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Phylogeny of Terrestrial Isopods Based on the Complete Mitochondrial Genomes, Subvert the Monophyly of Oniscidea

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Phylogeny of Terrestrial Isopods Based on the Complete Mitochondrial Genomes, Subvert the Monophyly of Oniscidea Rui Zhang Shanxi Normal University Ruru Chen Shanxi Normal University Jianmei An ( [email protected] ) Shanxi Normal University Carlos A. Santamaria University of South Florida Sarasota-Manatee Research article Keywords: Oniscidea, Phylogeny, new subfamily, Ligiidae, Ligiaidea Posted Date: May 21st, 2020 DOI: https://doi.org/10.21203/rs.3.rs-25479/v1 License: This work is licensed under a Creative Commons Attribution 4.0 International License. Read Full License Page 1/26 Abstract Background: Oniscidea is the only truly terrestrial taxon within the Crustacea, and vital to soil formation. However, the monophyly of suborder Oniscidea has been in dispute since 1995, with different studies disagreeing on whether the coastal Ligiidae are included within the suborder. To clarify the phylogenetic hypothesis of suborder Oniscidea, we sequenced the complete mitochondrial genomes of Ligia exotica (Roux, 1828) and Mongoloniscus sinensis (Dollfus, 1901). Results: Like most metazoan, the complete mitogenomes of two species with circular double strands. The structure and characters of mitogenomes of these two species are analyzed. The constructed phylogenetic analyses show that Oniscidea is polyphyletic group, with Ligia being more closely related to marine isopods (Valvifera + Cymothoida + Sphaeromatidea). Conclusions: We elevate the taxonomic status of the family Ligiidae to the suborder Ligiaidea which are with parallel rank with Oniscidea. Ligiaidea is much primitive than other exact terrestrial isopods. Crinocheta are strongly monophyly, family Agnaridae is more closely related to Porcellionidae rather than Armadillididae. Background Isopoda Latreille, 1817, with more than 10,300 species, is the largest taxon within Peracarida and contains species exhibiting amazing ecological diversity and morphological plasticity [1, 2]. The distribution range of the Isopoda ranges from the deep oceans to elevations of 4,700-m above sea level. Currently, the Isopoda is divided into several sub-orders, with all terrestrial species being placed in the Oniscidea [3, 4]. Members of this suborder are saprophagous residents of damp and gloomy environment, and most of them hide during the day and come out at night, due to their extreme sensitivity to temperature, humidity, light and other conditions in the environment. The suborder is currently separated into ve lineages: Ligiidae, Tylidae, Meaoniscidae, Synocheta and Crinocheta [5, 6]. Of these lineages, the two formers appear to contain at least some amphibian genera, with Ligia Fabricius 1798 being of particular interest as its morphological, physiological and behavioral characteristics have led them to be considered intermediate forms between the marine isopod ancestors of and the modern land-forms of the Oniscidea [6, 7]. Indeed, Schmidt (2008) reported the more primitive species in the Oniscidea is the Ligiidae based on the morphological features of 3527 species, and the evolution of terrestrial isopods was from aquatic to terrestrial, not pass through the fresh water stage [6]. Thus, understanding the placement of Ligiidae within the Oniscidea is critical to understand the evolution of terrestrial isopods. The Oniscidea have been regarded as a monophyletic group [5, 8, 9] based on shared morphological characters or phylogenetic analyses of one to two genes. Recent studies; however, have failed to capture the monophyly of the Oniscidea using various approaches and data types [10, 11, 12, 13, 14, 15]. Most recently, Dimitriou et al (2019) failed to recover the monophyly of the Oniscidea when carrying out phylogenetic reconstructions based on four highly conserved nuclear genes. In said study, Ligia species were reported to be most closely related to species within marine sub-orders instead of representing the Page 2/26 most basal split within a monophyletic Oniscidea clade, thus casting doubt not only in the placement of Ligiidae within the Oniscidea but also in our historical understanding of the evolutionary history of the terrestrial isopods. Considering additional support is needed for these ndings, in this study, we analyze the mitochondrial genomes (hereafter mitogenomes) of two Ligia species, as well as an additional 22 other isopod species, to explore the evolutionary path of the Oniscidea. Our goal is to clarify the phylogenetic relationships amongst the Oniscidea. Results Genome organization and base composition The mitochondrial genome of M. sinensis and L. exotica are circular, double-stranded DNA moledules, 16,018 and 14,978 bp in length respectively (Figs. 1 & 2). The complete mitogenome of M. sinensis contains 34 mt genes: 13 protein-coding genes (PCGs), 19 tRNA genes, and two rRNA genes (Fig. 1). It lacks three tRNA genes: TrnA, trnE, trnL1. The average A + T content of the M. sinensis mt genome is approximately 75.32%, which is higher than other isopods (typical range: 54.4%-71.2). 18 overlapping regions and 13 intergenic regions are found in the genome. (Table 1). Nucleotide frequencies of all mt genes of M. sinensis are listed (Table 2). Page 3/26 Table 1 Gene content of the Mongoloniscus sinensis. Mitogenome Length (bp) Feature Stranda Position Initiation Stop Anticodon Intergenic Codon Codon nucleotide cob - 1–1,107 1107 ATG TAA 64 nad5 + 1,172- 1713 ATT TAA * 2,884 trn-F + 2,885- 68 GAA -33b 2,952 trn-H - 2,920- 65 GTG 5 2,984 nad4 - 2,990- 1344 ATG TAA * 4,333 nad4l - 4,334- 279 ATT TAA -5 4,612 trn-P - 4,608- 58 TGG -4 4,665 nad6 + 4,662- 492 ATT TAA -2 5,153 trn-S2 + 5,152- 51 TGA -9 5,202 rrnL - 5,194- 1143 21 6,336 trn-Q - 6,358- 67 TTG 47 6,424 trn-M + 6,472- 58 CAT -16 6,529 nad2 + 6,514- 1005 ATG TAG -10 7,518 trn-C - 7,509- 54 GCA -18 7,562 trn-Y - 7,545- 56 GTA 4 7,600 *Gene borders are defned based on borders with adjacent genes. aPlus strand (+)/minus strand (−). bNegatve values represent overlapping nucleotdes. Page 4/26 Length (bp) Feature Stranda Position Initiation Stop Anticodon Intergenic Codon Codon nucleotide cox1 + 7,605- 1536 ATG TAA 1 9,140 trn-L2 + 9,142- 67 TAA -10 9,208 cox2 + 9,199- 672 ATC TAA -2 9,870 trn-K + 9,869- 58 TTT -13 9,926 trn-D + 9,914- 62 GTC -8 9,975 atp8 + 9,968 − 156 ATT TAA -13 10,123 atp6 + 10,111 − 675 ATG TAA * 10,785 cox3 + 10,786 − 828 ATG TAA -41 11,613 trn-R + 11,573 − 61 TCG 21 11,633 nad3 + 11,655 − 357 ATT TAA -41 12,011 trn-V + 11,971 − 55 TAC -9 12,025 *Gene borders are defned based on borders with adjacent genes. aPlus strand (+)/minus strand (−). bNegatve values represent overlapping nucleotdes. Page 5/26 Length (bp) Feature Stranda Position Initiation Stop Anticodon Intergenic Codon Codon nucleotide nad1 - 12,017 − 924 ATA TAA 1 12,940 trn-N + 12,942 − 67 GTT -2 13,008 rrnS + 13,007– 717 -17 13,723 trn-I + 13707– 62 TCA 4 13768 trn-W + 13,773 − 54 TCA 292 13,826 trn-G + 14,119 − 58 TCC 485 14,176 trn-T + 14,662 − 64 TGT 879 14,725 trn-S1 + 15,605 − 73 TCT 341 15,677 *Gene borders are defned based on borders with adjacent genes. aPlus strand (+)/minus strand (−). bNegatve values represent overlapping nucleotdes. Page 6/26 Table 2 Base composition of whole genome, protein-coding gene, rRNA Region A% C% G% T% A + G + AT GC +/-strand T% C% skew skew (strand) Isopoda ground pattern Whole 37.13 10.68 14.00 38.19 75.32 24.68 -0.014 0.134 genome cob (-) 30.17 15.9 11.47 42.46 72.63 27.37 -0.169 -0.162 - nad5 (+) 33.80 7.82 15.47 42.91 76.71 23.29 -0.119 0.328 + nad4 (-) 30.21 15.85 8.78 45.16 75.37 24.63 -0.198 -0.287 - nad4l (-) 34.41 9.32 9.68 46.59 81.00 19.00 -0.150 0.019 - nad6 (+) 33.74 6.71 10.98 48.58 82.32 17.68 -0.180 0.241 + rrnL(-) 40.24 9.97 10.24 39.55 79.79 20.21 0.009 0.013 - nad2 (+) 36.42 8.06 13.53 41.99 78.41 21.59 -0.071 0.230 + cox1 (+) 27.93 14.52 17.19 40.36 68.29 31.71 -0.182 0.084 + cox2 (+) 33.33 13.10 14.73 38.84 72.17 27.83 -0.076 0.059 + atp8 (+) 37.18 10.90 8.97 42.95 80.13 19.87 -0.072 -0.097 + atp6 (+) 32.00 11.26 14.81 41.93 73.93 26.07 -0.134 0.136 + cox3 (+) 27.78 14.86 16.18 41.18 68.96 31.04 -0.194 0.043 + nad3 (+) 31.37 9.24 14.85 44.54 75.91 24.09 -0.173 0.233 + nad1 (-) 30.30 13.1 12.88 43.72 74.03 25.97 -0.181 -0.008 - rrnS (+) 36.12 13.39 18.13 32.36 68.48 31.52 0.055 0.150 + The circular mitogenome of Ligia exotica is composed of 13 PCGs, 21 tRNA genes, two rRNA genes, one non-coding region, while only lacking the trnG gene (Fig. 2). The average A + T content of the L. exotica mt genome is approximately 59.13%. 17 overlapping regions and 13 intergenic regions are found in the genome (Table 3). Nucleotide frequencies of all mt genes of M. sinensis are listed (Table 4). Page 7/26 Table 3 Gene content of the Ligia exotica. Mitogenome Length (bp) Feature Stranda Position Initiation Stop Anticodon Intergenic Codon Codon nucleotide trnE + 663–724 62 TTC trnS1 + 725–787 63 TCT 17 cob - 805-1,938 1134 ATA TAA * trnT - 1,939- 59 TGT -8b 1,997 nad5 + 1,990- 1728 ATT TAG -8 3,717 trnF + 3,710- 59 GAA -2 3,768 trnH - 3,767- 62 GTG * 3,828 nad4 - 3,829- 1330 ATG T -7 5,158 nad4l - 5,152- 297 ATA TAA 6 5,448 trnP - 5,455- 62 TGG 1 5,516 nad6 + 5,518- 507 ATT TAG -2 6,024 trnS2 + 6,023 − 62 TGA * 6,084 rrnL - 6,085 − 1184 -7 7,268 trnV - 7,262- 59 TAC 2 7,320 trnQ - 7,323- 55 TTG 4 7,377 *Gene borders are defned based on borders with adjacent genes.
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    • • • • • • I att,AZ /• •• 21 - • '11 n4I3 - • v., -hi / NT I- r Arty 1 4' I, • • I • A • • • Printed in Great Britain by Lavenham Press NERC Copyright 1985 Published in 1985 by Institute of Terrestrial Ecology Administrative Headquarters Monks Wood Experimental Station Abbots Ripton HUNTINGDON PE17 2LS ISBN 0 904282 85 6 COVER ILLUSTRATIONS Top left: Armadillidium depressum Top right: Philoscia muscorum Bottom left: Androniscus dentiger Bottom right: Porcellio scaber (2 colour forms) The photographs are reproduced by kind permission of R E Jones/Frank Lane The Institute of Terrestrial Ecology (ITE) was established in 1973, from the former Nature Conservancy's research stations and staff, joined later by the Institute of Tree Biology and the Culture Centre of Algae and Protozoa. ITE contributes to, and draws upon, the collective knowledge of the 13 sister institutes which make up the Natural Environment Research Council, spanning all the environmental sciences. The Institute studies the factors determining the structure, composition and processes of land and freshwater systems, and of individual plant and animal species. It is developing a sounder scientific basis for predicting and modelling environmental trends arising from natural or man- made change. The results of this research are available to those responsible for the protection, management and wise use of our natural resources. One quarter of ITE's work is research commissioned by customers, such as the Department of Environment, the European Economic Community, the Nature Conservancy Council and the Overseas Development Administration. The remainder is fundamental research supported by NERC. ITE's expertise is widely used by international organizations in overseas projects and programmes of research.
  • Orden Isopoda: Suborden Oniscidea

    Orden Isopoda: Suborden Oniscidea

    Revista IDE@ - SEA, nº 78 (30-06-2015): 1–12. ISSN 2386-7183 1 Ibero Diversidad Entomológica @ccesible www.sea-entomologia.org/IDE@ Clase: Malacostraca Orden ISOPODA: Oniscidea Manual CLASE MALACOSTRACA Orden Isopoda: Suborden Oniscidea Lluc Garcia *Museu Balear de Ciències Naturals, Sóller, Mallorca (Illes Balears) Imagen superior: Oniscus asellus. Fotografía LL. Garcia 1. Breve definición del grupo y principales caracteres diagnósticos 1.1. Morfología. Generalidades. Los isópodos terrestres (Oniscidea) son crustáceos eumalacostráceos pertenecientes al orden Isopoda, aunque reúnen una serie de características morfológicas y fisiológicas relacionadas con su modo de vida terrestre que permiten considerarlos como un grupo natural bien definido, considerado actualmente como monofilético (Schmidt, 2002, 2003, 2008). Como todos los representantes del orden, su cuerpo está dor- soventralmente aplanado y se divide en tres partes bien diferenciables a simple vista: 1. El céfalon, en el que sitúan los ojos, en la mayoría de los casos compuestos; dos pares de ante- nas; y el aparato masticador con un par de mandíbulas, que son asimétricas, y dos pares de maxilas. En los isópodos terrestres el céfalon está compuesto por la cabeza propiamente dicha y por el primer seg- mento del pereion, soldado a ésta y llamado también segmento maxilipedal por insertarse en él los maxilí- pedos, que cubren el resto de piezas bucales. La división entre este segmento y el resto de la cabeza es invisible en vista dorsal en la gran mayoría de isópodos terrestres aunque sí que es apreciable en forma surcos laterales que lo separan de la región cefálica. Por eso se debe considerar más propiamente como un cefalotórax.
  • First Record of the Species Complex in the Ligia Baudiniana American Gulf

    First Record of the Species Complex in the Ligia Baudiniana American Gulf

    F1000Research 2017, 6:1602 Last updated: 16 NOV 2017 RESEARCH NOTE First record of the Ligia baudiniana species complex in the American Gulf of Mexico Coastline, as confirmed by morphological and molecular approaches [version 1; referees: 2 approved] Carlos A. Santamaria , Edgar T. Bischoff III, Moe Aye, Keith W. Phillips, Victoria Overmeyer Biology Program, College of Science and Mathematics, University of South Florida Sarasota-Manatee, Sarasota, FL, 34243, USA v1 First published: 30 Aug 2017, 6:1602 (doi: 10.12688/f1000research.12459.1) Open Peer Review Latest published: 30 Aug 2017, 6:1602 (doi: 10.12688/f1000research.12459.1) Referee Status: Abstract Ligia isopods exhibit a constrained morphology that makes identification difficult. In the Greater Caribbean, a convoluted taxonomic history has left the Invited Referees distributional limits of Ligia baudiniana unclear. To date, no confirmed records 1 2 of this species exist from the American Gulf of Mexico. Herein, we report the presence of L. baudiniana in Sarasota-Manatee Florida, as confirmed by version 1 morphological and molecular approaches. This is the first record of this species published report report in the region and a ~300Km extension of its range. Specimens were collected 30 Aug 2017 in mangroves, underscoring the importance of protecting these habitats. 1 Mary K. Wicksten, Texas A&M University, USA 2 Stefano Taiti, National Research Council (Italy), Italy Discuss this article Comments (0) Corresponding author: Carlos A. Santamaria ([email protected]) Author