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Type: Article
Published: 2019-05-10
Page range: 401–440
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Systematics of reptile-associated scale mites of the genus Pterygosoma (Acariformes: Pterygosomatidae) derived from external morphology

Department of Molecular Biology, Genetics & Immunology, Faculty of Biology & Environmental Sciences, Cardinal Stefan Wyszyński University, Wóycickiego 1/3, 01-938 Warsaw, Poland. Department of Animal Morphology, Adam Mickiewicz University, Faculty of Biology, Umultowska 89, 61-614 Poznan, Poland
Acari phylogeny evolution ectoparasites lizards Pterygosomatidae cospeciation

Abstract

The phylogeny of the mite genus Pterygosoma Peters, 1849 (Acariformes: Pterygosomatidae), permanent parasites of lizards of the families Agamidae, Gerrhosauridae and Liolaemidae (Reptilia: Squamata), was inferred with maximum parsimony, successive weighting and implied weighting approaches based on 182 characters of 48 ingroup and 12 outgroup species. All undertaken analyses questioned the monophyly of the genus. Based on this research, Pterygosoma includes 56 mite species associated with agamas from Africa and Asia (Sauria: Agamidae). Within the genus seven natural species groups were found: mutabilis, inermis, melanum, caucasica, fimbriata, singularis and foliosetis; 13 species of the genus were not assigned to any of the groups due to their unique morphological characters. For the ligare group of the subgenus Pterygosoma s. str. (7 species) associated with the South American tree lizards from the family Liolaemidae, a new genus, Neopterygosoma gen. nov., is established. The subgenus Gerrhosaurobia Lawrence, 1959 (3 species) associated with the African plated lizards of the family Gerrhosauridae is elevated to the genus rank. Diagnoses for the three genera are presented. Historical associations are reconstructed by fitting the obtained mite tree into the host topology on the family level. Results of coevolutionary analysis highlight the coincidence of both trees. The studies suggest that the ancestor of the genus Pterygosoma switched from the hosts of Gerrhosaurobia i.e. from the plated lizards (Gerrhosauridae) to the agamas (Agamidae), and the genus Pterygosoma has its biogeographic origin in North Africa, and colonized Asia via the Arabian Peninsula, which is congruent with the historical biogeography of its hosts.

References

  1. Baker, A.S. (2017) A redescription of Pterygosoma aegyptiaca Mostafa (Acari: Prostigmata: Pterygosomatidae), a little known ectoparasitic mite of spiny-tailed lizards (Squamata: Agamidae), with new morphological data for the Pterygosomatidae. Systematic & Applied Acarology, 22, 1970–1988.

    Bates, M.F., Tolley, K.A., Edwards, S., Davids, Z., Da Silva, M.J. & Branch, W.R. (2013) A molecular phylogeny of the African plated lizards, genus Gerrhosaurus Wiegmann, 1828 (Squamata: Gerrhosauridae), with the description of two new genera. Zootaxa, 3750, 465–493.

    Bertrand, M. (2002) Morphologic adaptations to parasitism on reptiles: Pterygosomatidae (Prostigmata: Raphignathina). In: Bernini, F., Nannelli, R., Nuzzaci, G. & de Lillo, E. (Eds.), Acarid Phylogeny and Evolution. Adaptations in mites and ticks. Kluwer Academic Publishers, Dordrecht, pp. 233–240.

    Bertrand, M. & Pedrono, M. (1999) Euryxeny and stenoxeny of the genus Geckobia Mégnin (Actinedida: Pterygosomatidae): Geckobia enigmatica n. sp collected from the Madagascan tortoise (Geochelone yniphora). Acarologia, 40, 147–153.

    Bertrand, M., Paperna, I. & Finkelman, S. (2000) Pterygosomatidae: descriptions et observations sur les genres Pterygosoma, Geckobia, Zonurobia et Hirstiella (Acari: Actinedida). Acarologia, 40, 275–304.

    Blankers, T., Townsend, T.M., Pepe, K., Reeder, T.W. & Wiens, J.J. (2013) Contrasting global-scale evolutionary radiations: phylogeny, diversification, and morphological evolution in the major clades of iguanian lizards. Biological Journal of the Linnean Society, 108, 127–143.

    Bochkov, A.V., Klimov, P.B. & Wauthy, G. (2011) Phylogeny and coevolutionary associations of makialgine mites (Acari, Psoroptidae, Makialginae) provide insight into evolutionary history of their hosts, strepsirrhine primates. The Journal of Linnean Zoology, 162, 1–14.

    Bochkov, A.V., Melnikov, D.A. & Nazarov, R.A. (2009) Pterygosoma (Pterygosoma) pseudotrapelus sp. nov. (Acariformes: Pterygosomatidae)—ectoparasite of Pseudotrapelus sinaitus (Squamata: Agamidae) from Jordan, Zootaxa, 2232, 61–68.

    Bochkov, A.V. & Mironov, S.V. (2000) Two new species of the genus Geckobia (Acari: Pterygosomatidae) from geckons (Lacertilia: Gekkonomorpha) with a brief review of host-parasite associations of the genus. Russian Journal of Herpetology, 7, 61–68.

    Bochkov, A.V. & O’Connor, B.M. (2006) [A review of the external morphology of the mite family Pterygosomatidae and its systematic position within the Prostigmata (Acari: Acariformes)]. Parazitologiya, 40, 201–214. [in Russian]

    Bochkov, A.V., O’Connor, B.M. & Wauthy, G. (2008) Phylogenetic position of the family Myobiidae within the Prostigmata (Acari: Acariformes). Zoologischer Anzeiger, 247, 15–45.

    Brooks, D.R. (1990) Parsimony analysis in historical biogeography and coevolution: Methodological and theoretical update. Systematic Zoology, 39, 14–30.

    Dittmar de la Cruz, K., Morando, M. & Avila, L. (2004) Description of a new pterygosomatid mite (Acari: Actinedida: Pterygosomatidae) parasitic on Liolaemus spp. (Iguania: Liolaemini) from Argentina. Zootaxa, 521, 1–6.

    Evans, S.E. (2003) At the feet of the dinosaurs: the early history and radiation of lizards. Biological reviews of the Cambridge Philosophical Society, 78, 513–551.

    Evans, S.E., Prasad, G.V.R. & Manhas, B.K. (2002) Fossil lizards from the Jurassic Kota Formation of India. Journal of Vertebrate Palaeontology, 22, 299–3123.

    Fain, A. (1994) Adaptation, specificity and host-parasite coevolution in mites (Acari). International Journal for Parasitology, 24, 1273–1283.

    Fajfer, M. (2012) Acari (Chelicerata)—Parasites of Reptiles. Acarina, 20, 108–129.

    Fajfer, M. & González-Acuña, D. (2013) Pterygosomatid mites of a new species group ligare (Acariformes: Pterygosomatidae: Pterygosoma) parasitizing tree iguanas (Squamata: Liolaemidae: Liolaemus). Zootaxa, 3693, 301–319.

    Fajfer, M. (2013a) Three new species of scale mites (Acari: Pterygosomatidae) parasitizing Agama sankaranica (Sauria: Agamidae) Zootaxa, 3700, 271–282.

    Fajfer, M. (2013b) Two New species of scale mites (Acari: Pterygosomatidae) parasitizing Agama agama (Sauria: Agamidae) from Kenya. Zootaxa, 3745, 257–262.

    Fajfer, M. (2014) Redescription of Pterygosoma patagonica (Acariformes: Pterygosomatidae) with new host and distribution data. International Journal of Acarology, 40, 160–164.

    Fajfer, M. & Melnikov, D. (2014) New species and records of scale mites (Acari: Pterygosomatidae) from Arabian agamid lizards (Squamata: Agamidae). Zootaxa, 3764, 401–417.

    Fajfer, M. (2015) Mites of the new species group nitidus (Acariformes: Pterygosomatidae: Geckobia), parasites of lizards in South America. Systematic Parasitology, 90, 213–20.

    Fajfer, M. (2016) Two new species of the genus Pterygosoma (Acariformes: Pterygosomatidae) parasitizing agamid lizards (Sauria: Agamidae) from the Indian subcontinent. Acta Parasitologica, 61, 343–354.

    Fajfer, M., Melnikov, D. & Dabert, M. (2016) Three new species of the genus Pterygosoma Peters, 1849 (Acariformes: Pterygosomatidae) from agamid lizards (Sauria: Agaminae) with DNA barcode data. Systematic Parasitology, 93, 791–814.

    Farris, J.S. (1969) A Successive Approximations Approach to Character Weighting. Systematic Zoology, 18, 374–385.

    Goloboff, P.A., Carpenter, J.M., Arias, J.S. & Esquivel, D.R.M. (2008a) Weighting against homoplasy improves phylogenetic analysis of morphological data sets. Cladistics, 24, 758–773.

    Goloboff, P.A., Farris, J.S. & Nixon, K.C. (2008b) TNT, a free program for phylogenetic analysis. Cladistics, 24, 774–786.

    Grandjean, F. (1939) Les segments postlarvaires de l’hysterosoma chez les oribatides (Acariens). Bulletin Societe Zoology France, 64, 273–284.

    Grandjean, F. (1941) La Chaetotaxie comparee des pattes chez las oribates (1er serie). Bulletin Societe Zoology France, 66, 33–50.

    Grandjean, F. (1944) Observations sure les Acariens de la famille des Stigmaeidae. Archives des Sciences physiques et naturelles, 26, 103–131.

    Grandjean, F. (1946) Au sujet de l’ organe de Claparede, des eupathides multiples et des taenidies mandibulaires chez les Acariens actinochitineux. Archives des Sciences physiques et naturelles, 28, 63–87.

    Grandjean, F. (1954) Observations sur les Oribatides. 28e. Série. Bulletin du Muséum national d'histoire naturelle, 26, 204–211.

    Hedges, S.B. & Vidal, N. (2009) Lizards, snakes, and amphisbaenians (Squamata. In: Hedges, S.B. & Kumar, S. (Eds.) The Timetree of Life. Oxford University Press, New York, pp. 383–389.

    Heredia, V., Vicente, N., Robles, C. & Halloy, M. (2014) Mites in the neotropical lizard Liolaemus pacha (Iguania: Liolaemidae): Relation to body size, sex and season. South American Journal of Herpetology, 9, 14–19.

    Jack, K.M. (1958) Notes on three species of Pterygosoma (Acarina: Pterygosomatidae) from Gerrhosaurid lizards. Parasitology, 48, 89–95.

    Jack, K.M. (1961) New species of Near Eastern agamid scale-mites (Acarina, Pterygosomidae) with notes on the developmental stages of Geckobia hemidactyli Law., 1936. Parasitology, 51, 241–256.

    Jack, K.M. (1962a) New species of Pterygosoma (Acari, Pterygosomatidae). Proceedings of the Zoological Society of London, 138, 579–603.

    Jack, K.M. (1962b) Observations on the genus Pterygosoma (Acari: Pterygosomatidae). Parasitology, 52, 261–295.

    Jack, K.M. (1964) Leg-chaetotaxy with special reference to the Pterygosomatidae (Acarina). Annals of the Natal Museum, 16, 152–171.

    Johnson, K.P., Drown, D.M. & Clayton, D.H. (2001) A data based parsimony method of cophylogenetic analysis. Zoologica Scripta, 30, 79–87.

    Khanjani, M., Pishehvar, S., Mirmoayedi, A. & Khanjani, M. (2013) A new species of Raphignathus Dugés (Acari: Raphignathidae) from Iran. Acarina, 21, 62–68.

    Kissling, W.D., Blach-Overgaard, A., Zwaan, R.E. & Wagner, P. (2016) Historical colonization and dispersal limitation supplement climate and topography in shaping species richness of African lizards (Reptilia: Agaminae). Scientific Reports, 6, 34014.

    Krantz, G.W. & Walter, D.E. (2009) A Manual of Acarology. 3rd Edition. Texas Tech University Press, Lubbock, 807 pp.

    Lawrence, R.F. (1935) The prostigmatic mites of South African lizards Parasitology, 27, 1–45.

    Lawrence, R.F. (1936) The prostigmatic mites of South African lizards. Parasitology, 28, 1–39.

    Lawrence, R.F. (1951) New parasitic mites from South African lizards. Annals of the Transvaal Museum, 21, 447–459.

    Lawrence, R.F. (1959) New mite parasites form South African lizards and bats. Transaction of the Royal Society of South Africa, 35, 569–576.

    Leaché, A.D., Chong, R.A., Papenfuss, T.J., Wagner, P., Böhme, W. & Andreas, S. (2009) Phylogeny of the genus Agama based on mitochondrial DNA sequence data. Bonner zoologische Beiträge, 56, 273278.

    Leaché, A.D., Chong, R.A., Papenfuss, T.J., Wagner, P., Böhme, W., Schmitz, A., Rödel, M. O., Lebreton, M., Ineich, I., Chirio, L., Bauer, A., Eniang, E.A. & Baha El Din, S. (2014) A hybrid phylogenetic-phylogenomic approach for species tree estimation in African Agama lizards with applications to biogeography, character evolution, and diversification. Molecular Phylogenetics and Evolution, 79, 215–230.

    Leaché, A. D., Grummer, J.A., Miller, M., Krishnan, S., Fujita, M.K., Böhme, W., Schmitz, A., Lebreton, M., Ineich, I., Chirio, L., Ofori-boateng, C., Eniang, E.A., Greenbaum, E., Rödel, M.O. & Wagner, P. (2016) Bayesian inference of species diffusion in the West African Agama agama species group (Reptilia, Agamidae). Systematics and Biodiversity, 15, 192–203.

    Macey, J.R., Schulte II, J.A., Larson, A., Ananjeva, A., Wang, Y., Pethiyagoda, R., Rastegar-Pouyani, N. & Papenfuss, T.J. (2000) Evaluating trans-Tethys migration: an example using acrodont lizard phylogenetics. Systematic Biology, 49, 233–256.

    Matthee, C.A. & Flemming, A.F. (2002) Population fragmentation in the southern rock agama, Agama atra: more evidence for vicariance in southern Africa. Molecular Ecology, 11, 465–471.

    Mostafa, A.R. (1974a) The genus Pterygosoma redefined, with a description of two new species from Egypt (Acarina: Pterygosomidae). Acarologia, Paris, 16, 94–99.

    Mostafa, A.R. (1974b) Biological and behavioral aspects of the lizard mite Pterygosoma mutabilis Jack, 1961 (Acarina: Pterygosomidae). Acarologia, Paris, 16, 100–105.

    Müller, K. (2004) PRAP—computation of Bremer support for large data sets. Molecular Phylogenetics and Evolution, 31, 780–782.

    Nagar, S.K., Kumar, K. & Raizada, R.N. (1978) Redescriptions and certain developmental stages of the pterygosomid mites of the Delhi State. The Annals of Zoology, 14, 93–118

    Norton, R.A. (1977) A review of F. Grandjean's system of leg chaetotaxy in the Oribatei and its application to the Damaeidae. In: Dindal, D.L. (Ed.), Biology of Oribatid Mites. S.U.N.Y College of Environmental Science and Forestry, Syracuse, pp. 33−61.

    Page, R.D.M. (1988) TreeView. Version 1.5.2. University of Glasgow, Glasgow. [verified 1 June 2008]

    Page, R.D.M. (1994) Parallel phylogenies reconstructing the history of host—parasite assemblages. Cladistics—The International Journal of the Willi Hennig Society, 10, 155–173.

    Page, R.D.M. (2001) NDE. NEXUS Data Editor 0.5.0. University of Glasgow, Glasgow. [program]

    Paredes-León, R., Klompen, H. & Pérez, T.M. (2012) Systematic revision of the genera Geckobiella Hirst, 1917 and Hirstiella Berlese, 1920 (Acari: Prostigmata: Pterygosomatidae) with description of a new genus for American species parasites on geckos formerly placed in Hirstiella. Zootaxa, 3510, 1–40.

    Prasad, V. (1975) A new genus and species of pterygosomatid mite (Acarina: Pterygosomatidae) from India. International Journal of Acarology, 1, 14–17.

    Pyron, R.A., Burbrink, F.T. & Wiens, J.J. (2013) A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evolutionary Biology, 13, 1–53.

    Rastegar-Pouyani, N. (2005) A multivariane analysis of geographic variation in the Trapelus agilis complex (Sauria: Agamidae) Amphibia-Reptilia, 26, 159–173.

    Schulte J.A. II., Macey J. R., Espinoza R.E. & Larson, A. (2000) Phylogenetic relationships in the iguanid lizard genus Liolaemus: multiple origins of viviparous reproduction and evidence for recurring Andean vicariance and dispersal. Biological Journal of the Linnean Society, 69, 75–102.

    Swofford, D.L. (2015) PAUP. Phylogenetic analysis using parsimony (* and other methods). Version 4. Sinauer Associates, Sunderland, Massachusetts. [software]

    Tałanda, M. (2018) An exceptionally preserved Jurassic skink suggests lizard diversification preceded fragmentation of Pangaea, Palaeontology, 61, 659–677.

    Townsend, T.M., Mulcahy, D.G., Noonan, B.P., Sites Jr., J.W., Kuczynski, C.A., Wiens, J.J. & Reeder, T.W. (2011) Phylogeny of iguanian lizards inferred from 29 nuclear loci, and a comparison of concatenated and species-tree approaches for an ancient, rapid radiation. Molecular Phylogenetics and Evolution, 61, 363–380.

    Trägårdh, I. (1905) Acariden aus Ägypten und dem Sudan. In: Jägerskiöld, L.A. (Ed.), Results of the Swedish Zoological Expedition to Egypt and the White Nile. Part II. Expedition. Library of the Royal University of Uppsala, Upsala, pp. 1–124.

    Uetz, P., Freed, P. & Hošek, J. (eds.), The Reptile Database. Updated 24 December 2016, cited 31 January 2017. Available from: http://www.reptile-database.org (accessed 20 March 2019)

    Wagner, P., Barej, M.F. & Schmitz, A. (2009) Studies on African Agama VII. A new species of the Agama agama-group (Linnaeus, 1758) (Sauria: Agamidae) from Cameroon & Gabon, with comments on Agama mehelyi Tornier, 1902. Bonner zoologische Beiträge, 56, 285–297.

    Wagner, P., Melville J., Wilms, T.M. & Schmitz, A. (2011) Opening a box of cryptic taxa—the first review of the North African desert lizards in the Trapelus mutabilis Merrem, 1820 complex (Squamata: Agamidae) with descriptions of new taxa. Zoological Journal of Linnaean Society, 163, 884–912.

    Wagner, P., Greenbaum, E. & Bauer, A. (2012) A new species of the Acanthocerus atricollis complex (Squamata: Agamidae) from Zambia. Salamandra, 48, 21–30.

    Zhang, Z.-Q. (2018) Repositories for mite and tick specimens: acronyms and their nomenclature. Systematic & Applied Acarology, 23 (12), 2432–2446.

    https://doi.org/10.11158/saa.23.12.12