Phylogeny of Feather Mite Subfamily Avenzoariinae ...

Molecular Phylogenetics and Evolution Vol. 20, No. 1, July, pp. 124 –135, 2001 doi:10.1006/mpev.2001.0948, available online at http://www.idealibrary.com on

Phylogeny of Feather Mite Subfamily Avenzoariinae (Acari: Analgoidea: Avenzoariidae) Inferred from Combined Analyses of Molecular and Morphological Data Jacek Dabert,* Miroslawa Dabert,† and Serge V. Mironov‡ *Department of Animal Morphology, A. Mickiewicz University, 28 Czerwca 1956/198, 61-485 Poznan, Poland; †Department of Biopolymer Biochemistry, Institute of Molecular Biology and Biotechnology, A. Mickiewicz University, Miedzychodzka 5, 60-371, Poznan, Poland; and ‡Zoological Institute, Russian Academy of Sciences, Universitetskaya emb. 1, 199-034 Saint-Petersburg, Russia Received August 7, 2000; revised January 16, 2001; published online May 2, 2001

Phylogenetic relationships among feather mites of the subfamily Avenzoariinae (Acari: Analgoidea: Avenzoariidae) were reconstructed by parsimony analysis of a combined data matrix. We analyzed 41 morphological characters and 246 molecular characters from a fragment of the 16S rDNA. Morphological trees were well supported at deep branches (genera and above), but showed much less support and resolution within genera. Molecular analyses produced trees with better resolution and support on terminal branches and worse support on basal branches. I MF index for the combined matrix pointed to the significant congruence of both data subsets with the whole of the data. The topology of the combined tree was close to the morphological tree in the deep branches and had wellresolved terminal branches as in the molecular tree. This suggests a considerable level of complimentarity between the two data sets. An analysis of association patterns of the mites and their hosts was conducted based on the results of the combined analyses for the Avenzoariinae and a phylogeny of their charadriiform hosts (compiled from various bird phylogeny hypotheses). The trees could be reconciled by the invoking of 12–13 cospeciation events, 6 –7 duplications, 2 host shifts, and 26 –29 sorting events. This suggests a high degree of cospeciation. © 2001 Academic Press Key Words: feather mites; Avenzoariinae; Charadriiformes; phylogeny; cospeciation; morphology; mtDNA; 16S rDNA; congruence tests.

INTRODUCTION Feather mites (Acari: Astigmata) are the most numerous and diverse group of ectoparasitic invertebrates associated with birds, with about 440 genera and over 2000 species described so far (Gaud and Atyeo, 1996). They live exclusively on the body surface, mostly on or in the feathers, but occasionally on or in the skin. Although some feather mites are true para1055-7903/01 $35.00 Copyright © 2001 by Academic Press All rights of reproduction in any form reserved.

sites, causing feather damages (e.g., Ascouracaridae) or skin lesions (e.g., some Epidermoptidae), most are commensals. Their entire life cycle takes place on the host body. Feather mites are good models for analyses of the evolution of host associations because of the clearly expressed relationships between certain feather mite taxa and their hosts. However, published studies on feather mites are largely limited to descriptive systematics and faunistic investigations. The first attempt to study relationships among feather mites was a phenetic analysis on the family Eustathiidae performed over 20 years ago (Moss et al., 1977). Phylogenetic studies using cladistic analyses are very recent (Dabert and Ehrnsberger, 1995, 1998; Dabert and Mironov, 1999; Mironov, 1991a,b, 1995; Mironov and Dabert, 1999). All of these analyses were based on external morphological characters only. Strong, but uniform, adaptive pressures due to environmental factors (airflow, incessant movement of feathers, uniform food source, and so on) is assumed to promote convergence in morphology among unrelated taxa living in the same particular microhabitat (e.g., vane surface, inside of the quill, down feathers) (Dabert and Mironov, 1999). As a result, morphological data for phylogenetic studies may contain high levels of homoplasy, resulting in unreliable results. Moreover, rapid speciation may result in a number of sibling species that are impossible to arrange phylogenetically on the base of morphology only. The subfamily Avenzoariinae is one example of a taxon in which within-group relationships and affinities with other subfamilies are hard to determine. The females share a rather uniform body plan, whereas the males show a range of morphotypes, especially with respect to the lobar region. Convergence in some of these variable male characteristics seems likely. Therefore, current understanding of the phylogeny of the subfamily is incomplete (Mironov, 1991a,b; Mironov and Dabert, 1999). Adequate resolution at the

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species level is especially elusive due to the mosaic-like distribution of morphological character states among species and the general lack of identifiable synapomorphies. For these reasons we have carried out a study at the molecular level. Mitochondrial DNA sequence data are assumed to be less sensitive to external selective pressure (Hedges and Sibley, 1994) and could allow improved reconstructions of phyletic relationships among avenzoariine feather mites. The 16S rDNA gene was chosen as a rapidly evolving marker which should provide adequate resolution at the species level. A combination of morphological and the newly developed molecular data is used to provide a more stable, and better supported, hypothesis of relationships for the Avenzoariinae. The family Avenzoariidae Oudemans, 1905 (Analgoidea) includes three subfamilies: the Avenzoariinae Oudemans, 1905 (11 genera, about 50 species); the Bonnetellinae Atyeo and Gaud, 1981 (8 genera, about 45 species); and the Pteronyssinae Oudemans, 1941 (18 genera, about 130 species). It represents one of the most ancient phylogenetic lines within the superfamily Analgoidea (Dabert and Mironov, 1999). All members of the family live on the flight feathers (Mironov, 1987). Host associations include a variety of bird orders, namely Charadriiformes, Procellariiformes, Pelecaniformes, Ciconiiformes, and Falconiformes. Notably, mites in the subfamily Avenzoariinae are associated exclusively with hosts in the order Charadriiformes, specifically in the suborders Charadrii, Lari, and Scolopaci. The first attempts to reconstruct the avenzoariine phylogeny at the generic level were made by Mironov (1991a,b, 1995). Although based on cladistic principles, these hand-generated reconstructions (Fig. 1A) may not represent the most parsimonious trees. An expanded and updated data matrix was reanalyzed with the PAUP software to find the most parsimonious tree (Mironov and Dabert, 1999). Relative to previous analyses, this analysis generated more details at the species level (Figs. 1B–1D). Monophyly of the subfamily Avenzoariinae is supported by (1) complete reduction of vertical setae vi, (2) reduction of ventral setae w and r on tarsi III, (3) well-developed opisthosomal lobes (occasional absence clearly involves secondary reduction), (4) well-developed and relatively enlarged cupules ia, im, and ip, (5) indented anal discs in the male, and (6) a tendency toward hypertrophy of legs IV in the male. Both hypotheses of relationships (Mironov, 1995; Dabert and Mironov, 1999) agree on the recognition of two distinct groupings within the subfamily, the Avenzoaria-like genera and the Bychovskiata-like genera (Figs. 1A and 1B). The only distinct difference between the two is in the structure of the adanal discs in males, with a multidentate corolla in Avenzoaria-like genera

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and a corolla with only two big opposite teeth in Bychovskiata-like genera. The plesiomorphic state of a smooth corolla is found in the remaining avenzoariids. The most variable and evolutionarily important characters in Avenzoariinae morphology are the structures of the genital apparatus and the male opisthosomal lobes. Well-developed triangular lobes, with an ovoid or triangular terminal cleft and a narrow and entire interlobar membrane, characterize the most primitive genera Attagivora and Laronyssus. They also lack modifications of the genital apparatus. The more evolved genera of the Avenzoaria group have enlarged interlobar membranes, separated terminal membranes with teeth, genital apodemes (absent in others), and fused epimeres I. In the Bychovskiata group the main tendency is toward shorter opisthosomal lobes. This probably appeared independently in several phyletic lines within the genus Bychovskiata. In contrast, the lobes are elongated in closely related genera Hemifreyana and Laronyssus. The most important disagreement between the two hypotheses concerns the position of the genus Bregetovia. According to the first hypothesis, Bregetovia is the sister taxon of the lineage (Pomeranzevia, (Avenzoaria, Pseudavenzoaria)). In the second hypothesis (Mironov and Dabert, 1999), this genus is the sistergroup of Pseudavenzoaria, within the broader lineage of (Pomeranzevia, (Avenzoaria, (Bregetovia, Pseudavenzoaria))). A second problem identified by Mironov and Dabert (1999) concerns the possible paraphyly of two genera: Avenzoaria contains the clade of Bregetovia– Pseudavenzoaria (Fig. 1C), whereas Bychovskiata includes Ovofreyana (Fig. 1D). MATERIALS AND METHODS Taxa and characters. The list of mite species, for which all morphological characters and nucleotide sequence data were collected, is presented in Table 1. A total of 32 mtDNA haplotypes from 26 mite species was analyzed. Among these, 28 unique sequences were analyzed phylogenetically. For sequence analysis ethanol-preserved samples were needed, and the sampling strategy was therefore significantly influenced by the availability of appropriate material. Representatives of two additional subfamilies of Avenzoariidae, Bonnetellinae (represented by Bonnetella fusca, Zachvatkinia larica, and Bdellorhynchus polymorphus) and Pteronyssinae (represented by Pteronyssoides striatus and Scutulanyssus obscurus), were chosen as close outgroups, while a species of Freyanoidea (Freyana anatina, Freyanidae) served as a distant outgroup. The morphological data set comprised 41 characters (Appendix). It includes data from Mironov and Dabert (1999) with supplementary character information for species not considered in the previous studies.

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FIG. 1. Previous hypotheses concerning phylogeny reconstruction of Avenzoariidae. (A) Mironov (1995); (B–D) Mironov and Dabert (1999).

Amplification and sequencing of mtDNA. Extraction of mite DNA was performed under conditions described in Dabert (1997). Amplification was accomplished with two primers, 16SA2 5⬘-TTTAATTGGTTACTTGTATGAATG-3⬘ (developed for feather mites) and 16C2 5⬘-CGCTGTTATCCCTAGAGTAT-3⬘ (based on Black and Piesman [1994], modified), and yielded a

product of about 200 bp. Amplified DNA was used as a template for direct cycle sequencing with the fmol Sequencing System (Promega Corp., Madison, WI). The original PCR primers were also used for sequencing. Sequences were read manually from autoradiographs. The alignment of the sequence data (GenBank PopSet 10518433) was prepared with Clustal X 1.64b


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TABLE 1 Feather Mites Used in the Present Study Mite species

Host species

1. Freyana anatina Freyaninae, Freyanidae, Freyanoidea 2. Pteronyssoides striatus Pteronyssinae, Avenzoariidae, Analgoidea 3. Scutulanyssus obscurus Pteronyssinae, Avenzoariidae, Analgoidea 4. Bdellorhynchus polymorphus Bonnetellinae, Avenzoariidae, Analgoidea 5. Bonnetella fusca Bonnetellinae, Avenzoariidae, Analgoidea 6. Zachvatkinia larica Bonnetellinae, Avenzoariidae, Analgoidea 7. Ovofreyana kurbanovae Avenzoariinae, Avenzoariidae, Analgoidea 8. Bychovskiata subcharadrii Avenzoariinae, Avenzoariidae, Analgoidea 9. Bychovskiata squatarolae Avenzoariinae, Avenzoariidae, Analgoidea 10. Bychovskiata intermedia Avenzoariinae, Avenzoariidae, Analgoidea 11. Bychovskiata dubia Avenzoariinae, Avenzoariidae, Analgoidea 12. Bychovskiata charadrii Avenzoariinae, Avenzoariidae, Analgoidea 13. Bychovskiata semipalmati Avenzoariinae, Avenzoariidae, Analgoidea 14. Bychovskiata hypoleuci Avenzoariinae, Avenzoariidae, Analgoidea 15. Pomeranzevia ninnii Avenzoariinae, Avenzoariidae, Analgoidea 16. Pseudavenzoaria indica Avenzoariinae, Avenzoariidae, Analgoidea 17. Pseudavenzoaria ochropodis Avenzoariinae, Avenzoariidae, Analgoidea 18. Bregetovia mucronata Avenzoariinae, Avenzoariidae, Analgoidea 19. Bregetovia limosae Avenzoariinae, Avenzoariidae, Analgoidea 20. Bregetovia obtusolobata Avenzoariinae, Avenzoariidae, Analgoidea 21. Avenzoaria totani 2-1 Avenzoariinae, Avenzoariidae, Analgoidea 22. Avenzoaria totani 2-2 Avenzoariinae, Avenzoariidae, Analgoidea 23. Avenzoaria totani 1-1 Avenzoariinae, Avenzoariidae, Analgoidea 24. Avenzoaria totani 1-2 Avenzoariinae, Avenzoariidae, Analgoidea 25. Avenzoaria tringae Avenzoariinae, Avenzoariidae, Analgoidea 26. Avenzoaria calidridis 2 Avenzoariinae, Avenzoariidae, Analgoidea 27. Avenzoaria calidridis 1-1 Avenzoariinae, Avenzoariidae, Analgoidea 28. Avenzoaria calidridis 1-2 Avenzoariinae, Avenzoariidae, Analgoidea 29. Avenzoaria calidridis 1-3 Avenzoariinae, Avenzoariidae, Analgoidea 30. Avenzoaria terekiae Avenzoariinae, Avenzoariidae, Analgoidea 31. Avenzoaria philomachi Avenzoariinae, Avenzoariidae, Analgoidea 32. Avenzoaria phalaropi Avenzoariinae, Avenzoariidae, Analgoidea

Anas platyrhynchos Anatidae, Anseriformes Fringilla coelebs Fringillidae, Passeriformes Delichon urbica Hirundinidae, Passeriformes Aythya fuligula Anatidae, Anseriformes Pandion haliaetus Accipitridae, Falconiformes Larus fuscus Laridae, Charadriiformes Vanellus leucurus Charadriidae, Charadriiformes Himantopus himantopus Recurvirostridae, Charadriiformes Pluvialis squatarola Charadriidae, Charadriiformes Charadrius leschenaulti Charadriidae, Charadriiformes Charadrius dubius Charadriidae, Charadriiformes Charadrius hiaticula Charadriidae, Charadriiformes Charadrius semipalmatus Charadriidae, Charadriiformes Actitis hypoleucos Scolopacidae, Charadriiformes Numenius arquata Scolopacidae, Charadriiformes Tringa solitaria Scolopacidae, Charadriiformes Tringa ochropus Scolopacidae, Charadriiformes Tringa erythropus Scolopacidae, Charadriiformes Limosa limosa Scolopacidae, Charadriiformes Tringa nebularia Scolopacidae, Charadriiformes Tringa totanus Scolopacidae, Charadriiformes Tringa totanus Scolopacidae, Charadriiformes Tringa glareola Scolopacidae, Charadriiformes Tringa glareola Scolopacidae, Charadriiformes Tringa nebularia Scolopacidae, Charadriiformes Calidris alpina Scolopacidae, Charadriiformes Calidris ferruginea Scolopacidae, Charadriiformes Calidris minuta Scolopacidae, Charadriiformes Calidris temminckii Scolopacidae, Charadriiformes Xenus cinereus Scolopacidae, Charadriiformes Philomachus pugnax Scolopacidae, Charadriiformes Phalaropus lobatus Scolopacidae, Charadriiformes

Note. Numbers after the specific name designate different haplotypes.

Sample source

GenBank Accession No.

Slonsk, Poland, 1996

AF005071

Kaliningrad, Russia, 1990

AF286438

Slonsk, Poland, 1996

AF286439

Kazakhstan, Russia, 1986

AF286423


AF286424


AF286440

Usbekistan, Russia, 1988

AF286435


AF286434


AF286433


AF286431


AF286429


AF286428

Michigan, USA, 1982

AF286432

Kirghiz, Russia, 1990

AF286430


AF005072

Santiago, Chile, 1988

AF286436


AF286437


AF286426


AF286425


AF286427

Mechelniki, Poland, 1996

AF286420


AF286444


AF286419


AF286443


AF286422


AF286416


AF286415


AF286442


AF286441


AF286421


AF286418


AF286417

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(Thompson et al., 1997). After alignment the number of characters was 246. Conserved motifs were used to improve and adjust the alignment by eye. Phylogenetic analysis. Parsimony analysis (branchand-bound option) was performed with PAUP 3.0s (Swofford, 1991b). This method was preferred over distancebased approaches because of better performance for short nucleotide sequences (Hillis et al., 1994) and because it enabled evaluation of the influence of different subsets of characters on the obtained phylogeny (Avise, 1994; Sites et al., 1996). All aligned positions were treated as unordered fivestate characters (four nucleotides and gap). Morphological and sequence data were analyzed both separately and combined. In the molecular analyses we tested different weighting schemes for transitions and transversions. All morphological characters were weighted equally. In combined analyses morphological characters were primarily weighted 1 and then 5 times as much as nucleotides, inversely reflecting their proportion in terms of number of informative characters. Such method of assigning differential weights is often applied in parsimony studies of combined data (Miyamoto, 1985; Hillis et al., 1994), although not all agree with this approach (e.g., Wenzel and Siddal, 1999). Phylogenetic signal was evaluated by the g1 test for skewness (Hillis, 1991; Hillis and Huelsenbeck, 1992) with the random trees option of PAUP. When multiple equally parsimonious trees were found, the strict and/or 50% majority-rule consensus tree was applied. Support for the internal branches of trees was estimated by decay/support indices (Bremer, 1988) calculated with AutoDecay 4.0 software (Eriksson, 1998). The Templeton test (Larson, 1994) was used to test the statistical significance of morphological and sequence data sets fit to the alternate tree topologies. The incongruence Miyamoto index I M for separate morphological and sequence data was calculated (Swofford, 1991a). For combined data we calculated the I MF index (Swofford, 1991a), which was statistically tested with the Xarn software (Farris, 1996) with 10,000 repetitions. The reconciliation method of Page (1990), as applied in TreeMap 1.0 (Page, 1995), was used to test the null hypothesis of host–parasite cospeciation. The significance of cospeciation evidence was examined by a randomization test under a proportional-to-distinguishable model (10,000 random trees). Choice of a proper bird phylogeny for comparison with the feather mite phylogeny turned out to be a serious problem. The published phylogenies are not detailed enough and are sometimes highly incongruent. So far, the work of Sibley and Ahlquist (1990) is the most comprehensive attempt at phylogeny reconstruction for birds. Generally, their hypotheses provide a good match with our results for feather mites phylogenies (Dabert and

Ehrnsberger, 1995, 1998; Dabert and Mironov, 1999; Mironov, 1998; Mironov and Dabert, 1999). For charadriiform birds we also tested a more detailed phylogeny reconstruction, prepared by Chu (1995). His reconstruction, based on a reanalysis of osteological data of Strauch (1978), is the most comprehensive and detailed cladistic analysis of Charadriiformes phylogeny so far. Although it includes all the relevant host taxa, the resolution of the consensus trees is too weak for the reconciliation method (both host and parasite trees must be fully resolved). Reducing the host data matrix to those taxa associated with feather mite taxa did not improve resolution or branch support. This is not unexpected given that Chu used a combination of a relatively small number of informative characters and a large taxon set. We adjusted this charadriiform phylogeny by considering results from phylogenetic analyses of subgroups made by Mickevich and Parenti (1980) and Christian et al. (1992) and broader analyses of shore bird systematics by Sibley and Monroe (1990) and Hayman et al. (1991). The charadriiform tree shown here is thus a compilation of various hypotheses and is a provisional reconstruction only. Therefore, the results of the comparison of bird–mite phylogenies should be treated cautiously. Preparation and editing of the data matrices was done with the NEXUS Data Editor 0.4.5 (Page, 1999). Drawing and editing of the trees was done with TreeView 1.5.2 (Page, 1996, 1998). Reconciled trees were drawn with TreeMap and were modified in Microsoft Word 97. RESULTS Phylogenetic signal. Both morphological and sequence data sets contained statistically significant phylogenetic structure and were significantly more leftward skewed than the distribution from random data matrices (g 1 ⫽ ⫺0.682 and ⫺0.456, respectively, both P ⬍ 0.01). Also, the combined data matrix had a significant phylogenetic signal (g 1 ⫽ ⫺0.641, P ⬍ 0.01). Morphological analysis. Parsimony analysis of 41 morphological characters produced nine equally most parsimonious trees: length ⫽ 326, CI ⫽ 0.877, RI ⫽ 0.948. The 50% majority-rule consensus tree, with decay indices, is presented in Fig. 2. The strict consensus tree is very similar to the majority-rule tree, with the exception of the fully polytomous Avenzoaria genus. This tree is characterized by relatively well-supported and stable deep branches, i.e., genera and below (mean decay index d ⫽ 12.3), and weaker resolution and support for terminal branches, i.e., within genera (mean d ⫽ 5.3), especially in Avenzoaria and partly in Bychovskiata. The status of the genus Pseudavenzoaria is unclear. In three of the equally most parsimonious


FIG. 2. Morphological (left) and sequence (right) data. Morphological 50% majority-rule consensus tree of nine most parsimonious trees: 41 characters, length ⫽ 326, CI ⫽ 0.877, RI ⫽ 0.948. Sequence 50% majority-rule consensus tree of eight most parsimonious trees: 246 bp, length ⫽ 500, CI ⫽ 0.458, RI ⫽ 0.512. Numbers below branches designate decay indices.

trees it is a monophyletic sister genus to Bregetovia: ((Ps. ochropodis, Ps. indica), Bregetovia ssp.). In other trees it is a paraphyletic: ((Bregetovia ssp., Ps. indica), Ps. ochropodis) or ((Bregetovia ssp., Ps. ochropodis), Ps. indica). mtDNA analysis. Parsimony analysis of all 246 molecular characters produced eight equally most parsimonious trees: length ⫽ 500, CI ⫽ 0.458, RI ⫽ 0.512. Different weighting procedures did not substantially alter the tree topology. The 50% majority-rule consensus tree is depicted with decay indices in Fig. 2. The strict consensus tree differs from the majority-rule tree in unresolved relationships between Avenzoaria philomachi-terekiae and Pseudavenzoaria indica-ochropodis only. The consensus indices, although much lower than those for the morphological analysis, are not worse than the critical value 0.451 for 28 taxa (Sanderson and Donoghue, 1989). In contrast to the morphological tree, this tree has better resolution and better support in the terminal branches (mean d ⫽ 8.5, P ⬎ 0.05). Yet generally it is worse supported, especially on deep branches (mean d ⫽ 3.1, P ⬍ 0.003). The arrangement of the lineages Avenzoaria–Pomeranzevia, Bregetovia– Pseudavenzoaria, and Bychovskiata–Ovofreyana is not

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stable; half of the most parsimonious trees support the subtree (Avenzoaria group, (Bregetovia group, Bychovskiata group)) and the other half suggest (Bregetovia group, (Avenzoaria group, Bychovskiata group)). Pseudavenzoaria is a paraphyletic taxon in all trees, usually with Ps. indica as the most basal species. Molecular analysis also showed some differences in sequences originating from representatives of single mite species from different hosts. It concerns Avenzoaria totani and A. calidridis. The first species was collected from the Wood Sandpiper Tringa glareola and the Redshank T. totanus. Sequences of mites from both hosts differ in 10 –11 substitutions (4 –5 transitions, 3 transversions, 3 insertions/deletions). Individuals from the same host species collected in Poland and east Russia were identical (T. totanus) or differed in only 1 substitution (T. glareola). A similar situation was observed in A. calidridis. Sequences of A. calidridis from the Curlew Sandpiper C. ferruginea, the Little Stint C. minuta, and the Temminck’s Stint C. temminckii are identical, but they differ in 9 nucleotide positions (6 transitions, 1 transversion, 2 insertions/deletions) from A. calidridis from the Dunlin Calidris alpina. The maximum-likelihood distances counted for these sequences (uniform rate of heterogeneity, HKY substitution model) are 0.035 for A. totani and 0.044 for A. calidridis. Surprisingly, these morphologically indistinguishable variants show levels of intraspecific genetic differentiation that are similar to those found between closely related species such as Bychovskiata dubia and B. hypoleuci (10 different nucleotide positions, distance ⫽ 0.031). This level of genetic differentiation is similar to that found among other closely related mite taxa, e.g., in ticks (Dabert et al., 1999). Notably, differentiation levels for some morphologically distinct species, e.g., Bregetovia obtusolobata and B. limosae, are much lower (5 different nucleotide positions, distance ⫽ 0.009). Combined analysis. Parsimony analysis of the combined matrix (246 molecular characters ⫹ 41 morphological characters, all characters weighted 1) produced 19 equally most parsimonious trees with consensus completely consistent with the results of the molecular analysis alone. This indicates that a huge number of molecular characters dominated the fewer morphological characters. The subsequent analysis with morphological characters weighted 5 times higher than molecular characters produced two equally most parsimonious trees: length ⫽ 852, CI ⫽ 0.609, RI ⫽ 0.753. The 50% majority-rule consensus tree (same as the strict consensus tree) with decay indices is shown in Fig. 3. This tree is better resolved and supported than either the molecular or the morphological consensus trees. In its deep branches it has much better support (mean d ⫽ 14.0, P ⫽ 0.02) than the molecular tree and slightly better (not significantly, P ⬎ 0.05)

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FIG. 3. Combined data. 50% majority-rule consensus tree of two most parsimonious trees: 246 bp ⫹ 41 morphological characters, morphological characters weighted 5 times that of molecular characters, length ⫽ 848, CI ⫽ 0.607, RI ⫽ 0.750.

support than the morphological tree. In its terminal branches it has support similar to that of the sequence tree (mean d ⫽ 8.6) but better resolution and support (not significantly, P ⬎ 0.05) than the morphological tree. The topology of the combined tree resembled the morphological tree in its deep branches and the molecular tree in the good resolution of the terminal branches. Incongruences. The I M index for consensus morphology and sequences trees was 0.162. The topologies of molecular and morphological trees differed significantly. Based on Templeton’s test both data sets showed significant differences in their fit to the alternate tree topologies (P ⬍ 0.01 for both comparisons). Cross comparisons constraining one data set to the optimal topology for the other data set all produced the same results (P ⬍ 0.01). The I MF value of 0.066 is relatively low and shows significant congruence (P ⫽ 0.273 in Xarn) of both data subsets with the whole of the data. Extent of host–parasite cospeciation. The reconciliation analysis was done with two restrictions. First,

the well-documented shift of the ancestor of Bychovskiata hypoleuci from plover genus Charadrius to scolopacid Common Sandpiper Actitis hypoleucos (Dabert, 1992; Mironov and Dabert, 1999). Second, the Bregetovia limosae shift to godwits Limosa ssp. This genus has apparently originated on larger tattlers of the genus Tringa and from here colonized godwits. Doing so, it has partially squeezed out the native avenzoariine fauna, i.e., Avenzoaria punctata (Mironov and Dabert, 1999). The reconciled tree of all mites, Avenzoariinae plus outgroups (combined tree 1) with that of the hosts (Sibley and Ahlquist, 1990, with modifications) indicate 16 cospeciation events, 9 duplications, 2 host shifts (as constrained), and 38 –39 sorting events. The reconciliation made for combined tree 2 gave the same results. These values suggest cospeciation as a significant (P ⬍ 0.001) factor in the evolution of these mite– bird associations. Figure 4 depicts the reconciled tree prepared for the Avenzoariinae (combined tree 1) and their charadriiform hosts (compiled tree). This reconstruction required 13 cospeciation events, 6 duplications, 2 host shifts (as constrained), and 26 sorting events. The use of alternate hypotheses of bird phylogeny, e.g., Mickevich and Parenti (1980) or Christian et al. (1992), did not alter these results. Comparison with the Chu (1995) reconstruction reduced the number of cospeciation events (to 12) while increasing the number of noncoevolutionary events (7 duplications, 29 sorting events). Reconciliation with combined tree 2 gave identical results. The level of 13 cospeciation events shows a very high and statistically significant (P ⫽ 0.001) degree of mite– bird cospeciation. It should be noted that the most ambiguous set of relationships in the host trees, involving relationships among Phalaropus, Limosa, Xenus, and Actitis, had no influence on the statistical significance of the cospeciation test, because of host shifts involving Limosa and Actitis. DISCUSSION Comparison of recent results with previous hypotheses. The results obtained from the combined analysis of molecular and morphological data are almost completely consistent with the hypothesis of Mironov and Dabert (1999). The most striking difference concerns the status of the genus Avenzoaria. According to previous hypothesis this genus is paraphyletic (Fig. 1C). None of the current set of analyses support those hypotheses and Avenzoaria is always a monophyletic group (Figs. 2–3). However, the position of the cluster Bregetovia–Pseudavenzoaria within the Avenzoariinae is ambiguous. Combined and morphological analyses place this grouping as sister group of Avenzoaria. In trees obtained from molecular data its position was different: either it was a sister clade to the Bychovski-


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FIG. 4. Reconciled trees of shore birds (gray tree) and avenzoariin feather mites (black tree). Black circles, cospeciations; black squares, duplications; short dashes, sorting events (extinction, “missing the boat”); arrows, host switches; B, bird taxa; M, mite taxa.

ata–Ovofreyana cluster or sister group to a lineage including all remaining Avenzoariinae. The differences in the sequence composition between Avenzoaria and Bregetovia–Pseudavenzoaria were very pronounced and various experiments with alternate alignments have never succeeded in joining these mites in a monophyletic group. The nature of these differences (case of rate differentiation, species evolution vs gene evolution, unidentified morphological convergencies) should be cleared up by further investigations using various molecular markers. Both Mironov and Dabert (1999) and present studies rejected the separation of the genus Bregetovia from the Pseudavenzoaria–Avenzoaria clade, as initially postulated by Mironov (1991a, (1995). The clade Bregetovia–Pseudavenzoaria is well defined by 11 molecu-

lar and 5 morphological synapomorphies and exemplifies one of the best-supported clusters in all analyses. However, the taxonomic status of the genus Pseudavenzoaria remains unclear. According to Mironov and Dabert (1999) and traditional systematics it is a genus. This status was not confirmed in the present study. We have studied a long series of material and reanalyzed the synapomorphies used in former cladistic phylogeny reconstruction for defining the genus Pseudavenzoaria. It led us to the conclusion that the main synapomorphy—the structure of terminal membranes in males—was misinterpreted. In fact the terminal membranes in Pseudavenzoaria are either similar to those of Avenzoaria (Ps. ochropodis) or to those of Pomeranzevia (Ps. indica). The second synapomorphy, the straightened opisthosomal lobes, was

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weak and variable. Both present analyses, morphological and molecular, place these two species as paraphyletic basal species in the genus Bregetovia. The present study has not given an unambiguous resolution concerning the taxonomic status of the genus Ovofreyana. Morphological and combined analyses support the placement of this taxon within the genus Bychovskiata, but Ovofreyana is the sister genus to Bychovskiata in all most parsimonious trees based on sequence data. Sequence analysis distinguishes some haplotypes in morphologically undistinguishable species. We suppose that in the case of A. calidridis and A. totani we are dealing with species in statu nascendi. Separation of the populations on different hosts has already led to genetic, but not yet to morphological differentiation. Is there a difference between morphological and molecular trees? Combined phylogenetic analyses, which incorporate various data sources, attract attention (Baum, 1992; Rodrigo, 1993; Chippindale and Wiens, 1994; Bull et al., 1993; Wiens, 1998). Recently there have been many studies using combined (morphology– sequences, sequences–sequences) analyses to infer the phylogeny reconstructions of different groups of organisms (e.g., Flook et al., 1999; Graham et al., 1998; Hedges and Sibley, 1994; Liu and Miyamoto, 1999; Miyamoto, 1996; Normak and Lanteri, 1998; Poe, 1996; Quicke and Belshaw, 1999; Sites et al., 1996). The results recovered from molecular data sets are sometimes incongruent with those from morphological data sets. The reasons for these incongruencies are variously explained as, for example, convergencies among morphological characters (Quicke and Belshaw, 1999; Hedges and Sibley, 1994) or molecular characters (Reeder and Wiens, 1996), low phylogenetic signal in the morphological data (Graham et al., 1998), ancient introgression of DNA (Manos et al., 1999), long-branch attraction in molecular data (Tang et al., 1999), or hybrid origin of parthenogenetic taxa (Normak and Lanteri, 1998). The incongruencies are common also among molecular data sets (Harrington and Maijala, 1998; Chippindale et al., 1999). A good review of this problem is given by Quicke and Belshaw (1999). Nevertheless, when different data matrices are analyzed together they may complement and reinforce one another, giving better supported phylogenetic hypotheses than separate analyses (Crespi et al., 1998; Dubuisson et al., 1998; Remsen and DeSalle, 1998; Littlewood et al., 1999; Klompen et al., 2000; Wiegmann et al., 2000). In the case of Avenzoariinae the differences between the trees obtained from molecular and morphological data sets are the result of different resolutions of data. Sequence analysis performs well for intrageneric and lower relationships. However, deep branches are

poorly resolved or supported. The inverse situation prevails in the morphological analyses. They provide generally good resolution and support for the basal nodes, but are weak at resolving lower level relationships. Despite distinct differences in tree topology the results of the two analyses are not totally incongruent. After all, polytomies are not incongruent with wellresolved trees; they simply show lack of resolution. The combination of both data sets resulted in high resolution throughout the tree. The results of the combined total evidence analysis are thus better than those for each of the separate analyses, combining the stability of the morphological trees with the good low-level resolution of the molecular trees. Cospeciation. Every kind of study comparing host and parasite phylogenies needs as prerequisite wellcorroborated hypotheses of relationships for each of the coexisting organisms. Relying upon our present and previous analyses, we believe that the current phylogeny reconstruction of Avenzoariinae is close to the natural phylogeny. Unfortunately, we are less confident about the bird host tree. Moreover, more detailed coevolutionary studies, e.g., comparing the evolutionary rates of host and parasite organisms, can be accomplished only by sequence analysis of both parasites and hosts with a single molecular marker (Page et al., 1998). We would like to address this question in future studies. Despite these reservations, the present analysis of combined morphological and molecular data has confirmed our previous hypotheses about close cospeciation of Avenzoariinae with their hosts. The division of Avenzoariinae into two big branches mirrors the division of the Charadriiformes into two parvorders— Charadriida and Scolopacida (sensu Sibley and Ahlquist, 1990)- and supports the paraphylly of waders (Charadrii ⫹ Scolopaci) as postulated by some recent authors (Strauch, 1978; Sibley and Ahlquist, 1990; Chu, 1995). The evolutionary parallelism is better expressed between the suborder Charadrii and the Bychovskiata-like group clades than between the Scolopaci and the Avenzoaria-like group. It indicates a relatively more recent origin of host–parasite associations in Charadrii than in Scolopaci and an earlier origin of Scolopaci than Charadrii. An alternative explanation may be found in the greater morphological, biological, and behavioral diversity of Charadrii, compared to the relatively uniform waders of the Scolopaci, hence the possibility of greater errors in phylogeny reconstruction of Scolopaci than of Charadrii. It may also lead to higher levels of host switching, which is more probable between hosts of similar habits and similar niches (Scolopaci) than switches between more differentiated Charadrii.

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APPENDIX Character Species

11111111112222222222233333333344 12345678901234567890123456789012345678901

Avenzoaria calidridis 1-1 Avenzoaria calidridis 2 Avenzoaria phalaropi Avenzoaria philomachi Avenzoaria totani 1-1 Avenzoaria totani 2-1 Avenzoaria terekiae Avenzoaria tringae Bdellorhynchus polymorphus Bonnetella fusca Bregetovia limosae Bregetovia mucronata Bregetovia obtusolobata Bychovskiata charadrii Bychovskiata dubia Bychovskiata hypoleuci Bychovskiata intermedia Bychovskiata semipalmati Bychovskiata squatarolae Bychovskiata subcharadrii Freyana anatina Ovofreyana kurbanovae Pomeranzevia ninnii Pseudavenzoaria indica Pseudavenzoaria ochropodis Pteronyssoides striatus Scutulanyssus obscurus Zachvatkinia larica

11100100000121111100211100000001000000000 11100100000121111100211100000001000000000 11100100000121111100211100000001000000000 11100100000121111100211100000001000000000 11100100000121111100211200000002000000000 11100100000121111100211200000002000000000 11100100000121111100211100000001000000000 11100100000121111100211200000002000000000 11100111101100000000100n00000000000000100 11100111122210000000100n00000000000000100 11100100000121111100310411121110000100100 11100100000121111100310411121000000100100 11100100000121111100310411121110000100100 11100100000121111011100n00000000001111111 11100100000121111011100n00000000001111101 11100100000121111011100n00000000001111111 11100100000121111011100n00000000001100001 11100100000121111011100n00000000002111111 11100100000121111011100n00000000000000001 11100100000121111010100n00000000000000000 00000000000000000001010000000000100000200 11100100010121111011100n00000000113000000 11100100000121111100100n00000000000000000 11100100000121111100112511110000000000100 11100100000121111100210311110000000000100 11111000200110000000100n00000000000000000 11111000200110000000100n00000000000000000 11100111122200000000100n00000000000000100

1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16. 17. 18. 19. 20. 21. 22. 23. 24. 25. 26. 27. 28. 29. 30.

Condylophore guide. 0 —absent; 1—present. Setae s of tarsus IV. 0 —present; 1—absent. Form of condylophores. 0 —short; 1—long, zigzag-like, flexible. Lacunae in lateral sclerites. 0 —absent; 1—present. Ventral membrane of tarsus I. 0 —absent; 1—present. Lateral sclerite margins. 0 — clear; 1—thin. Setae s of tarsus III in male. 0 —setiform; 0 —lanceolate. Tarsus IV in male. 0 —simple; 1—short, cone-like. Position of setae cp and c3. 0 —c3 anterior to cp; 1—approximately at the same level; 2—c3 posterior to cp. Adanal shields. 0 —absent; 1— one pair of big sclerites; 2— complex sclerites. Hysteronotal shield in female. 0 — entire; 1—reduced laterally; 2—pygidial part separated, central part with deep incision or also separated into two pairs; 3— completely absent; 4 —pygidial shield separated, central fragment not incised or separated. Interlobar membrane in male. 0 —absent; 1—present mainly on internal margins of lobes; 2— occupies almost whole terminal cleft. Vertical setae vi. 0 —two setae; 1— one seta; 2—setae absent. Setae of tarsus III. 0 —tree ventral setae; 1— one ventral seta. Cupules ia, im, ih, ip. 0 —indistinct; 1—well developed. Genital setae in male. 0 —short, adjacent bases; 1—rather large, distant from one another. Anal discs. 0 —flat, disc-like; 1— cup-like or cylindrical. Indentation of corolla. 0 —smooth; 1—multidentate. Pair of budges in corolla. 0 — budges absent; 1—two opposite budges in corolla. Position of cupules ia to setae c2. 0 — cupules lateral to setae c2; 1— cupules medial. Terminal membranes in male. 0 —absent; 1—present, without teeth; 2—with teeth heterogenous in form and size (acute and rounded); 3— bimodal margin: without teeth in homomorphs, with acute apex in heteromorphs; 4 —acute teeth equal in size and form. Opisthosomal (pygidial) shield in tritonymph. 0 —absent; 1—present. Number of acute teeth in terminal membrane with heterogenous teeth. 0 —absent; 1—two acute teeth; 2—four to five teeth. Form of opisthosomal shield(s) in tritonymph. 0 —well developed, covers almost whole hysteronotum; 1—short stick-like; 2—short triangular; 3—long triangular; 4 —fused into single shield with acute anterior end; 5—with ovoid anterior end. Genital acetabules. 0 — out of genital apodemes; 1— on genital apodemes. Sclerotized terminal margin (lamella) in female. 0 —absent; 1—present. Prodorsal shield in tritonymph. 0 —without posterior extension; 1—with posterior extension. Terminal membrane in tritonyphes. 0 —absent; 1—rounded; 2—with acute medial angle. Processus of femur II in heteromorphic males. 0 —absent; 1—present. Striation in prodorsal shield in male. 0 —absent; 1—present.

134 31. 32. 33. 34. 35. 36. 37. 38. 39. 40. 41.

DABERT, DABERT, AND MIRONOV Dimorphis of opisthosoma in males. 0 —absent; 1—present. Terminal cleft in tritonymph. 0 —absent; 1—small, semicircular; 2—as big wide U; 3—as narrow long U. Lateral membranes of hysterosoma. 0 —absent; 1—present. Anterior tip of epimerites III. 0 —stick-like; 1—T-shaped. Internal spermaduct. 0 — cylindrical; 1—asymmetrical; 2—narrow tube; 3—funnel-like. Sclerotized margin between setae h3 in female. 0 —absent; 1—present. Lateral rounded extension on hysteronotal shield. 0 —absent; 1—present. Humeral shields in tritonymph. 0 —absent; 1—present. Setae 4a. 0 —4a posterior to genital apparatus; 1—at level of genital apparatus; 2—4a anterior to genital apparatus. Posterior processus of humeral shield in tritonymph. 0 —absent; 1—present. Position of setae h2, h3 in females. 0 — out of hysteronotal shield; 1— on posterior margin of hysteronotal shield.

ACKNOWLEDGMENTS We thank Hans Klompen, Ohio State University for critical reading of the manuscript and helpful comments. This work was supported by Grant 6 P204 029 06 of the State Committee for Scientific Research, Poland.

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