Origin and evolution of earthworms belonging to the family Megascolecidae in China

doi:10.17520/biods.2018105

Abstract

Abstract:

A total of 579 Megascolecidae species have been reported in China through 2017. Most belong to the genera Amynthas and Metaphire. The family’s rich diversity merits further investigation into its evolutionary history. The arc of research indicates that analysis based on taxonomical and molecular methods reveals the evolutionary history of the family Megascolecidae in China. This paper summarizes updated findings regarding origin, speciation and dispersal of Megascolecidae in China, and discusses the evolution of major familial characteristics (e. g. spermathecal pores, caeca). Several analyses suggest that the ancestors of Megascolecidae in China may have come from the Indo-China Peninsula. Speciation radiation likely occurred after the Cretaceous-Palaeogene mass extinction, and species richness increased rapidly during the Cenozoic period. Ancestral range reconstruction analysis shows that species-groups are polyphyletic and that evolutionary reversal often resulted in sharp evolution of caeca, so we suggest that the current taxonomic system of Megascolecidae, which is based on a few morphological characters, should be reconstructed. We also note that the specific mechanism of evolution in Megascolecidae has not been studied. Hence, future research to reveal the specific evolutionary mechanism of Megascolecidae earthworms requires more systematic sampling of this family, combined with morphological research, phylogeny construction and analysis of geographical patterns, geological history and environmental factors.

http://jtp.cnki.net/bilingual/detail/html/SWDY201810005

Key words: Megascolecidae, earthworm, origin, speciation, evolution of characteristics

Jibao Jiang, Jiangping Qiu. Origin and evolution of earthworms belonging to the family Megascolecidae in China[J]. Biodiv Sci, 2018, 26(10): 1074-1082.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.biodiversity-science.net/EN/10.17520/biods.2018105

https://www.biodiversity-science.net/EN/Y2018/V26/I10/1074

Figures/Tables 4

Fig. 1 Distribution diagram of investigated Megascolecidae species in China before 2017. Some provinces with no surveys are blank.

Fig. 2 Divergence times of major groups belong to the family Megascolecidae from China. Mt09P, Outgroup; Mt33M, Belonging to genus Perionyx; Mt70M and Mt51T, Belonging to genus Amynthas.

Fig. 3 Projection map of phylogenetic tree of the family Megascolecidae from China

Fig. 4 Diversification of Megascolecidae species from China through time

References 42

[1]	Bouché MB (1972) Lombriciens de France: Écologie et Systématique. Institut National de la Recherche Agronomique, Paris.
[2]	Bouché MB (1983) The establishment of earthworm communities. In: Earthworm Ecology (ed. Satchell JE), pp. 431-448. Springer Netherlands, Dordrecht.
[3]	Bouché MB (1998) L'éolution spatiotemporelle des lombrixiens. Documents Pédozoologiques et Intégrologiques, 3, 1-28.
[4]	Byrne M, Yeates DK, Joseph L, Kearney M, Bowler J, Williams MAJ, Cooper S, Donnellan SC, Keogh JS, Leys R (2008) Birth of a biome: Insights into the assembly and maintenance of the Australian arid zone biota. Molecular Ecology, 17, 4398-4417.
[5]	Chang CH, Chen JH (2005) Taxonomic status and intraspecific phylogeography of two sibling species of Metaphire (Oligochaeta: Megascolecidae) in Taiwan. Pedobiologia, 49, 591-600.
[6]	Chang CH, Lin SM, Chen JH (2008) Molecular systematics and phylogeography of the gigantic earthworms of the Metaphire formosae species group (Clitellata, Megascolecidae). Molecular Phylogenetics and Evolution, 49, 958-968.
[7]	Chen Y (1956) Earthworms in China. Science Press,Beijing . (in Chinese)
	[陈义 (1956)中国蚯蚓. 科学出版社, 北京.]
[8]	Christensen B (1984) Asexual propagation and reproductive strategies in aquatic Oligochaeta. Hydrobiologia, 115, 91-95.
[9]	Christensen B (1994) Annelida-Clitellata. In: Reproductive Biology of Invertebrates, Vol. VI, Part B (eds Adiyodi KG, Adiyodi RG), pp. 1-23. John Wiley & Sons, Hoboken.
[10]	Csuzdi C (2012) Earthworm species, a searchable database. Opuscula Zoologica, 43, 97-99.
[11]	Domínguez J, Aira M, Breinholt JW, Stojanovic M, James SW, Pérez-Losada M (2015) Underground evolution: New roots for the old tree of lumbricid earthworms. Molecular Phylogenetics and Evolution, 83, 7-19.
[12]	Gates GE (1972) Burmese earthworms: An introduction to the systematics and biology of megadrile oligochaetes with special reference to Southeast Asia. Transactions of the American Philosophical Society, 62, 1-326.
[13]	Huang J, Xu Q, Sun ZJ, Wang C, Zheng DM (2006) Research on earthworm resources of China. I. Checklist and distribution. Journal of China Agricultural University, 11, 9-20. (in Chinese with English abstract)
	[黄健, 徐芹, 孙振钧, 王冲, 郑东梅 (2006) 中国蚯蚓资源研究. I. 名录及分布. 中国农业大学学报, 11, 9-20.]
[14]	James SW (2005) Preliminary molecular phylogeny in the Pheretima group of genera (Crassiclitellata: Megascolecidae) using Bayesian analysis. In: Advances in Earthworm Taxonomy II (Annelida: Oligochaeta) (eds Pop VV, Pop AA), pp. 129-142. Cluj University Press, Cluj-Napoca.
[15]	Jamieson BGM (1988) On the phylogeny and higher classification of the Oligochaeta. Cladistics, 4, 367-401.
[16]	Jiang JB (2016) Taxonomy and Molecular Phylogeny of the Family Megascolecidae Earthworms from China. PhD dissertation, Shanghai Jiao Tong University, Shanghai. (in Chinese with English abstract)
	[蒋际宝 (2016) 中国巨蚓科蚯蚓分类与分子系统发育研究. 博士学位论文, 上海交通大学, 上海.]
[17]	Keppel G, Lowe AJ, Possingham HP (2009) Changing perspectives on the biogeography of the tropical South Pacific: Influences of dispersal, vicariance and extinction. Journal of Biogeography, 36, 1035-1054.
[18]	Mazaud D, Bouché MB (1980) Introduction en surpopulation et migrations de lombriciens marqués. In: Soil Biology as Related to Land Use Practices (ed. Dindal DL), pp. 687-701. EPA, Washington, DC.
[19]	Michaelsen W (1900) Oligochaeta. R. Friedländer und Sohn, Berlin.
[20]	Michaelsen W (1921) Neue und wenig bekannte Oligochäten aus skandinavischen Sammlungen. Arkiv för Zoologi, 13, 1-25.
[21]	Michaelsen W (1929a) Zur Stammesgeschichte der Oligochäten. Zwiss Zoology, 134, 693-716.
[22]	Michaelsen W (1929b) The Oligochaete fauna of China. Lingnan Science Journal, 8, 157-166.
[23]	Michaelsen W (1931) The Oligochaeta of China. Peking Natural History Bulletin, 5, 1-24.
[24]	Omodeo P (1998) History of Clitellata. Italian Journal of Zoology, 65, 51-73.
[25]	Pérez-Losada M, Breinholt JW, Porto PG, Aira M, Domínguez J (2011) An earthworm riddle: Systematics and phylogeography of the Spanish Lumbricid Postandrilus. PLoS ONE, 6, e28153.
[26]	Qiu JP, Bouché MB (1998) Révision des taxons supraspécifiques de Lumbricoidea. Documents Pédozoologiques et Intégrologiques, 3, 179-216.
[27]	Qiu JP, Bouché MB, Patricio S (1998) Gathering, rationalization and managment of knowledge applied to the earthworm biodiversity. Documents Pédozoologiques et Intégrologiques, 3, 57-118.
[28]	Qiu JP (1999) Earthworms and their application in environment protection. I. Earthworms and their functions in ecosystem. Journal of Shanghai Agricultural College, 17, 227-232. (in Chinese with English abstract)
	[邱江平 (1999) 蚯蚓及其在环境保护上的应用. I. 蚯蚓及其在自然生态系统中的作用. 上海农学院学报, 17, 227-232.]
[29]	Qiu JP (2000) Earthworms and environmental protection. Guizhou Science, 18, 116-133. (in Chinese with English abstract)
	[邱江平 (2000) 蚯蚓与环境保护. 贵州科学, 18, 116-133.]
[30]	Shen HP, Tsai CF, Tsai SC (2002) Description of a new earthworm belonging to the genus Amynthas (Oligochaeta: Megascolecidae) from Taiwan and its infraspecific variation in relation to elevation. Raffles Bulletin of Zoology, 50, 1-8.
[31]	Shen HP, Chang CH, Chih WJ (2016) Four new earthworm species of the genus Amynthas (Megascolecidae: Oligochaeta) from southwestern Taiwan with re-description of tungpuensis Tsai, Shen and Tsai, 1999. Journal of Natural History, 50, 1889-1910.
[32]	Sims RW, Easton EG (1972) A numerical revision of the earthworm genus Pheretima auct. (Megascolecidae: Oligochaeta) with the recognition of new genera and an appendix on the earthworms collected by the Royal Society North Borneo Expedition. Biological Journal of the Linnean Society, 4, 169-268.
[33]	Sun J (2013) Taxonomy and Molecular Phylogeny of Amynthas Earthworms from China. PhD dissertation, Shanghai Jiao Tong University, Shanghai. (in Chinese with English abstract)
	[孙静 (2013) 中国远盲属蚯蚓分类学及分子系统发育研究.博士学位论文, 上海交通大学, 上海.]
[34]	Sun J, James SW, Jiang JB, Yao B, Zhang LL, Liu M, Qiu JP, Hu F (2017) Phylogenetic evaluation of Amynthas earthworms from South China reveals the initial ancestral state of spermathecae. Molecular Phylogenetics and Evolution, 115, 106-114.
[35]	Tsai CF, Shen HP, Tsai SC (2000a) Native and exotic species of terrestrial earthworms (Oligochaeta) in Taiwan with reference to Northeast Asia. Zoological Studies, 39, 285-294.
[36]	Tsai CF, Tsai SC, Liaw GJ (2000b) Two new species of protandric pheretimoid earthworms belonging to the genus Metaphire (Megascolecidae: Oligochaeta) from Taiwan. Journal of Natural History, 34, 1731-1741.
[37]	Wares JP, Turner TF (2003) Phylogeography and diversification in aquatic mollusks. In: Molecular Systematics and Phylogeography of Mollusks (eds Lydeard C, Lindberg D), pp. 229-269. Smithsonian Books, Washington, DC.
[38]	Zhang WX, Hendrix PF, Dame LE, Burke RA, Wu J, Neher DA, Li JX, Fu SL (2013) Earthworms facilitate carbon sequestration through unequal amplification of carbon stabilization compared with mineralization. Nature Communications, 4, 2576.
[39]	Zhao Q (2012) Taxonomy, Phylogeny and Paleogeography of Pheretimoid Earthworm Species (Megascolecidae: Amynthas, Metaphire) in Hainan Island (China). PhD dissertation, University of Rennes 1, Rennes.
[40]	Zhao Q (2015) Taxonomy, Phylogeny and Paleogeography of Pheretimoid Earthworm Species in Hainan Island (China). PhD dissertation, Shanghai Jiao Tong University, Shanghai. (in Chinese with English abstract)
	[赵琦 (2015) 中国海南岛环毛类蚯蚓分类学、系统发育学和古生物地理学研究. 博士学位论文, 上海交通大学, 上海.]
[41]	Zhao Q, Zhang M, Dong Y, Qiu JP (2017) New species of Megascolecidae (Oligochaeta) from Hainan Island, China. Annales Zoologici, 67, 221-227.
[42]	Zhu H (2016) Biogeographical evidences help revealing the origin of Hainan Island. PLoS ONE, 11, e0151941.