glazko, G. V. & Nei, M. 2002. Overcredibility of molecular phylogenies obtained by Bayesian phylogenetics. Proc. Natl. Acad. Sci. U. S. A. 99:16138-16143. https://doi.org/10.1073/pnas.212646199
  44. Verbruggen, H. 2014. Morphological complexity, plasticity, and species diagnosability in the application of old species names in DNA-based taxonomies. J. Phycol. 50:26-31. https://doi.org/10.1111/jpy.12155
  45. Wynne, M. J. & Schneider, C. W. 2010. Addendum to the synoptic review of red algal genera. Bot. Mar. 53:291-299. https://doi.org/10.1515/BOT.2010.039
  46. Wynne, M. J. & Schneider, C. W. 2016. Third addendum to the synoptic review of red algal genera. Bot. Mar. 59:397-404.
  47. Wynne, M. J. & Schneider, C. W. 2022. Fifth addendum to the synoptic review of red algal genera. Bot. Mar. 65:141-151. https://doi.org/10.1515/bot-2021-0093
  48. Yang, L. -E., Deng, Y. -Y., Xu, G. -P., Russell, S., Lu, Q. -Q. & Brodie, J. 2020. Redefining Pyropia (Bangiales, Rhodophyta): four new genera, resurrection of Porphyrella and description of Calidia pseudolobata sp. nov. from China. J. Phycol. 56:862-879. https://doi.org/10.1111/jpy.12992
  49. Zuccarello, G. C., West, J. A. & Kamiya, M. 2018. Non-monophyly of Bostrychia simpliciuscula (Ceramiales, Rhodophyta): multiple species with very similar morphologies, a revised taxonomy of cryptic species. Phycol. Res. 66:100-107. https://doi.org/10.1111/pre.12207