Stasis and diversity in living fossils: Species delimitation and evolution of lingulid brachiopods

Ryutaro Goto; Tsuyoshi Takano; Koji Seike; Momo Yamashita; Gustav Paulay; Ku'ulei S Rodgers; Cynthia L Hunter; Piyoros Tongkerd; Shin'ichi Sato; Jae-Sang Hong; Kazuyoshi Endo

doi:10.1016/j.ympev.2022.107460

Stasis and diversity in living fossils: Species delimitation and evolution of lingulid brachiopods

Mol Phylogenet Evol. 2022 Oct:175:107460. doi: 10.1016/j.ympev.2022.107460. Epub 2022 Mar 28.

Authors

Affiliations

¹ Seto Marine Biological Laboratory, Field Science Education and Research Center, Kyoto University, 459 Shirahama, Nishimuro, Wakayama 649-2211, Japan; Museum of Zoology and Department of Ecology and Evolutionary Biology, University of Michigan, 1109 Geddes Avenue, Ann Arbor, MI 48109-1079, USA; Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8564, Japan. Electronic address: gotoryutaro@gmail.com.
² Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8564, Japan; Meguro Parasitological Museum, 4-1-1 Shimomeguro, Meguro, Tokyo 153-0064, Japan.
³ Geological Survey of Japan, National Institute of Advanced Industrial Science and Technology, 1-1-1 Highashi, Tsukuba, Ibaraki 305-0046, Japan; Department of Natural Environmental Studies, Graduate School of Frontier Sciences, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8564, Japan.
⁴ Geological Survey of Japan, National Institute of Advanced Industrial Science and Technology, 1-1-1 Highashi, Tsukuba, Ibaraki 305-0046, Japan; National Museum of Nature and Science, Amakubo 4-1-1, Tsukuba 305-0005, Japan.
⁵ Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA.
⁶ Hawaii Institute of Marine Biology, School of Ocean and Earth Science and Technology, University of Hawaii, Kaneohe, HI 96744, USA.
⁷ School of Life Sciences, 2450 Campus Road, University of Hawaii, Honolulu, HI 96822, USA.
⁸ Department of Biology, Faculty of Science, Chulalongkorn University, Phyathai Road, Patumwan, Bangkok 10330, Thailand.
⁹ Institute of Geosciences, Shizuoka University, Oya 836, Shizuoka 422-8529, Japan.
¹⁰ Department of Ocean Science, College of Natural Sciences, Inha University, Incheon 22212, Republic of Korea.
¹¹ Department of Earth and Planetary Science, School of Science, The University of Tokyo, 7-3-1 Hongo, Tokyo 113-0033, Japan.

PMID: 35358691
DOI: 10.1016/j.ympev.2022.107460

Abstract

The Lingulidae are often considered living fossils, because they have shown little morphological change since the Paleozoic. Limited morphological variation has also made the taxonomic study of living lingulids challenging. We investigated species diversity and phylogenetic relationships of extant lingulids and show that they are substantially more diverse than realized, demonstrating that morphological stasis was commonly accompanied by speciation. Species delimitation based on cytochrome c oxidase subunit I (COI) gene sequences from 194 specimens sampled from East Asia, Australia, Oceania, and the Americas suggested 14-22 species in the lingulids (9-17 species in Lingula and 4-5 species in Glottidia), in contrast to the 11-12 species currently recognized globally in the family. Four-gene phylogenetic analyses supported the sister relationship between Lingula and Glottidia. Within Lingula, L. adamsi, which possesses large, brownish shells, was recovered as sister to all remaining Lingula species, which have more or less greenish shells. Within the greenish Lingula clade, the 'L. anatina' complex was sister to the clade that includes the 'L. reevei' complex. The 'L. anatina' complex was further separated into two major clades with partly separate ranges centered on (i) temperate East Asia, and (ii) the tropical west-central Pacific. Within Glottidia, Pacific species were nested within Atlantic species. Time-calibrated phylogenetic analyses suggested that Lingula likely originated in the early Cretaceous contrary to a previously proposed hypothesis advocating a Cenozoic origin. The separation of Lingula and Glottidia appears to date from the Mesozoic, not from the Carboniferous, contrary to a previous hypothesis. Overall, our results uncovered substantial cryptic diversity in lingulids, which will form the basis for conservation and further taxonomic revision.

Keywords: Biogeography; Cryptic species; DNA barcoding; Indo-West Pacific; Isthmus of Panama; Lingula.

Publication types

Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Animals
Asia, Eastern
Fossils*
Hydrozoa*
Invertebrates / genetics
Phylogeny