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Phylogenetic Position of Phthiraptera (Insecta: Paraneoptera) and Elevated Rate of Evolution in Mitochondrial 12S and 16S Rdna

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Phylogenetic Position of Phthiraptera (Insecta: Paraneoptera) and Elevated Rate of Evolution in Mitochondrial 12S and 16S Rdna MOLECULAR PHYLOGENETICS AND EVOLUTION Molecular Phylogenetics and Evolution 29 (2003) 102–114 www.elsevier.com/locate/ympev Phylogenetic position of Phthiraptera (Insecta: Paraneoptera) and elevated rate of evolution in mitochondrial 12S and 16S rDNA Kazunori Yoshizawaa,* and Kevin P. Johnsonb a Systematic Entomology, Department of Ecology and Systematics, Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan b Illinois Natural History Survey, 607 East Peabody Drive, Champaign, IL 61820-6970, USA Received 21 August 2002; revised 16 February 2003 Abstract Phthiraptera (chewing and sucking lice) and Psocoptera (booklice and barklice) are closely related to each other and compose the monophyletic taxon Psocodea. However, there are two hypotheses regarding their phylogenetic relationship: (1) monophyletic Psocoptera is the sister group of Phthiraptera or (2) Psocoptera is paraphyletic, and Liposcelididae of Psocoptera is the sister group of Phthiraptera. Each hypothesis is supported morphologically and/or embryologically, and this problem has not yet been resolved. In the present study, the phylogenetic position of Phthiraptera was examined using mitochondrial 12S and 16S rDNA sequences, with three methods of phylogenetic analysis. Results of all analyses strongly supported the close relationship between Phthiraptera and Liposcelididae. Results of the present analyses also provided some insight into the elevated rate of evolution in mitochondrial DNA (mtDNA) in Phthiraptera. An elevated substitution rate of mtDNA appears to originate in the common ancestor of Phthiraptera and Liposcelididae, and directly corresponds to an increased G + C content. Therefore, the elevated substitution rate of mtDNA in Phthiraptera and Liposcelididae appears to be directional. A high diversity of 12S rDNA secondary structure was also observed in wide range of Phthiraptera and Liposcelididae, but these structures seem to have evolved independently in different clades. Ó 2003 Elsevier Science (USA). All rights reserved. 1. Introduction morphology of Phthiraptera and Psocoptera and con- cluded that the family Liposcelididae of Psocoptera is Phthiraptera (chewing and sucking lice) and Pso- the sister group of Phthiraptera, making Psocoptera coptera (booklice, barklice, and psocids) have long been paraphyletic. However, almost all character states sup- recognized to be closely related to each other, and to- porting sister group relationship between Phthiraptera gether compose the monophyletic taxon Psocodea (e.g., and Liposcelididae are loss characters, and Lyal (1985) Kristensen, 1995). Monophyly of Psocodea is strongly mentioned that they may have evolved independently by supported by specialized hypopharingeal structure responding to their similar habitat. (Rudolph, 1982, 1983) and molecular data (Wheeler Phthiraptera are permanent ectoparasites of birds et al., 2001). In contrast, there are two alternative hy- and mammals. Background of the origin of parasitism potheses about the phylogenetic position of Phthirap- in Phthiraptera includes many interesting evolutionary, tera. In the traditional taxonomic system, the order morphological, and systematic problems (Barker, 1994; Psocoptera is treated as an independent order and the Waage, 1979). For example, was the louse ancestor order Phthiraptera is placed as its sister group. Mono- commensal with vertebrates? Was there a single or phyly of Psocoptera is supported by the egg structure multiple origin of parasitism in lice? Reliable estimation and the embryonic orientation (Seeger, 1979). Alterna- of the phylogenetic position of Phthiraptera would tively, Lyal (1985) extensively investigated the external provide a basis to answer these questions. In the present study, we investigate the phylogenetic position of * Corresponding author. Fax: +81-11-706-4939. Phthiraptera based on the mitochondrial 12S and 16S E-mail address: [email protected] (K. Yoshizawa). rDNA sequences. 1055-7903/$ - see front matter Ó 2003 Elsevier Science (USA). All rights reserved. doi:10.1016/S1055-7903(03)00073-3 K. Yoshizawa, K.P. Johnson / Molecular Phylogenetics and Evolution 29 (2003) 102–114 103 Mitochondrial 12S and 16S rDNA were selected for by Page et al. (2002) and a 16S rDNA alignment for several reasons, including the slow evolutionary rate, the insects is provided by Buckley et al. (2000). These sec- utility in the phylogenetic analyses of higher insect ondary structure models were used as alignment profiles. groups, and the existence of universal insect primers and Hickson et al. (2000) mentioned that results of 12S ease of reliable PCR amplification (Simon et al., 1994). rDNA alignment by ClustalW are improved with small Additionally, mitochondrial genomes of Phthiraptera gap and gap-extension costs. Thus, we tried alignments are interesting because of their apparently elevated with several pairs of Gap:Gap-extension costs (Gap substitution rates (Simmons and Weller, 2001). Hafner costs 10, 15, and 20; Gap-extension costs 0.1, 1, 3, and et al. (1994) and Page et al. (1998) reported an elevated 6.66). With high Gap-extension cost (e.g., 15:6.66 which rate of substitution in louse mitochondrial genes (COI is the default setting of ClustalX), genetic distances of and cyt-b) relative to vertebrate hosts. Johnson et al. some sequence pairs exceeded 1.0 which must be avoi- (2003) showed an elevated rate of substitution in louse ded. With lower Gap-extension costs, many stem re- mitochondrial COI gene relative to aphids. However, gions were recovered in the alignment, and different cost these studies lacked data of closest relatives of lice sets provided very similar alignments. Here 10:1 was (Psocoptera). Therefore, it is not clear whether the selected since it recovered the maximum numbers of phenomenon is unique to lice and when and how the stem regions. However, with other cost sets such as phenomenon originated. The present study is based on 20:0.1, results more closely matched secondary structure two mitochondrial genes and includes wide range of models for a few stem regions. Thus, such regions were Phthiraptera and Psocoptera, which will provide in- manually edited based on alignments resulting from sights about the origin of the elevated rate of evolution different costs to make the total alignment a closer in mitochondrial genes of lice and their relatives. match to secondary structure models. Hickson et al. (2000) also mentioned that different costs may be ap- propriate for different regions, especially where large 2. Materials and methods insertions or deletions occur. A NEXUS file of the aligned sequences is available from the following URL 2.1. Taxon sampling and sequence determination address or by request to the first author. <http://in- sect3.agr.hokudai.ac.jp/psocid/data/index.html> Specimens stored in 99.5% ethanol were used for the Each sequence was divided into two data sets (dis- study. Total DNA was extracted from 49 specimens cussed below). We performed partition homogeneity test following the methods described by Cruickshank et al. (Farris et al., 1994, 1995) to compare the homogeneity (2001). The samples include one neuropteran (root), of each data set using PAUP 4.0b10 PPC (Swofford, three hemipterans (closer outgroup of Psocodea), 27 2002). We also compared signal of each data set by psocopterans (including six Liposcelis), and 18 phthi- comparing positional congruence of the resulting trees rapterans (including three amblyceran, 14 ischnoceran, (Estabrook, 1992) using RadCon (Thorley and Page, and one anopluran lice) (Table 1). Primer sets 2000). 12Sai + 12Sbi and 16Sar + 16Sbr (Simon et al., 1994) were used to amplify partial sequences of mitochondrial 2.3. Phylogenetic analysis 12S and 16S rDNA, respectively. Modified 12Sbi primer (1 mer deleted from the 30 end) was used to amplify 12S As an initial analysis, equally weighted maximum rDNA of Bovicola. Reaction cycle was 94 °C for 30 fol- parsimonious (MP) analysis was performed with 100 lowed by 40 cycles of 94 °C for 3000,45°C for 4500, and TBR replication. However, G + C contents of the pres- 72 °C for 6000. Amplified products were purified using ent data set are highly variable among taxa (from 43.9% PCR Purification Kit (Qiagen) and sequenced by of Bovicola to 19.6% of Hemipsocus: DGC ¼ 24:3%) CEQ2000 DNA Analysis System (Beckman Coulter) which can be a problem for some phylogenetic analysis following manufacturerÕs protocols. Sequences of Het- methods, such as equally weighted parsimony (Galtier erodoxus macropus (Phthiraptera: Amblycera) and and Gouy, 1995). Thus, as an alternative method, Triatoma dimidiata (Hemiptera: Heteroptera) were ob- neighbor-joining (NJ) analysis was performed using tained from GenBank (Table 1). LogDet distances, which can correct the nonstationarity of base composition (Lockhart et al., 1994). The pro- 2.2. Alignment and data evaluation portion of invariant sites (0.1417) was estimated using maximum-likelihood. The difficulties of multiple sequence alignment of We also performed maximum-likelihood (ML) analy- louse 12S rDNA were stated by Paterson et al. (2000) sis, which is relatively robust to the nonstationary data and Page et al. (2002). Here, we aligned sequences using (Galtier and Gouy, 1995). Parameters for ML analysis Secondary Structure Mode of ClustalX (Thompson were estimated using Modeltest 3.06 (Posada and Cran- et al., 1997). A 12S rDNA alignment for lice is provided dall, 1998). As a result of Modeltest, the GTR + I + G 104 Table 1 K. Yoshizawa, K.P. Johnson / Molecular
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