Hostname: page-component-8448b6f56d-wq2xx Total loading time: 0 Render date: 2024-04-19T20:51:56.199Z Has data issue: false hasContentIssue false

Phylogenetic and ecomorphologic diversifications of spiriferinid brachiopods after the end-Permian extinction

Published online by Cambridge University Press:  08 September 2020

Zhen Guo
Affiliation:
State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences (Wuhan), Wuhan430074, PR China. E-mail: zhenguo@cug.edu.cn, zhong.qiang.chen@cug.edu.cn
Zhong-Qiang Chen*
Affiliation:
State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences (Wuhan), Wuhan430074, PR China. E-mail: zhenguo@cug.edu.cn, zhong.qiang.chen@cug.edu.cn
David A. T. Harper
Affiliation:
Palaeoecosystems Group, Department of Earth Sciences, Durham University, DurhamDH1 3LE, U.K. E-mail: david.harper@durham.ac.uk
*
*Corresponding author.

Abstract

The Order Spiriferinida spanning the latest Ordovician to Early Jurassic is a small group of brachiopods overshadowed by other taxon-rich clades during the Paleozoic. It diversified significantly after the end-Permian extinction and became one of the four major clades of Triassic brachiopods. However, the phylogeny and recovery dynamics of this clade during the Triassic still remain unknown. Here, we present a higher-level parsimony-based phylogenetic analysis of Mesozoic spiriferinids to reveal their evolutionary relationships. Ecologically related characters are analyzed to indicate the variances in ecomorphospace occupation and disparity of spiriferinids through the Permian–Triassic (P-Tr) transition. For comparison with potential competitors of the spiriferinids, the pre-extinction spiriferids are also included in the analysis. Phylogenetic trees demonstrate that about half of the Mesozoic families appeared during the Anisian, indicating the greatest phylogenetic diversification at that time. Triassic spiriferinids reoccupied a large part of the ecomorphospace released by its competitor spiriferids during the end-Permian extinction; they also fully exploited the cyrtiniform region and developed novel lifestyles. Ecomorphologic disparity of the spiriferinids dropped greatly in the Early Triassic, but it rebounded rapidly and reached the level attained by the pre-extinction spiriferids in the Late Triassic. The replacement in ecomorphospace occupation between spiriferids and spiriferinids during the P-Tr transition clearly indicates that the empty ecomorphospace released by the extinction of Permian spiriferids was one of the important drivers for the diversification of the Triassic spiriferinids. The Spiriferinida took over the empty ecomorphospace and had the opportunity to flourish.

Type
Articles
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press on behalf of The Paleontological Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Data available from the Dryad Digital Repository:https://doi.org/10.5061/dryad.sf7m0cg3r

References

Literature Cited

Ager, D. V. 1967. Brachiopod palaeoecology. Earth-Science Reviews 3:157179.CrossRefGoogle Scholar
Anderson, P. S. L. 2009. Biomechanics, functional patterns, and disparity in Late Devonian arthrodires. Paleobiology 35:321342.CrossRefGoogle Scholar
Anderson, P. S. L., Friedman, M., Brazeau, M. D., and Rayfield, E. J.. 2011. Initial radiation of jaws demonstrated stability despite faunal and environmental change. Nature 476:206209.CrossRefGoogle ScholarPubMed
Baeza-Carratalá, J. F., Manceñido, M. O., and Joral, F. García. 2016. Cisnerospira (Brachiopoda, Spiriferinida), an atypical Early Jurassic spire bearer from the Subbetic Zone (SE Spain) and its significance. Journal of Paleontology 90:10811099.CrossRefGoogle Scholar
Bapst, D. W., Bullock, P. C., Melchin, M. J., Sheets, H. D., and Mitchell, C. E.. 2012. Graptoloid diversity and disparity became decoupled during the Ordovician mass extinction. Proceedings of the National Academy of Sciences USA 109:34283433.CrossRefGoogle ScholarPubMed
Brazeau, M. D. 2011. Problematic character coding methods in morphology and their effects. Biological Journal of the Linnean Society 104:489498.CrossRefGoogle Scholar
Campbell, J. D. 1968. Rastelligera (Brachiopoda) of the Upper Triassic of New Zealand. Transactions of the Royal Society of New Zealand (Geology) 6:2337.Google Scholar
Carlson, S. J. 1991. A phylogenetic perspective on articulate brachiopod diversity and the Permo-Triassic extinction. Pp. 119142 in Dudley, E. C., ed. The unity of evolutionary biology, proceedings of the 4th International Congress of Systematic and Evolutionary Biology. Dioscorides Press, Portland, Ore.Google Scholar
Carlson, S. J. 2016. The evolution of Brachiopoda. Annual Review of Earth and Planetary Sciences 44:409438.CrossRefGoogle Scholar
Carlson, S. J., and Fitzgerald, P. C.. 2008. Sampling taxa, estimating phylogeny and inferring macroevolution: an example from Devonian terebratulide brachiopods. Earth and Environmental Science Transactions of the Royal Society of Edinburgh 98:311325.CrossRefGoogle Scholar
Carter, J. L., and Johnson, J. G.. 2006. Order Spiriferinida. Pp. 18771937 in Brachiopoda 5, Rhynchonelliformea (part). Part H of Kaesler, R. L., ed. Treatise on invertebrate paleontology. Geological Society of America, Boulder, Colo., and University of Kansas, Lawrence.Google Scholar
Carter, J. L., Johnson, J. G., Gourvennec, R., and Hou, H. F.. 1994. A revised classification of the spiriferid brachiopods. Annals of the Carnegie Museum 63:327374.Google Scholar
Chen, Z. Q., and Benton, M. J.. 2012. The timing and pattern of biotic recovery following the end-Permian mass extinction. Nature Geoscience 5:375383.CrossRefGoogle Scholar
Chen, Z. Q., Shi, G. R., and Kaiho, K.. 2002. A new genus of rhynchonellid brachiopod from the lower Triassic of South China and implications for timing the recovery of Brachiopoda after the end-Permian mass extinction. Palaeontology 45:149164.CrossRefGoogle Scholar
Chen, Z. Q., Campi, M. J., Shi, G. R., and Kaiho, K.. 2005a. Post-extinction brachiopod faunas from the Late Permian Wuchiapingian coal series of South China. Acta Palaeontologica Polonica 50:343363.Google Scholar
Chen, Z. Q., Kaiho, K., and George, A. D.. 2005b. Survival strategy of brachiopod fauna from the end-Permian mass extinction. Palaeogeography, Palaeoclimatology, Palaeoecology 224:232269.CrossRefGoogle Scholar
Chen, Z. Q., Kaiho, K., and George, A. D.. 2005c. Early Triassic recovery of the brachiopod faunas from the end-Permian mass extinction: a global review. Palaeogeography, Palaeoclimatology, Palaeoecology 224:270290.CrossRefGoogle Scholar
Chen, Z. Q., Kaiho, K., George, A. D., and Tong, J. N.. 2006a. Survival brachiopod faunas of the end-Permian mass extinction from the Southern Alps (Italy) and South China. Geological Magazine 143:301327.CrossRefGoogle Scholar
Chen, Z. Q., Shi, G. R., Yang, F. Q., Gao, Y. Q., Tong, J. N., and Peng, Y. Q.. 2006b. An ecologically mixed brachiopod fauna from Changhsingian deep-water basin of South China: consequence of end-Permian global warming. Lethaia 39:7990.CrossRefGoogle Scholar
Chen, Z. Q., Zhao, L. S., Wang, X. D., Luo, M., and Guo, Z.. 2018. Great Paleozoic–Mesozoic biotic turnings and paleontological education in China: a tribute to the achievements of Professor Zunyi Yang. Journal of Earth Science 29:721732.CrossRefGoogle Scholar
Ciampaglio, C. N. 2004. Measuring changes in articulate brachiopod morphology before and after the Permian mass extinction event: do developmental constraints limit morphological innovation? Evolution and Development 6:260274.CrossRefGoogle ScholarPubMed
Ciampaglio, C. N., Kemp, M., and McShea, D. W.. 2001. Detecting changes in morphospace occupation patterns in the fossil record: characterization and analysis of measures of disparity. Paleobiology 27:695715.2.0.CO;2>CrossRefGoogle Scholar
Congreve, C. R., and Lamsdell, J. C.. 2016. Implied weighting and its utility in palaeontological datasets: a study using modelled phylogenetic matrices. Palaeontology 59:447462.CrossRefGoogle Scholar
Congreve, C. R., Krug, A. Z., and Patzkowsky, M. E.. 2015. Phylogenetic revision of the Strophomenida, a diverse and ecologically important Palaeozoic brachiopod order. Palaeontology 58:743758.CrossRefGoogle Scholar
Cooper, G. A. 1972. Homeomorphy in recent deep-sea brachiopods. Smithsonian Contributions to Paleobiology 11:125.Google Scholar
Cowen, R., and Rudwick, M. J. S.. 1970. Deltidial spines in the Triassic brachiopod Bittnerula. Paläontologische Zeitschrift 44:8285.CrossRefGoogle Scholar
Curry, G. B., and Brunton, C. H. C.. 2007. Stratigraphic distribution of brachiopods. Pp. 29013081 in Brachiopoda 6, Supplement. Part H of Selden, P. A., ed. Treatise on invertebrate paleontology. Geological Society of America, Boulder, Colo., and University of Kansas, LawrenceGoogle Scholar
Dagys, A. S. 1974. Triasovye brakhiopody (morfologia, sistema, filogeniia, stratigraficheskoe znachenie i biogeografiia. Akademiia Nauk SSSR, Sibirskoe Otdelenie, Institut Geologii i Geofiziki, Trudy 214:1387.Google Scholar
Dagys, A. S. 1996. Remarks on the classification of punctate spiriferids. Pp. 9193 in Copper, P., and Jin, J. S., eds. Brachiopods. Proceedings of the 3rd International Brachiopod Congress, Sudbury, Ontario, September 1995. Balkema, Rotterdam.Google Scholar
Dick, D. G., and Maxwell, E. E.. 2015. The evolution and extinction of the ichthyosaurs from the perspective of quantitative ecospace modelling. Biology Letters 11:20150339.CrossRefGoogle ScholarPubMed
Erwin, D. H. 2007. Disparity: morphological pattern and developmental context. Palaeontology 50:5773.CrossRefGoogle Scholar
Gourvennec, R., and Carter, J. L.. 2007. Spiriferida and Spirifernida. Pp. 27722796 in Brachiopoda 6, Supplement. Part H of Selden, P. A., ed. Treatise on invertebrate paleontology. Geological Society of America, Boulder, Colo., and University of Kansas, Lawrence.Google Scholar
Gower, J. C. 1971. A general coefficient of similarity and some of its properties. Biometrics 27:857871.CrossRefGoogle Scholar
Guo, Z., Chen, Z. Q., and Harper, D. A. T.. 2020. The Anisian (Middle Triassic) brachiopod fauna from Qingyan, Guizhou, south-western China. Journal of Systematic Palaeontology 18:647701.CrossRefGoogle Scholar
Harper, D. A. T., and Moran, R.. 1997. Fossils explained 20: brachiopod life styles. Geology Today 13:235238.CrossRefGoogle Scholar
He, W. H., Zhang, K. X., Chen, Z. Q., Yan, J. X., Yang, T. L., Zhang, Y., Gu, S. Z., and Wu, S. B.. 2015. A new genus Liaous of early Anisian Stage (Middle Triassic) brachiopods from southwestern China: systematics, reassessment of classification of the Spiriferinioidea, community paleoecology, and paleoenvironmental implications. Journal of Paleontology 89:966979.CrossRefGoogle Scholar
Huang, Y. G., Chen, Z. Q., Wignall, P. B., and Zhao, L. S.. 2017. Latest Permian to Middle Triassic redox condition variations in ramp settings, South China: pyrite framboid evidence. Geological Society of America Bulletin 129:229243.CrossRefGoogle Scholar
Huang, Y. G., Chen, Z. Q., Algeo, T. J., Zhao, L. S., Baud, A., Bhat, G. M., Zhang, L., and Guo, Z.. 2019. Two-stage marine anoxia and biotic response during the Permian–Triassic transition in Kashmir, northern India: pyrite framboid evidence. Global and Planetary Change 172:124139.CrossRefGoogle Scholar
Ivanova, E. A. 1972. Osnovnyye zakonomernosti evolyutsii spiriferid (Brachiopoda). Paleontologicheskiĭ Zhurnal 1972:2842.Google Scholar
Johnson, J. G., and Blodgett, R. B.. 1993. Russian Devonian brachiopod genera Cyrtinoides and Komiella in North America. Journal of Paleontology 67:952958.CrossRefGoogle Scholar
Korn, D., Hopkins, M. J., and Walton, S. A.. 2013. Extinction space: a method for the quantification and classification of changes in morphospace across extinction boundaries. Evolution 67:27952810.Google ScholarPubMed
Lamsdell, J. C., and Selden, P. A.. 2016. From success to persistence: identifying an evolutionary regime shift in the diverse Paleozoic aquatic arthropod group Eurypterida, driven by the Devonian biotic crisis. Evolution 71:95110.CrossRefGoogle ScholarPubMed
Lee, S., Shi, G. R., Park, H., and Tazawa, J.-I.. 2016. Antitropicality and convergent evolution: a case study of Permian neospiriferine brachiopods. Palaeontology 59:109138.CrossRefGoogle Scholar
Lee, S., Jung, J., and Shi, G. R.. 2018. A three-dimensional geometric morphometric study of the development of sulcus versus shell outline in Permian neospiriferine brachiopods. Lethaia 51:114.CrossRefGoogle Scholar
Lloyd, G. T. 2016. Estimating morphological diversity and tempo with discrete character-taxon matrices: implementation, challenges, progress, and future directions. Biological Journal of the Linnean Society 118:131151.CrossRefGoogle Scholar
Ogg, J. G., and Chen, Z. Q.. 2020. The Triassic period. Chap. 25 in Gradstein, F. M., Ogg, J. G., Schmitz, M., and Ogg, G. M., eds. Geologic time scale 2020. Elsevier, Amsterdam.Google Scholar
R Core Team. 2018. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org.Google Scholar
Rong, J. Y., and Cocks, L. R. M.. 1994. True Strophomena and a revision of the classification and evolution of strophomenoid and “strophodontoid” brachiopods. Palaeontology 37:651694.Google Scholar
Rudwick, M. J. S. 1970. Living and fossil brachiopods. Hutchinson University Library, London.Google Scholar
Ruta, M., Angielczyk, K. D., Fröbisch, J., and Benton, M. J.. 2013. Decoupling of morphological disparity and taxic diversity during the adaptive radiation of anomodont therapsids. Proceedings of the Royal Society of London B 280:20131071.Google ScholarPubMed
Schreiber, H. A., Bitner, M. A., and Carlson, S. J.. 2013. Morphological analysis of phylogenetic relationships among extant rhynchonellide brachiopods. Journal of Paleontology 87:550569.CrossRefGoogle Scholar
Sclafani, J. A., Congreve, C. R., Krug, A. Z., and Patzkowsky, M. E.. 2018. Effects of mass extinction and recovery dynamics on long-term evolutionary trends: a morphological study of Strophomenida (Brachiopoda) across the Late Ordovician mass extinction. Paleobiology 44:603619.CrossRefGoogle Scholar
Shen, S. Z., and Clapham, M. E.. 2009. Wuchiapingian (Lopingian, Late Permian) brachiopods from the Episkopi Formation of Hydra Island, Greece. Palaeontology 52:713743.CrossRefGoogle Scholar
S. Z., Shen, Jin, Y. G., Zhang, Y., and Weldon, E. A.. 2017. Permian brachiopod genera on type species of China. Pp. 651881 in Rong, J. Y., Jin, Y. G., Shen, S. Z., and Zhan, R. B., eds. Phanerozoic brachiopod genera of China. Science Press, Beijing.Google Scholar
Shiino, Y. 2010. Passive feeding in spiriferide brachiopods: an experimental approach using models of Devonian Paraspirifer and Cyrtospirifer. Lethaia 43:223231.CrossRefGoogle Scholar
Shiino, Y., and Angiolini, L.. 2014. Hydrodynamic advantages in the free-living spiriferinide brachiopod Pachycyrtella omanensis: functional insight into adaptation to high-energy flow environments. Lethaia 47:216228.CrossRefGoogle Scholar
Shiino, Y., and Kuwazuru, O.. 2010. Functional adaptation of spiriferide brachiopod morphology. Journal of Evolutionary Biology 23:15471557.CrossRefGoogle ScholarPubMed
Shiino, Y., and Kuwazuru, O.. 2011. Theoretical approach to the functional optimisation of spiriferide brachiopod shell: optimum morphology of sulcus. Journal of Theoretical Biology 276:192198.CrossRefGoogle Scholar
Song, H. J., Wignall, P. B., Chu, D. L., Tong, J. N., Sun, Y. D., Song, H. Y., He, W. H., and Tian, L.. 2014. Anoxia/high temperature double whammy during the Permian–Triassic marine crisis and its aftermath. Scientific Reports 4:4132.CrossRefGoogle ScholarPubMed
Stubbs, T. L., and Benton, M. J.. 2016. Ecomorphological diversifications of Mesozoic marine reptiles: the roles of ecological opportunity and extinction. Paleobiology 42:547573.CrossRefGoogle Scholar
Sun, D. L., Xu, G. R., and Qiao, L.. 2017. Triassic brachiopod genera on type species of China. Pp. 8831011 in Rong, J. Y., Jin, Y. G., Shen, S. Z., and Zhan, R. B., eds. Phanerozoic brachiopod genera of China. Science Press, Beijing.Google Scholar
Sun, Y. D., Joachimski, M. M., Wignall, P. B., Yan, C. B., Chen, Y. L., Jiang, H. S., Wang, L. N., and Lai, X. L.. 2012. Lethally hot temperatures during the Early Triassic greenhouse. Science 388:366370.CrossRefGoogle Scholar
Sun, Y. D., Orchard, M. J., Kocsis, Á. T., and Joachimski, M. M.. 2020. Carnian–Norian (Late Triassic) climate change: evidence from conodont oxygen isotope thermometry with implications for reef development and Wrangellian tectonics. Earth and Planetary Science Letters 534:116082.CrossRefGoogle Scholar
Swofford, D. L. 2003. PAUP*. Phylogenetic analysis using parsimony (*and other methods), Version 4.0a166. Sinauer Associates, Sunderland, Mass.Google Scholar
Trotter, J. A., Williams, I. S., Nicora, A., Mazza, M., and Rigo, M.. 2015. Long-term cycles of Triassic climate change: a new δ18O record from conodont apatite. Earth and Planetary Science Letters 415:165174.CrossRefGoogle Scholar
Vörös, A., Kocsis, Á. T., and Pálfy, J.. 2016. Demise of the last two spire-bearing brachiopod orders (Spiriferinida and Athyridida) at the Toarcian (Early Jurassic) extinction event. Palaeogeography, Palaeoclimatology, Palaeoecology 457:233241.CrossRefGoogle Scholar
Vörös, A., Kocsis, Á. T., and Pálfy, J.. 2019. Mass extinctions and clade extinctions in the history of brachiopods: brief review and a post-Paleozoic case study. Rivista Italiana di Paleontologia e Stratigrafia 125:711724.Google Scholar
Waterhouse, J. B. 2016. On the evolution and classification of Spiriferida (Brachiopoda). Earthwise 14:1434.Google Scholar
Williams, A., Brunton, C. H. C., and MacKinnon, D. I.. 1997. Morphology. Pp. 321422 in Brachiopoda 1, Introduction. Part H of Kaesler, R. L., ed. Treatise on invertebrate paleontology. Geological Society of America, Boulder, Colo., and University of Kansas, Lawrence.Google Scholar
Wu, H. T., Shi, G. R., and Sun, Y. L.. 2019. The latitudinal gradient of shell ornament—a case study from Changhsingian (Late Permian) brachiopods. Earth-Science Reviews 197:102904.CrossRefGoogle Scholar
Xu, G. R., and Liu, G. C.. 1983. Systematic description; some problems in the research of Triassic brachiopods. Pp. 6783 in Yang, Z. Y., Xu, G. R., Wu, S. B., He, Y. L., Liu, G. C., and Yin, J. R., eds. Triassic of the south Qilian Mountains. Geological Publishing House, Beijing.Google Scholar
Yang, Z. Y., and Xu, G. R.. 1966. Triassic brachiopods of central Gueizhou (Kueichow) Province, China. China Industry Publishing House, Beijing.Google Scholar