Exp Appl Acarol (2008) 44:77–88 DOI 10.1007/s10493-008-9140-3
Ecological and morphological attributes of parthenogenetic Japanese Schwiebea species (Acari: Acaridae) Kimiko Okabe · Norihide Hinomoto · Barry M. OConnor
Received: 27 December 2007 / Accepted: 5 March 2008 / Published online: 18 March 2008 © Springer Science+Business Media B.V. 2008
Abstract We examined life history traits and spermathecal morphology of both sexual and thelytokous Schwiebea mite species to determine ecological and morphological attributes during the evolution of parthenogenesis in this lineage. We reconstructed a molecular phylogeny of eight Japanese species using the internal transcribed spacer 1 (ITS1) of the ribosomal DNA (rDNA) and compared the sex ratio, developmental period, and egg number (fecundity) of each species within a species group by rearing them in the laboratory. Habitat preference was also analyzed from both collection and literature data. The reconstructed molecular phylogeny suggested that parthenogenesis evolved independently multiple times in this lineage. There were three clusters in the tree, in each of which the idiosoma, leg, setae, and spermathecal morphology of females was similar or identical; this suggested that mites in the same cluster were sister species. There was no relationship between sexual mode and life history traits or habitat preference. These results suggest that sexual and asexual species use diVerent microhabitats. Because S. similis (sexual), S. elongata (thelytokous), and S. estradai (thelytokous) were in the same cluster and spermathecae of the Wrst two were similar while that of the last was distinctively reduced, we hypothesized that speciation occurred in this order and that spermathecae are reduced and eventually lost during the course of parthenogenetic evolution. Keywords Life history trait · Molecular phylogeny · Sex ratio · Spermatheca · Thelytoky · Astigmata
K. Okabe (&) Forestry and Forest Products Research Institute, Tsukuba, Ibaraki 305-8687, Japan e-mail:
[email protected] N. Hinomoto National Institute of Agrobiological Sciences, Tsukuba, Ibaraki 305-8634, Japan B. M. OConnor Museum of Zoology, University of Michigan, Ann Arbor, MI 48109-1079, USA
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Introduction Many mites and ticks have evolved parthenogenetic reproductive modes, including arrhenotoky, thelytoky, and possibly deuterotoky (e.g., Oliver 1977; Norton et al. 1993; suspected deuterotoky reported by Okabe and OConnor 2003). For a founder, asexual reproduction is preferable when establishing a local population in a patchy habitat (e.g., temporal arrhenotoky in spider mites, Helle and Pijnacker 1985; ensliniellines associated with wasps, Okabe and Makino 2003), although parthenogenetic ascids are not superior colonizers (Walter and Lindquist 1995). While thelytokous species can take advantage of fast population growth by maintaining good genes, a lack of mating costs, and settling down in a new habitat with a small number of individuals, disadvantages or a so-called evolutionary dead end are expected because of the loss of new genetic combinations in the population (summarized by Norton et al. 1993). Despite the potential dead end, oribatids such as Desmonomata include species-rich parthenogenetic lineages, which is unexpected given that the low genetic diversity in asexual organisms is assumed to lead to extinction (Norton et al. 1993; Maraun et al. 2003, 2004; HeethoV et al. 2007). Because oribatids commonly live in continuous rather than patchy habitats and their parthenogenetic mode is generally thelytoky, the parthenogenetic mode that is adaptive for colonizers might not be thelytoky but arrhenotoky, which maintains a key element of sexual reproduction (i.e., recombination). Thus, to discuss theories associated with parthenogenesis, we should thoroughly distinguish one mode from another. Bdelloid rotifers and darwinulid ostracods also have species-rich thelytokous lineages (Butlin et al. 1998; Birky et al. 2005). In the thelytokous lineage, oribatid mites re-evolved sexuality from asexual ancestors, perhaps by re-functioning of spanandric males (Domes et al. 2007b). To reveal why thelytokous organisms diversify rather than go extinct, there are two possible approaches: genetic and ecological. Genetically, automictic meiosis has been proposed to explain why many organisms still employ a thelytokous reproductive mode but have not gone extinct (Wrensch et al. 1994; Schaefer et al. 2006). Ecologically, although there is little evidence for it, thelytoky is favored because organisms can avoid the costs associated with sexuality. It could be possible to explain why thelytokous species do not go extinct by examining the attributes of thelytokous life histories in lineages containing sexual and asexual sister species. The Astigmata, which are closely related to the Desmonomata of the Oribatida, show great taxonomic and ecological diversity (Domes et al. 2007c). Parthenogenesis evolved in the Astigmata (although it is less frequent than in the Desmonomata) in the Histiostomatidae as both arrhenotoky and thelytoky (Hughes and Jackson 1958), in the Winterschmidtiidae probably as arrhenotoky (Cowan 1984; Klompen et al. 1987; Okabe and Makino 2003), and in the Acaridae as thelytoky (Okabe and OConnor 2001a). While the advantage of arrhenotoky in the Ensliniellinae (Winterschmidtiidae) is clear, i.e., compensating for a male-less situation in a new host nest (Cowan 1984; Klompen et al. 1987; Okabe and Makino 2003), advantages and disadvantages of thelytokous life histories in Acaridae are not well known. Thelytokous species have life history traits and morphologies reXecting an asexual life cycle; for example, there are few to no males in a population (Okabe and OConnor 2003) and male morphology is reduced (Norton and Palmer 1991). Those life history traits might explain what life history traits should evolve in thelytokous species and/ or why thelytoky is expansive rather than destructive. Morphological traits might explain why re-evolution of sexuality is unlikely common. In this context, acarids are an ideal group of mites in which to study the evolution of reproductive mode because (1) the family includes morphologically and ecologically well
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studied species, (2) not all species are parthenogenetic but all parthenogenetic species are thelytokous, and (3) most species are easy to rear in the laboratory. The acarid genus Schwiebea contains multiple thelytokous species (Okabe and OConnor 2001a). For our morphological examination, we targeted the spermatheca, because in Astigmata it is distinctive, functionally important only for sexual species, and its morphology (i.e., shape, size, and appendages) varies among congeneric species. For example, mites in the Schwiebea barbei group have very similar external morphology throughout ontogeny, and only the spermathecae diVer between species (Manson 1972; Fain 1977; Fain and Fauvel 1988; Fain and Pagani 1989; Fain and Ferrando 1990; Okabe and OConnor 2000). In this study, to determine (1) if asexuality is connected to certain life history traits to avoid extinction and (2) if re-evolution of sexuality is possible, we examined life history traits and the morphology of sexual and asexual Schwiebea species. For these examinations, we compared sexual and asexual sister species because we expected that genetically close species would show explicit diVerences, rather than generalizing across many but not closely related species. Sister species were determined by molecular analysis. We collected living Schwiebea mites in Japan for both molecular and rearing experiments. We individually reared eight species (four of which are thelytokous), including sister species groups, to determine diVerences in life history traits (i.e., developmental period) and sex ratio associated with thelytoky. We also tried to determine if spermathecal morphology reXects sexual mode after conWrming that sister species have similar morphology. Because thelytokous Schwiebea species were only conWrmed by Okabe and OConnor (2000, 2001a), we analyzed only the Japanese species whose sexual mode we had conWrmed.
Materials and methods Mite collections Mites were collected in the Weld from diVerent environments (summarized in Table 1). Although it is diYcult to collect negative data on habitats (i.e., habitat types not suitable for a given species), we collected mites at as many sites as possible and included published and unpublished records to estimate habitat attributes. Colonies of Schwiebea sp3 and S. similis collected in the Weld and reared on dry yeast were donated by Dr. Y. Kuwahara. We collected the other mites in the Weld with associated organic material, including soil. The materials were packed in plastic bags with tight zipper-lock closures and maintained with wet Wlter paper sprinkled with dry yeast in an incubator at 25°C for about 2 weeks. Living mites were preserved in 99.5% ethanol for the molecular study or were reared using the mass rearing methods described by Okabe and OConnor (2001b). We maintained one population per species and used them for experiments. Molecular analysis DNA extraction, ampliWcation, cloning, and sequencing Mites were preserved in ethanol (99.5%) at 4°C until DNA extraction. DNA was extracted from mites using a GenomicPrep Cell and Tissue DNA Isolation Kit (GE Healthcare). Approximately 30 mites of each species were placed in 1.5-ml microcentrifuge tubes, submerged in liquid nitrogen for a few minutes, and then fully homogenized using pipette tips
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with 100 l of cell lysis solution. Further procedures were according to the manufacturer’s instructions. Finally, DNA was dissolved in 100 l of TE buVer (10 mM Tris–HCl [pH 8.0] and 0.1 mM ethylenediaminetetraacetic acid [EDTA]). PCR was performed in a total volume of 50 l, containing 1.0 l of mite DNA solution. The reaction buVer consisted of 0.2 mM dNTPs, 0.1 M each primer, 1.5 mM MgCl2, and 1.0 unit of Ex Taq DNA polymerase (Takara Bio) in 1£ Ex Taq buVer. The primer sequences were obtained from Hinomoto and Takafuji (2001): rD02 (5⬘-GTC GTA ACA AGG TTT CCG TAG G-3⬘) and rD03 (5⬘-TGG CTG CGT TCT TCA TCG-3⬘). The reaction mixture was put into a 0.2-ml thin-walled PCR tube, and ampliWcation was performed on an iCycler thermal cycler (Biorad) with the following proWle: 94°C for 3 min, followed by 35 cycles of 94°C for 1 min, 55°C for 1 min, and 72°C for 2 min. The Wnal strand elongation at 72°C was for 10 min. The resultant PCR products were puriWed using a Minelute PCR PuriWcation Kit (Qiagen) and dissolved in 10 l of H2O. The PCR ampliWed fragments were ligated into the pGEM-T vector (Promega) and introduced into Escherichia coli JM109 cells following the manufacturer’s instructions. Positive clones were cultured in LB medium after blue/white selection on LB agar plates, and plasmids were extracted by an automated plasmid extractor (PI-100, Kurabo). A sequencing reaction based on three plasmids was conducted with primers SP6 (5⬘-TAA TAC GAC TCA CTA TAG GGC GA-3⬘) and T7 (5⬘-ATT TAG GTG ACA CTA TAG AAT AC-3⬘), using a BigDye® Terminator Cycle Sequencing Kit and an ABI PRISM® 3100 Genetic Analyzer (Applied Biosystems) according to the manufacturer’s instructions. Sequence analysis Sequences obtained were aligned using CLUSTAL W (Thompson et al. 1994). We eliminated coding regions (18S and 5.8S) based on the sequences of Rhizoglyphus robini deposited in DDBJ (accession number DQ372568) and used only the internal transcribed spacer 1 (ITS1) sequence for analysis. Phylogenies were inferred using maximum likelihood (ML), neighbor-joining (NJ), and maximum parsimony (MP) in PAUP*4.0b10 (SwoVord 2000). The appropriate model for the ML analysis was selected by hierarchical likelihood ratio tests (hLRTs) in MODELTEST version 3.06 (Posada and Crandall 1998); the Hasegawa–Kishino–Yano model with rate variation among sites and a proportion of invariable sites (HKY + I + G; Hasegawa et al. 1985) represented the best Wt model of nucleotide substitution (2-test, P < 0.001). The starting tree was obtained using the NJ algorithm. For the NJ analysis, genetic distances were calculated using the same model. The same analyses were also performed on 10,000 bootstrapped data sets to estimate the conWdence of each branch for NJ and MP analyses. For ML, bootstrap values were obtained from 100 resamplings. Analyses of life history traits and spermathecal morphology We investigated the developmental period from egg to adult, fecundity (i.e., number of eggs laid per female), and sex ratio of S. aroajoae Fain, S. estradai Fain et Ferrando, Schwiebea sp1 (morphologically similar to Lamtoglyphus coineaui Fain), and Schwiebea sp3 (morphologically identical to S. aroajoae) by rearing them on mycelia of Botrytis cinerea Pers.:Fr. or Flammulina veltipes (Curt. ex Fr.) Sing. [both stock cultures were maintained at the Forestry and Forest Products Research Institute (FFPRI)] at 25°C following the individual rearing methods described by Okabe and OConnor (2001b). We used life history trait data documented by Okabe and OConnor (2001a) for S. elongata Banks, S. similes
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Reproductive mode
100
78.7 96.0
80.0
Schwiebea sp2 Asexual (thelytokous)
Group B S. araujoae Asexual (thelytokous) Schwiebea sp3 Asexual (thelytokous)
Group C S. similis
Asexual (thelytokous)
S. estradai
63.98 § 40.4 (40)g Forest litter (preserved in an incubator) 23.38 § 12.7 (16)h Peat-moss in bog Forest litter
Aqueduct water
Because the infected plant was imported, the mite might be accidentally introduced with it from out of Japan
f
In this study Fain and Ferrando (1990)e
Fain and Pagani (1989)
Mean developmental periods and fecundity were compared within a group. DiVerent superior alphabets show that the means are signiWcantly diVerent (P < 0.05)
Habitats showed materials from which each species were collected in Japan
Peat-moss in bog Salmon gills
Original species description
56.0 § 16.3 (26)g
Insect larva
e
14.0 § 0.9 (24)g
Okabe and OConnor (2001a), Banks (1906)e , Cooreman (1959) and Manson (1972) also from plant roots Fain and Fauvel (1988)
9.59 § 1.6 (50)h
137.6 § 57.2 (20)h Organic soil, termite nest, swimming pool, plant root
Okabe and OConnor (2001a) Manson (1972)e
Swimming pool, decaying plant In this study, Fain (1977)e also in a pool Horticultural plantf In this study
Okabe and OConnor (2001a)
Okabe and OConnor (2001a) Fain (1977)e
In this study
Sources
10.53 § 1.41 (43)i 97.85 § 81.6 (20)g Organic soil, green onion Plant root
11.35 § 1.94 (49)g 167.5 § 66.6 (12) 9.88 § 1.4 (46)h 90.40 § 56.6 (16)
19.37 § 1.46 (30)h 41.40 § 27.6 (16)h Peat-moss in bog
18.90 § 1.88 (20)h
8.91 § 0.8 (43)g
Habitatd
d
Both females and males are included
Mean § SD (n)
c
Females/(total egg numbers ¡ dead immature numbers)
b
a
100
Asexual 99.7 (may be deuterotokous)
S. elongate
Sexual
60.0
65.9
Female Developmental Egg numbers ratio (%)a period (at 25ºC)b,c (at 25ºC)c
Sexual
S. lebruni
Group A Schwiebea sp1 Sexual
Species
Table 1 Life history traits of Japanese Schwiebea mites with documented habitat information
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Manson, S. lebruni Fain, and Schwiebea sp2 (morphologically similar to S. lebruni in the study) in the analyses. Living females of the collected species were preserved in 70% ethanol and mounted in Hoyer medium after clearing with a mixture of lactophenol and Nesbitt Xuid (Krantz 1978). We identiWed mite species and examined spermathecal morphology under a compound microscope with phase and diVerential interference contrast.
Results Phylogeny of Schwiebea based on molecular analysis Sequences from 10 mite species were successfully aligned with few insertions and/or deletions (i.e., indels). The sequences were deposited in DDBJ (accession numbers AB370048– AB370080). The length of the overlapped region was about 596 bp after elimination of indels, and our analyses were based on this region. Based on the hLRTs, HKY + I + G (Hasegawa et al. 1985) was selected as the most appropriate model (2-test, P < 0.01). The Data Analysis in Molecular Biology and Evolution (DAMBE) test using the parameter values obtained above, in which the index of substitution saturation (Iss = 0.5808) was signiWcantly lower than the critical Iss value (Iss.c = 0.7231), showed little saturation among haplotypes; therefore, this region is suitable for molecular phylogenetic analysis of these species. The ML tree constructed using these parameters is shown in Fig. 1. All clones within a species formed a single clade with high bootstrap support. There were three well-distinguished clades; the Wrst consisted of Schwiebea sp1, Schwiebea sp2, and S. lebruni (hereafter referred as “group A”), the second consisted of S. similis, S. elongata, and S. estradai (group B), and the last consisted of S. araujoae and Schwiebea sp3 (group C). Evolution of parthenogenesis Based on the molecular phylogeny, parthenogenesis evolved at least three times in the Schwiebea lineage (Fig. 1). The three main clades each included a parthenogenetic species, and the sexual species were ancestral in groups A and B. All parthenogenetic species were thelytokous, and the proportion of males was very low or zero (Table 1). Spermathecal morphology Each group on the same line in Fig. 2 had similar spermathecal morphology. However, in group A, Schwiebea sp1 diVered from S. lebruni and Schwiebea sp2 in DNA sequence as well as in spermathecal morphology. Parthenogenetic Schwiebea sp3 and S. araujoae in group C were identical to each other, not only in spermathecal morphology but also in female idiosomal, leg, and setal morphology. Only spermathecae showed a consistent diVerence between groups (Fig. 2). Although female idiosoma, dorsal and ventral setae, prodorsal sclerites, and legs including setae and solenidia were identical in S. similes, S. elongata, and S. estradai, these species could be distinguished based on spermathecal morphology and DNA sequence (Figs. 1 and 2). When comparing spermathecal morphology, S. estradai diVered from the others by having a reduced spermatheca, whereas the spermathecae of S. similis and S. elongata were very similar. The spermatheca of one S. estradai population was reduced but somewhat similar to that of S. similis and S. elongata (e.g., see the duct and accessory organs at the
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Schwiebea sp2
100/100/100
98/100/92
A 100/100/100
Schwiebea lebruni
59/96/60
100/100/100
Schwiebea sp1
100/100/100
Schwiebea araujoae
83/100/85
B 100/100/100
100/-/-
100/100/100
100/100/100
100/100 /100
Schwiebea sp3
Schwiebea estradai
Schwiebea elongata
C
Schwiebea similis 100/100/100
100/100/100
100/100/100
Rhizoglyphus robini
Histiogaster rotundus
0.1
Fig. 1 Neighbor-joining tree (HKY + I + G) inferred from sequences of the internal transcribed spacer 1 (ITS1) of nuclear ribosomal DNA for 10 species. Rhizoglyphus robini and Histiogaster rotundus are used as outgroup. The scale of distances is shown under the tree. Numbers at nodes indicate bootstrap values (%) of 10,000 NJ, 10,000 maximum parsimony and 100 ML replicates, respectively, though only values over 50 are indicated
connection of the duct and the spermatheca of S. estradai [a] in Fig. 2), whereas the spermatheca of another S. estradai population had a remnant spermathecal duct connected to the copulatory opening.
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Group A
Schwiebea sp1
S. lebruni
Schwiebea sp2
Group B
10µm
Schwiebea sp3
S. araujoae
Group C
S. similis
S. elongata
S. estradai(a) S. estradai(b)
Fig. 2 Spermatheca morphology of eight Japanese Schwiebea mites. Three species on the Wrst line are included in the group A, two on the middle in the group B and three on the bottom in the group C. Schwiebea elongata and S. estradai indicated morphological variations in spermatheca but the most typical ones were diagramed
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Life history traits The percent of males never reached 50% in any Schwiebea species without treatment (Table 1). Although the female proportion of most thelytokous species was around 100%, S. araujoae had a relatively high proportion of males. There was no relationship between reproductive mode and developmental period or fecundity; sexual Schwiebea sp1 and asexual S. elongata and Schwiebea sp3 had short developmental periods, whereas the other asexual species (S. elongata and Schwiebea sp2) were most and least fecund, respectively. The developmental period diVered signiWcantly among group B species (Kruskal–Wallis test, P < 0.0001), but the sexual species did not necessarily develop fastest or slowest. Additionally, fecundity diVered among species in group B (Kruskal–Wallis test, P < 0.0004). There was no correlation between egg number and developmental period in the eight species (r = ¡0.66031) or within a group. No particular habitat characteristics were found in the Schwiebea species. In group A, sexual mites were collected from forest litter or peat moss, and asexual mites were collected from plant materials in a bog, which was as moist as in the peat-moss wetland. In group B, although sexual S. similis were collected in a drier habitat, sexual S. elongata were found in a wide range of habitats (Table 1). The presumed temperature in the peat moss was lowest, particularly in winter, because the wetland was located above 1,000 m in elevation. However, there was no relationship between temperature and reproductive mode.
Discussion Previous theories have stated that parthenogenesis is favored in physically unpredictable and complex environments (e.g., Bell 1982), although Norton et al. (1993) concluded that asexual species are adaptive in abiotically unstable and biotically depauperate environments because of their broadly adaptive genomes based on a general-purpose genotype (Lynch 1984). However, as Okabe and OConnor (2001a) demonstrated, there were no consistent characteristics of thelytokous habitats (Table 1); both sexual and asexual species were collected in an oligotrophic environment (a peat-moss bog) in group A, and both sexual and asexual species appeared in nutrient-rich soil (organic agricultural soil) in group C. Because none of the species we used failed to recolonize under the same rearing conditions, we suspect that congeneric species generally have very similar life history traits and that our hypothesis that a comparison of sexual and asexual sister species could demonstrate diVerent life history traits was not supported. However, our experiment was conducted only in a nutrient-rich environment, and asexual species could have tolerated lower nutrient availability. Because we collected both sexual and asexual species in the same sites (e.g., peat-moss bog) but never in the same sample, sexual and asexual species might use diVerent microhabitats. Many authors have tried to categorize niches for parthenogenetic (thelytokous) species, such as freshwater rather than marine, aquatic rather than terrestrial, higher altitudes and latitudes, disturbed rather than stable habitats, and smaller islands or archipelagos rather than continental areas (Maynard Smith 1978; Bell 1982). However, in the Mesostigmata, parthenogenetic ascid mites likely prefer stable soil or soil-like habitats (Walter and Lindquist 1995), and all-female uropodines are associated with forest soil and litter rather than unstable habitats (Bioszyk et al. 2004). In parthenogenetic oribatids, biotic uncertainty does not determine sexual mode, and the current theories (biotic-uncertainty, Muller’s ratchet, and general-purpose genotype) were not supported (Cianciolo and Norton 2006).
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The only known life history traits are that (1) they are not fast recolonizers and (2) they do not produce high numbers of eggs compared to sexual species (Domes et al. 2007a). Schwiebea species are also commonly collected in soil, although soil dwellers are not restricted to this genus (OConnor 1984). Both egg number and the developmental period of asexual species were inferior to those of sexual species in group A and S. estradai in group B (Table 1). This result also suggests that thelytokous species are not always fast colonizers. A very low proportion or absence of males is associated with thelytoky, which is common in Schwiebea mites that have a low proportion of males both in sexual and asexual species (this study; see Woodring 1969 for S. roketti). Schwiebea araujoae had a higher male ratio than a sexual species (S. similis). Although we do not have any evidence to support our hypothesis, we suspect that this might be because (1) the sex ratio is unstable in certain thelytokous Schwiebea, as S. elongata had 50% males in a population after the females who had male oVspring were selected (Okabe and OConnor 2003), or (2) we calculated the sex ratio from one sample. Schwiebea mites tend to inhabit relatively similar environments to those generally inhabited by oribatids (soil and forest litter), whereas acarids are often found in patchy habitats (OConnor 1994). Since many thelytokous mites in the Mesostigmata, Oribatida, and Astigmata inhabit soil and litter, we suggest that these habitats are highly associated with mite thelytoky. It seems that, biotically and/or abiotically, the soil environment reduces male numbers in the mite population and eventually leads to asexuality (thelytoky). According to the sex ratio theory (Hamilton 1967), the male ratio tends to be low in populations in which inbreeding is common. We suspect that this mating system is possible in Schwiebea because they are slow moving, have high fecundity, and are colonial. However, to conWrm this, more genetic studies are needed. Female morphology (and sometimes that of males and deutonymphs) was more similar within a group than among groups. Among the morphological traits we examined, the spermatheca was the best characteristic by which to distinguish species (Fig. 2). For instance, Schwiebea sp3 diVers from S. aroujoae based on the molecular analysis and spermathecal morphology, although both species are asexual and have very similar idiosomal shape and setation on the dorsum and legs (Figs. 1 and 2). Although the function corresponding to spermathecal shape is unknown, the varied but reduced spermathecae in S. estradai (100% female) suggest that thelytokous mites can eventually lose the spermatheca. We suspect that spermatheca (a) in Fig. 2 is ancestral and spermatheca (b) in Fig. 2 is more derived in S. estradai because spermatheca (a) is similar to that of S. similis, the shared sexual ancestor of S. estradi and S. elongata, which can produce more males than S. estradi. Therefore, we hypothesize that speciation occurred from sexual to asexual, and in the asexual lineage from S. elongata to S. estradi. Although parthenogenetic speciation has been documented in the Oribatida (Laumann et al. 2007), this is the Wrst report of asexual speciation in the Astigmata. We also hypothesize that thelytokous Schwiebea is losing its spermatheca. Once the spermatheca is lost, re-evolution of sexuality does not seem possible. Although we examined only a few species, the reconstructed molecular tree suggests that parthenogenesis evolved independently multiple times in the Schwiebea lineage. Our results also suggest that ancestrally thelytokous species never speciated into a sexual species. To conWrm this hypothesis, more species of this and related genera should be examined. Acknowledgments We thank Drs. Y. Kuwahara of Kyoto Gakuen University, N. Mori of Kyoto University, K. Tagami of Tsukuba University, and S. Shimano of Miyagi University of Education for donation of Schwiebea species. The mite collection technique was originally developed by Dr. Kuwahara. Two anonymous reviewers provided valuable comments that improved this manuscript.
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