East asian-eastern north american disjunction in the Onoclea sensibilis species complex: vicariance or peripatry?


K. Berry


DOI: https://doi.org/10.31111/palaeobotany/2021.12.88


Annotation

Disjunction between East Asian and eastern North American plants has been recognized since the time of Darwin. Although there is considerable evidence for congruent vicariance associated with late Neogene/Quaternary cooling among angiosperms, similar studies among specific fern families (e.g., Osmundaceae Martinov) have appeared incongruous with this pattern. Pteridologists continue to debate whether long-distance dispersal of wind-blown spores could have produced intercontinental disjunctions among ferns. To date, however, state-of-the-art historical biogeographical approaches have not been applied to this problem. In this investigation, multiple chloroplast gene (rbcL, atpA, atpB, and matK) sequences for ferns in the family Onocleaceae Pic. Serm. are drawn from GenBank, including those from the recently sequenced chloroplast genome of the East Asian fern O. sensibilis L. var. interrupta Maxim., and used to create molecular phylogenies using Bayesian (BEAUTi and BEAST) techniques. Using contemporary approaches for relaxed molecular clock divergence time estimation with fossil calibration, divergence time estimates for East Asian and eastern North American populations in the Onoclea sensibilis species complex are consistently reconstructed as the Pliocene (ca. 5 – 3.4 Ma), and the best-fitting historical biogeographic model is a DIVA-like (exclusively vicariant) model using BIOGEOBEARS in RASP4, with a low probability of peripatry. Accordingly, these molecular and fossil data appear congruent with the pattern observed among angiosperms, despite the propensity for long-distance dispersal of wind-blown spores in pteridophytes. The lack of evidence for peripatry in this lineage may be related to the presence of short-lived green spores in onocleoid ferns; however, this hypothesis requires further investigation.


Key words: ferns, biogeography, Onoclea sensibilis, vicariance, peripatry, disjunction


Section: Articles


How to cite

Berry K. 2021. East asian-eastern north american disjunction in the Onoclea sensibilis species complex: vicariance or peripatry? Palaeobotany, 12: 88–94. https://doi.org/10.31111/palaeobotany/2021.12.88


Received 10.09.2021; accepted for publication 20.11.2021


References

Ballantine, A. P., Rybczynski, N., Baker, P. A., Harrington, C. R., White, D. 2006. Pliocene Arctic temperature constraints from the growth rings and isotopic composition of fossil larch. – Palaeogeography, Palaeoclimatology, Palaeoecology, 242: 188–200. https://doi.org/10.1016/j.palaeo.2006.05.016

Barrington, D. S. 1993. Ecological and historical factors in fern biogeography. – Journal of Biogeography, 20: 275–279. https://doi.org/10.2307/2845635

Bouckaert, R., Vaughan, T. G., Barido-Sottani, J., Duchéne, S., Fourment, M., Gavryushkina, A., Heled, J., Jones, G., Kühnert, D., De Maio, N., Matschiner, M., Mendes, F. K., Müller, N. F., Ogilvie, H. A., du Plessis, L., Popinga, A., Rambaut, A., Rasmussen, D., Siveroni, I., Suchard, M. A., Wu, C.-H., Xie, D., Zhang, C., Stadler, T., Drummond, A. J. 2019. BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. – PLoS Computational Biology, 15: 1–28.

De la Vega, E., Chalk, T. B., Wilson, P. A., Bysani, R. P., Foster, G. L. 2020. Atmospheric CO2 during the mid-Piacenzian warm period. – Nature Scientific Reports, 10: 1–8. https://doi.org/10.1038/s41598-020-67154-8

Dolan, A. M., Haywood, A. M., Hunter, S. J., Tindall, D. J., Pickering, S. J. 2015. Modelling the enigmatic late Pliocene glacial event – marine isotope stage M2. – Global and Planetary Change, 128: 47–60.

Du, X.-Y., Lu, J.-M., Zhang, L.-B., Wen, J., Kuo, L.-Y., Mynssen, C. M., Schneider, H., Li, D.-Z. 2021. Simultaneous diversification of Polypodiales and angiosperms in the Mesozoic. – Cladistics, 37: 1–22. https://doi.org/10.1111/cla.12457

Edgar, R. C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. – Nucleic Acids Research, 32: 1792–1797. https://doi.org/10.1093/nar/gkh340

Fletcher, T. L., Telka, A., Rybczynski, N., Matthews, J. V., Jr. 2021. Neogene and early Pleistocene flora from Alaska, USA and Arctic/Subarctic Canada: new data, intercontinental comparisons and correlations. – Palaeontologia Electronica, 21: 1–62. https://doi.org/10.26879/1121

Gastony, G. J., Ungerer, M. C. 1997. Molecular systematics and a revised taxonomy of the onocleoid ferns (Dryopteridaceae: Onocleaceae). – American Journal of Botany, 84: 840–849. https://doi.org/10.2307/2445820

Goloboff, P. A., Catalano, S. A. 2012. GB-to-TNT: facilitating creation of matrices from GenBank and diagnosis of results in TNT. – Cladistics, 28: 503–513. https://doi.org/10.1111/j.1096-0031.2012.00400.x

Goloboff, P. A., Catalano, S. A. 2016. TNT version 1.5, including a full implementation of phylogenetic morphometrics. – Cladistics, 32: 221–238. https://doi.org/10.1111/cla.12160

Gray, A. 1859. Diagnostic characters of new species of phanogomous plants collected in Japan by Charles Wright, botanist of the U.S. North Pacific Exploring Expedition, with observations upon the relations of the Japanese flora to that of North America, and of other parts of the north temperate zone. – Memorial of American Academy of Arts and Sciences, Nature Sciences, 6: 377–453. https://doi.org/10.2307/25057953

Gray, A. 1878. Forest geography and archaeology, a lecture delivered before the Harvard University Natural History Society. – American Journal of Science and Arts, 16: 85–94, 183–196. https://doi.org/10.2475/ajs.s3-16.93.183

Kato, M. 1993. Biogeography of ferns: dispersal and vicariance. – Journal of Biogeography, 20: 265–274. https://doi.org/10.2307/2845634

Li, C., Lu, S., Ma, J., Gai, Y., Yang, Q. 2016. Phylogeographic history of the woodwardioid ferns, including species from Himalaya. – Palaeoworld, 25: 318–324. https://doi.org/10.1016/j.palwor.2014.10.004

Li, H.-L. 1952. Floristic relationships between eastern Asia and eastern North America. – Transactions of the American Philosophical Society, 42: 371–429. https://doi.org/10.2307/1005654

Lieberman, B. S. 2000. Paleobiogeography: using fossils to study global change, plate tectonics, and evolution. New York: Kluwer Academic, 208 p.

Lloyd, R. M. 1971. Systematics of the onocleoid ferns. – University of California Publications in Botany, 61: 1–93.

Lloyd, R. M., Klekowski, E. J., Jr. 1970. Spore germination and viability in Pteridophyta: evolutionary significance of chlorophyllous spores. – Biotropica, 2: 129–137. https://doi.org/10.2307/2989770

Maddison, W. P., Maddison, D. R. 2008. Mesquite: a modular system for evolutionary analysis. Version 3.61. http://www.mesquiteproject.org (accessed 6 August 2021)

Matzke, N. J. 2014. Model selection in historical biogeography reveals that founder-event speciation is a crucial process in island clades. – Systematic Biology, 63: 951–970. https://doi.org/10.1093/sysbio/syu056

Moran, R. C. 2008. Diversity, biogeography, and floristics. – Biology and Evolution of Ferns and Lycophytes. Cambridge: Cambridge University Press, p. 367–394. https://doi.org/10.1017/CBO9780511541827.015

Mountier, C. F., Case, B. S., Perrie, L., Brownsey, P., Paterson, A. M., Curran, T. J., Buckley, H. L. 2018. Patterns of range size in New Zealand ferns and lycophytes. – New Zealand Journal of Ecology, 42: 248–261. https://doi.org/10.20417/nzjecol.42.22

Rambaut, A. 2018. FigTree v.1.4.: Tree Figure Drawing Tool. – Institute of Evolutionary Biology, University of Edinburgh.

Rambaut, A., Drummond, A. J. 2021. TreeAnnotator v. 2.6.4. – Institute of Evolutionary Biology, University of Edinburgh.

Rothwell, G. W., Stockey, R. A. 1991. Onoclea sensibilis in the Paleocene of North America, a dramatic example of structural and ecological stasis. – Review of Palaeobotany and Palynology, 70: 113–124. https://doi.org/10.1016/0034-6667(91)90081-D

Sessa, E. B., Juslén, A., Väre, H., Chambers, S. M. 2017. Into Africa: molecular phylogenetics and historical biogeography of sub-Saharan woodferns (Dryopteris). – American Journal of Botany, 104: 1–10. https://doi.org/10.3732/ajb.1600392

Vakhrameev, V. A. 1991. Jurassic and Cretaceous floras and climates of the Earth. Cambridge: Cambridge University Press, 318 p.

Wolf, P. G., Schneider, H., Ranker, T. A. 2001. Geographic distributions of homosporous ferns: does dispersal obscure evidence of vicariance? – Journal of Biogeography, 28: 263–270. https://doi.org/10.1046/j.1365-2699.2001.00531.x

Wolfe, J. A., Tanai, T. 1980. The Miocene Seldovia Point Flora from the Kenai Group, Alaska. – United States Geological Survey Professional Paper, 1105: 1–52. https://doi.org/10.3133/pp1105

Wood, P., Besnard, G., Beerling, D. J., Osborne, C. P., Christian, P.-A. 2020. Phylogenomics indicates the “living fossil” Isoetes diversified in the Cenozoic. – PLoSONE, 15: 1–28. https://doi.org/10.1371/journal.pone.0227525

Xing, F. W., Kato, M. 2013. Onocleaceae. – Flora of China, Vol. 2–3 (Pteridophytes). St. Louis: Missouri Botanical Garden Press, p. 408–410.

Xiang, J.-Y., Wen, J., Peng, H. 2015. Evolution of the eastern Asian-North American biogeographic disjunctions in ferns and lycophytes. – Journal of Systematics and Evolution, 53: 2–32. https://doi.org/10.1111/jse.12141

Xiang, Q.-Y., Soltis, D. E., Soltis, P. S., Manchester, S. R., Crawford, D. H. 2000. Timing the eastern Asian-eastern North American floristic disjunction: molecular clock corroborates paleontological estimates. – Molecular Phylogenetics and Evolution, 15: 462–472. https://doi.org/10.1006/mpev.2000.0766

Yamakawa, C., Konishi, S. 2013. Fossil fern fronds from the early Pleistocene Kobiwako Group in Minakuchi, Shiga Prefecture, central Japan. – Journal of Fossil Research, 45: 61–69.

Yatabe, Y., Nishida, H., Murakami, N. 1999. Phylogeny of Osmundaceae inferred from rbcL nucleotide sequences and comparison to the fossil evidence. – Journal of Plant Research, 112: 397–404. https://doi.org/10.1007/PL00013894

Yu, Y., Blair, C., He, X. J. 2020. RASP 4: Ancestral state reconstruction for multiple genes and characters. – Molecular Biology and Evolution, 37: 604–606. https://doi.org/10.1093/molbev/msz257

Yu, Y., Harris, A. J., Blair, C., He, X. J. 2015. RASP (Reconstruct Ancestral State in Phylogenies): a tool for historical biogeography. – Molecular Phylogenetics and Evolution, 87: 46–49. https://doi.org/10.1016/j.ympev.2015.03.008

Yu, Y., Harris, A. J., He, X. J. 2010. S-DIVA (Stastistical Dispersal-Vicariance Analysis): A tool for inferring biogeographic histories. – Molecular Phylogenetics and Evolution, 56: 848–850. https://doi.org/10.1016/j.ympev.2010.04.011