Abstract
The genus Sheathia consists of over 20 species primarily distributed in Asia, Europe, Oceania, North America, and Africa. However, the origin and evolution of this genus remain unclear. Two gametophyte stage specimens (SAS18052 and SAS18523) and two “Chantransia” stage specimens (YTS19161 and YTS19017) were collected from Shanxi and Henan Provinces in China, respectively. Based on morphological data, isolates YTS19161 and YTS19017 were similar to Audouinella pygmaea, whereas the morphological characteristics of SAS18052 and SAS18523 were in good agreement with the circumscription description of S. longipedicellata. Molecular sequences of rbcL, COI-5P, and psbA were used to investigate the phylogenetic, evolutionary, and biogeographic origin of the genus Sheathia. The three molecular markers supported that the two gametophyte stage specimens belong to S. longipedicellata, while the isolates YTS19161 and YTS19017 were the “Chantransia” of S. longipedicellata. Ancestral area reconstruction and divergence time estimation speculated that Sheathia originated in North America, a portion of the Pangaea at approximately 328.07–184.73 million years ago (Ma). Our relaxed molecular clock analysis suggests that the Florideophyceae diverged approximately 741.04 (894.36–631.70) Ma. The major divergences in this class involved the emergence of Nemaliophycidae [ca. 662.01 (779.83–580.51) Ma], and the split of orders Batrachospermales and Thoreales [ca. 456.10 (552.80–367.88) Ma].
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Data Availability Statement
The data that support the findings of this study are available on request from the corresponding author.
References
Aguirre J, Perfectti F, Braga J C. 2010. Integrating phylogeny, molecular clocks, and the fossil record in the evolution of coralline algae (Corallinales and Sporolithales, Rhodophyta). Paleobiology, 36(4): 519–533, https://doi.org/10.1666/09041.1.
Aguirre J, Riding R, Braga J C. 2000. Diversity of coralline red algae: origination and extinction patterns from the early Cretaceous to the Pleistocene. Paleobiology, 26(4): 651–667, https://doi.org/10.1666/0094-8373(2000)026<0651:docrao>2.0.co;2.
Bengtson S, Sallstedt T, Belivanova V, Whitehouse M. 2017. Three-dimensional preservation of cellular and subcellular structures suggests 1.6 billion-year-old crown-group red algae. PLoS Biology, 15(3): e2000735, https://doi.org/10.1371/journal.pbio.2000735.
Berney C, Pawlowski J. 2006. A molecular time-scale for eukaryote evolution recalibrated with the continuous microfossil record. Proceedings of the Royal Society B. Biological Sciences, 273(1596): 1867–1872, https://doi.org/10.1098/rspb.2006.3537.
Betts H C, Puttick M N, Clark J W, Williams T A, Donoghue P C J, Pisani D. 2018. Integrated genomic and fossil evidence illuminates life’s early evolution and eukaryote origin. Nature ecology & evolution, 2(10): 1556–1562, https://doi.org/10.1038/s41559-018-0644-x.
Butterfield N J, Knoll A H, Swett K. 1990. A bangiophyte red alga from the Proterozoic of arctic Canada. Science, 250(4977): 104–107, https://doi.org/10.1126/science.11538072.
Butterfield N J. 2000. Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes. Paleobiology, 26(3): 386–404, https://doi.org/10.1666/0094-8373(2000)026<0386:bpngns>2.0.co;2.
Condie K C. 1982. Plate Tectonics & Crustal Evolution. Pergamon Press, New York. 492p.
Condon D, Zhu M Y, Bowring S, Wang W, Yang A H, Jin Y G. 2005. U-Pb ages from the neoproterozoic doushantuo formation, China. Science, 308(5718): 95–98, https://doi.org/10.1126/science.1107765.
Drummond A J, Ho S Y W, Phillips M J, Rambaut A. 2006. Relaxed phylogenetics and dating with confidence. PLoS Biology, 4(5): e88, https://doi.org/10.1371/journal.pbio.0040088.
Drummond A J, Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7(1): 214, https://doi.org/10.1186/1471-2148-7-214.
Entwisle T J, Vis M L, Chiasson W B, Necchi O Jr, Sherwood A R. 2009. Systematics of the Batrachospermales (Rhodophyta)—a synthesis. Journal of Phycology, 45(3): 704–715, https://doi.org/10.1111/j.1529-8817.2009.00686.x.
Felsenstein J. 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. Journal of Molecular Evolution, 17(6): 368–376, https://doi.org/10.1007/bf01734359.
Feng J, Chen L, Wang Y N, Xie S L. 2015. Molecular systematics and biogeography of Thorea (Thoreales, Rhodophyta) from Shanxi, China. Systematic Botany, 40(2): 376–385, https://doi.org/10.1600/036364415x688763.
Gibson T M, Shih P M, Cumming V M, Fischer W W, Crockford P W, Hodgskiss M S W, Wörndle S, Creaser R A, Rainbird R H, Skulski T M, Halverson G P. 2018. Precise age of Bangiomorpha pubescens dates the origin of eukaryotic photosynthesis. Geology, 46(2): 135–138, https://doi.org/10.1130/g39829.1.
Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52(5): 696–704, https://doi.org/10.1080/10635150390235520.
Han J F, Nan F R, Feng J, Lv J P, Liu Q, Kociolek J P, Xie S L. 2018. Sheathia jinchengensis (Batrachospermales, Rhodophyta), a new freshwater red algal species described from North China. Phytotaxa, 367(1): 63–70, https://doi.org/10.11646/phytotaxa.367.1.7.
Han J F, Nan F R, Feng J, Lv J P, Liu Q, Liu X D, Xie S L. 2020. Affinities of four freshwater putative “Chantransia” stages (Rhodophyta) in Southern China from molecular and morphological data. Phytotaxa, 441(1): 47–59, https://doi.org/10.11646/phytotaxa.441.1.4.
Han X J. 2012. Phylogenetic Relationship of Audouinella based on Gene Sequences. Shanxi University, Taiyuan. 65p. (in Chinese with English abstract)
Hua D, Shi Z X. 1996. A new species of Batrachospermum from Jiangsu, China. Acta Phytotaxonomica Sinica, 34(3): 324–326. (in Chinese with English abstract)
Ji L, Xie S L, Feng J, Chen L, Wang J. 2014. Molecular systematics of four endemic Batrachospermaceae (Rhodophyta) species in China with multilocus data. Journal of Systematics and Evolution, 52(1): 92–100, https://doi.org/10.1111/jse.12058.
Johnston E T, Dixon K R, West J A, Buhari N, Vis M L. 2018. Three gene phylogeny of the Thoreales (Rhodophyta) reveals high species diversity. Journal of Phycology, 54(2): 159–170, https://doi.org/10.1111/jpy.12618.
Knoll A H, Wörndle S, Kah L C. 2013. Covariance of microfossil assemblages and microbialite textures across an upper Mesoproterozoic carbonate platform. Palaios, 28(7): 453–470, https://doi.org/10.2110/palo.2013.p13-005r.
Kumano S. 2002. Freshwater Red Algae of the World. Biopress Ltd, Bristol. 375p.
Magallón S, Hilu K W, Quandt D. 2013. Land plant evolutionary timeline: gene effects are secondary to fossil constraints in relaxed clock estimation of age and substitution rates. American Journal of Botany, 100(3): 556–573, https://doi.org/10.3732/ajb.1200416.
Nan F R, Feng J, Lv J P, Liu Q, Xie S L. 2016. Evolutionary history of the monospecific Compsopogon genus (Compsopogonales, Rhodophyta). Algae, 31(4): 303–315, https://doi.org/10.4490/algae.2016.31.10.22.
Nan F R. 2017. Investigation on the Phylogenetics and Evolution History of Different Lineages in Freshwater Rhodophyta Based on Phylogenomic Analysis. Shanxi University, Taiyuan. 142p. (in Chinese with English abstract)
Necchi O Jr, Agostinho D C, Vis M L. 2018. Revision of Batrachospermum section Virescentia (Batrachospermales, Rhodophyta) with the establishment of the new genus, Virescentia stat. nov. Cryptogamie, Algologie, 39(3): 313–338, https://doi.org/10.7872/crya/v39.iss3.2018.313.
Necchi O Jr, Filho A G, Paiano M O. 2019a. Revision of Batrachospermum sections Acarposporophytum and Aristata (Batrachospermales, Rhodophyta) with the establishment of the new genera Acarposporophycos and Visia. Phytotaxa, 395(2): 51–65, https://doi.org/10.11646/phytotaxa.395.2.1.
Necchi O Jr, Garcia Fo A S, Paiano M O, Vis M L. 2019b. Revision of Batrachospermum section Macrospora (Batrachospermales, Rhodophyta) with the establishment of the new genus Montagnia. Phycologia, 58(6): 582–591, https://doi.org/10.1080/00318884.2019.1624143.
Necchi O Jr, West J A, Ganesan E K, Yasmin F, Rai S K, Rossignolo N L. 2019c. Diversity of the genus Sheathia (Batrachospermales, Rhodophyta) in northeast India and east Nepal. Algae, 34(4): 277–288, https://doi.org/10.4490/algae.2019.34.10.30.
Necchi O Jr, Zucchi M R. 1995. Systematics and distribution of freshwater Audouinella (Acrochaetiaceae, Rhodophyta) in Brazil. European Journal of Phycology, 30(3): 209–218, https://doi.org/10.1080/09670269500650991.
Nylander J A, Olsson, U, Alstrom P, Sanmartin I. 2008. Accounting for phylogenetic uncertainty in biogeography: a Bayesian approach to dispersal vicariance analysis of the thrushes (Aves: Turdus). Systematic Biology, 57(2): 257–268, https://doi.org/10.1080/10635150802044003.
Parfrey L W, Lahr D J G, Knoll A H, Katz L A. 2011. Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proceedings of the National Academy of Sciences of the United States of America, 108(33): 13624–13629, https://doi.org/10.1073/pnas.1110633108.
Posada D, Buckley T R. 2004. Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Systematic Biology, 53(5): 793–808, https://doi.org/10.1080/10635150490522304.
Rambaut A, Suchard M A, Xie D, Drummond A J. 2014. Tracer v1.6. Computer program and documentation distributed by the author. http://beast.community/tracer. Accessed on 2015-01-15.
Rambaut A. 2009. FigTree, version 1.3.1. Computer program distributed by the author. http://tree.bio.ed.ac.uk/software/figtree/. Accessed on 2011-01-04.
Ronquist F, Huelsenbeck J P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19(12): 1572–1574, https://doi.org/10.1093/bioinformatics/btg180.
Rossignolo N L, Necchi O Jr. 2016. Revision of section Setacea of the genus Batrachospermum (Batrachospermales, Rhodophyta) with emphasis on specimens from Brazil. Phycologia, 55(4): 337–346, https://doi.org/10.2216/15-144.1.
Salomaki E D, Kwandrans J, Eloranta P, Vis M L. 2014. Molecular and morphological evidence for Sheathia gen. nov. (Batrachospermales, Rhodophyta) and three new species. Journal of Phycology, 50(3): 526–542, https://doi.org/10.1111/jpy.12179.
Saunders G W. 1993. Gel purification of red algal genomic DNA: an inexpensive and rapid method for the isolation of polymerase chain reaction-friendly DNA. Journal of Phycology, 29(2): 251–254, https://doi.org/10.1111/j.0022-3646.1993.00251.x.
Saunders G W. 2005. Applying DNA barcoding to red macroalgae: a preliminary appraisal holds promise for future applications. Philosophical Transactions of the Royal Society B: Biological sciences, 360(1462): 1879–1888, https://doi.org/10.1098/rstb.2005.1719.
Scotese C R, Bambach R K, Barton C, van der Voo R, Ziegler A M. 1979. Paleozoic base maps. The Journal of Geology, 87(3): 217–277.
Sharpe S C, Eme L, Brown M W, Roger A J. 2015. Timing the origins of multicellular eukaryotes through phylogenomics and relaxed molecular clock analyses. In: Ruiz-Trillo I, Nedelcu AM eds. Evolutionary Transitions to Multicellular Life. Springer, Dordrecht. p.3–29.
Sheath R G. 1984. The biology of freshwater red algae. In: Round F E, Chapman D J eds. Progress in Phycological Research. BioPress Ltd, Bristol. p.89–157.
Shi Z X. 2006. Flora Algarum Sinicarum Aquae Dulcis. Tomus XIII, Rhodophyta and Phaeophyta. Science Press, Beijing, China. p.1–77. (in Chinese)
Sun C H, Liu X F, Liu X D, Guo X W, Guo D C, Xu J P, Liu X Y, Hua D. 2001. Studies on physiological and ecological speciality of Batrachospermum longipedicellatum. Resources Science, 23(3): 93–96. (in Chinese with English abstract)
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28(10): 2731–2739, https://doi.org/10.1093/molbev/msr121.
Thompson J D, Gibson T J, Plewniak F, Jeanmougin F, Higgins D G. 1997. The Clustal-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25(24): 4876–4882, https://doi.org/10.1093/nar/25.24.4876.
van den Hoek C, Mann D, Jahns H M, Jahns M. 1995. Algae: An Introduction to Phycology. Cambridge University Press, Cambridge. 614pp.
Vis M L, Lee J, Eloranta P, Chapuis I S, Lam D W, Necchi Jr O. 2020. Paludicola gen. nov. and revision of the species formerly in Batrachospermum section Turfosa (Batrachospermales, Rhodophyta). Journal of Phycology, 56(4): 844–861, https://doi.org/10.1111/jpy.13001.
Vis M L, Saunders G W, Sheath R G, Dunse K, Entwisle T J. 1998. Phylogeny of the Batrachospermales (Rhodophyta) inferred from rbcL and 18S ribosomal DNA gene sequences. Journal of Phycology, 34(2): 341–350, https://doi.org/10.1046/j.1529-8817.1998.340341.x.
Vis M L, Sheath R G. 1996. Distribution and systematics of Batrachospermum (Batrachospermales, Rhodophyta) in North America. 9. Section Batrachospermum: description of five new species. Phycologia, 35(2): 124–134, https://doi.org/10.2216/i0031-8884-35-2-124.1.
Vis M L, Sheath R G. 1997. Biogeography of Batrachospermum gelatinosum (Batrachospermales, Rhodophyta) in North America based on molecular and morphological data. Journal of Phycology, 33(3): 520–526, https://doi.org/10.1111/j.0022-3646.1997.00520.x.
Xiao S H, Zhang Y, Knoll A H. 1998. Tree-dimensional preservation of algae and animal embryos in a Neoproterozoic phosphorite. Nature, 391(6667): 553–558, https://doi.org/10.1038/35318.
Xie S L, Ling Y J. 2004. A taxonomic study of freshwater red algae from Shanxi province, North China. Acta Botanica Boreali-Occidentalia Sinica, 24(8): 1489–1492. (in Chinese with English abstract)
Xie S L. 2001. Studies on Batrachospermales (Rhodophyta) from China. Doctoral Dissertation, Institute of Hydrobiology, Chinese Academy of Sciences. (in Chinese with English abstract)
Yang E C, Boo S M, Bhattacharya D, Saunders G W, Knoll A H, Fredericq S, Graf L, Yoon H S. 2016. Divergence time estimates and the evolution of major lineages in the florideophyte red algae. Scientific Reports, 6(1): 21361, https://doi.org/10.1038/srep21361.
Žuljević A, Kaleb S, Peña V, Despalatović M, Cvitković I, De Clerck O, Le Gall L, Falace A, Vita F, Braga J C, Antolić B. 2016. First freshwater coralline alga and the role of local features in a major biome transition. Scientific Reports, 6(1): 19642, https://doi.org/10.1038/srep19642.
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Dr. N. R. C. Eva (University of Puerto Rico, USA) is acknowledged for the English editing.
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Supported by the National Natural Science Foundation of China (Nos. 31670208, 41871037, 31800172) and the Fund for Shanxi “1331 Project”
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343_2021_1075_MOESM7_ESM.xls
Table S3. Pairwise distance (lower-left matrix) and number of nucleotide variance (upper-right matrix) of rbcL sequence among the taxa in this study.
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Table S4. Pairwise distance (lower-left matrix) and number of nucleotide variance (upper-right matrix) of COI-5P sequence among the taxa in this study.
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Table S5. Pairwise distance (lower-left matrix) and number of nucleotide variance (upper-right matrix) of psbA sequence among the taxa in this study.
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Han, J., Nan, F., Feng, J. et al. Phylogenetic, evolutionary, and biogeographic origin of the genus Sheathia (Batrachospermales, Rhodophyta). J. Ocean. Limnol. 40, 729–744 (2022). https://doi.org/10.1007/s00343-021-1075-0
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DOI: https://doi.org/10.1007/s00343-021-1075-0