Hostname: page-component-546b4f848f-gfk6d Total loading time: 0 Render date: 2023-06-03T23:55:27.199Z Has data issue: false Feature Flags: { "useRatesEcommerce": true } hasContentIssue false

High diversity and low genetic structure of feather mites associated with a phenotypically variable bird host

Published online by Cambridge University Press:  17 January 2018

Sofía Fernández-González
Departamento de Biodiversidad, Ecología y Evolución, Facultad de Biología, Universidad Complutense de Madrid, 28040 Madrid, Spain
Antón Pérez-Rodríguez
Departamento de Biodiversidad, Ecología y Evolución, Facultad de Biología, Universidad Complutense de Madrid, 28040 Madrid, Spain
Heather C. Proctor
Department of Biological Sciences, University of Alberta, T6G 2E9 Edmonton, Alberta, Canada
Iván De la Hera
Departamento de Biodiversidad, Ecología y Evolución, Facultad de Biología, Universidad Complutense de Madrid, 28040 Madrid, Spain
Javier Pérez-Tris*
Departamento de Biodiversidad, Ecología y Evolución, Facultad de Biología, Universidad Complutense de Madrid, 28040 Madrid, Spain
Author for correspondence: Javier Pérez-Tris, E-mail:


Obligate symbionts may be genetically structured among host individuals and among phenotypically distinct host populations. Such processes may in turn determine within-host genetic diversity of symbionts, which is relevant for understanding symbiont population dynamics. We analysed the population genetic structure of two species of feather mites (Proctophyllodes sylviae and Trouessartia bifurcata) in migratory and resident blackcaps Sylvia atricapilla that winter sympatrically. Resident and migratory hosts may provide mites with habitats of different qualities, what might promote specialization of mite populations. We found high genetic diversity of within-host populations for both mite species, but no sign of genetic structure of mites between migratory and resident hosts. Our results suggest that, although dispersal mechanisms between hosts during the non-breeding season are unclear, mite populations are not limited by transmission bottlenecks that would reduce genetic diversity among individuals that share a host. Additionally, there is no evidence that host phenotypic divergence (associated with the evolution of migration and residency) has promoted the evolution of host-specialist mite populations. Unrestricted dispersal among host types may allow symbiotic organisms to avoid inbreeding and to persist in the face of habitat heterogeneity in phenotypically diverse host populations.

Research Article
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)



Current address: Department of Zoology and Entomology, Faculty of Natural Sciences, University of the Free State, 9301 Bloemfontein, South Africa.

Current address: School of Biological, Earth and Environmental Sciences, University College Cork, Cork, Ireland.


Atyeo, WT and Braasch, NL (1966) The feather mite genus Proctophyllodes (Sarcoptiformes: Proctophyllodidae). Bulletin of the University of Nebraska State Museum 5, 1354.Google Scholar
Barrett, LG, Thrall, PH, Burdon, JJ and Linde, CC (2008) Life history determines genetic structure and evolutionary potential of host-parasite interactions. Trends in Ecology & Evolution 23, 678685.CrossRefGoogle ScholarPubMed
Criscione, CD (2008) Parasite co-structure: broad and local scale approaches. Parasite-Journal de la Societé Francaise de Parasitologie 15, 439443.Google ScholarPubMed
Dabert, J, Ehrnsberger, R and Dabert, M (2008) Glaucalges tytonis sp. n. (Analgoidea, Xolalgidae) from the barn owl Tyto alba (Strigiformes, Tytonidae): compiling morphology with DNA barcode data for taxon descriptions in mites (Acari). Zootaxa 1719, 4152.Google Scholar
Dabert, M, Coulson, SJ, Gwiazdowicz, DJ, Moe, B, Hanssen, SA, Biersma, EM, Pilskog, HE and Dabert, J (2015) Differences in speciation progress in feather mites (Analgoidea) inhabiting the same host: the case of Zachvatkinia and Alloptes living on Arctic and long-tailed skuas. Experimental and Applied Acarology 65, 163179.CrossRefGoogle ScholarPubMed
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) Jmodeltest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.CrossRefGoogle ScholarPubMed
De la Hera, I, Pérez-Tris, J and Tellería, JL (2009) Migratory behaviour affects the trade-off between feather growth rate and feather quality in a passerine bird. Biological Journal of the Linnean Society 97, 98105.CrossRefGoogle Scholar
De la Hera, I, Pérez-Tris, J and Tellería, JL (2012) Habitat distribution of migratory and sedentary blackcaps Sylvia atricapilla wintering in southern Iberia: a morphological and biogeochemical approach. Journal of Avian Biology 43, 333340.CrossRefGoogle Scholar
Díaz-Real, J, Serrano, D, Pérez-Tris, J, Fernández-González, S, Bermejo, A, Calleja, JA, De la Puente, J, De Palacio, D, Martínez, JL, Moreno-Opo, R, Ponce, C, Frías, O, Tella, JL, Moller, AP, Figuerola, J, Pap, PL, Kovacs, I, Vagasi, CI, Meléndez, L, Blanco, G, Aguilera, E, Senar, JC, Galván, I, Atienzar, F, Barba, E, Cantó, JL, Cortés, V, Monros, JS, Piculo, R, Vogeli, M, et al. (2014) Repeatability of feather mite prevalence and intensity in Passerine birds. PLoS ONE 9, 12.CrossRefGoogle ScholarPubMed
Doña, J, Moreno-García, M, Criscione, CD, Serrano, D and Jovani, R (2015 a) Species mtDNA genetic diversity explained by infrapopulation size in a host-symbiont system. Ecology and Evolution 5, S801S809.CrossRefGoogle Scholar
Doña, J, Díaz-Real, J, Mironov, S, Bazaga, P, Serrano, D and Jovani, R (2015 b) DNA barcoding and minibarcoding as a powerful tool for feather mite studies. Molecular Ecology Resources 15, 12161225.CrossRefGoogle ScholarPubMed
Doña, J, Proctor, H, Mironov, S, Serrano, D and Jovani, R (2016) Global associations between birds and vane-dwelling feather mites. Ecology 97, 3242.CrossRefGoogle ScholarPubMed
Doña, J, Potti, J, De La Hera, I, Blanco, G, Frías, O and Jovani, R (2017 a) Vertical transmission in feather mites: insights into its adaptive value. Ecological Entomology 42, 492499.CrossRefGoogle Scholar
Doña, J, Sweet, AD, Johnson, KP, Serrano, D, Mironov, S and Jovani, R (2017 b) Cophylogenetic analyses reveal extensive host-shift speciation in a highly specialized and host-specific symbiont system. Molecular Phylogenetics and Evolution 115, 190196.CrossRefGoogle Scholar
Emlen, ST (1995) An evolutionary theory of the family. Proceedings of the National Academy of Sciences USA 92, 80928099.CrossRefGoogle Scholar
Excoffier, L and Lischer, HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564567.CrossRefGoogle ScholarPubMed
Fernández-González, S, De la Hera, I, Pérez-Rodríguez, A and Pérez-Tris, J (2013) Divergent host phenotypes create opportunities and constraints on the distribution of two wing-dwelling feather mites. Oikos 122, 12271237.CrossRefGoogle Scholar
Fernández-González, S, Pérez-Rodríguez, A, de la Hera, I, Proctor, HC and Pérez-Tris, J (2015) Different space preferences and within-host competition promote niche partitioning between symbiotic feather mite species. International Journal for Parasitology 45, 655662.CrossRefGoogle ScholarPubMed
Fretwell, SD and Lucas, HL Jr. (1970) On territorial behavior and other factors influencing habitat distribution in birds. Part I: theoretical development. Acta Biotheoretica 19, 1636.CrossRefGoogle Scholar
Garland, T and Adolph, SC (1994) Why not to do two-species comparative studies – limitations on inferring adaptation. Physiological Zoology 67, 797828.CrossRefGoogle Scholar
Hall, TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symposium Series 41, 9598.Google Scholar
Harper, SE, Spradling, TA, Demastes, JW and Calhoun, CS (2015) Host behaviour drives parasite genetics at multiple geographic scales: population genetics of the chewing louse, Thomomydoecus minor. Molecular Ecology 24, 41294144.CrossRefGoogle ScholarPubMed
Hartl, DL and Clark, AG (2007) Principles of Population Genetics. Sunderland, MA: Sinauer Associates Inc.Google Scholar
Hedrick, PW (2000) Genetics of Populations. Burlington, MA: Jones and Bartlett Publishers.Google Scholar
Hewitt, GM (2001) Speciation, hybrid zones and phylogeography – or seeing genes in space and time. Molecular Ecology 10, 537549.CrossRefGoogle ScholarPubMed
Johnson, KP, Williams, BL, Drown, DM, Adams, RJ and Clayton, DH (2002) The population genetics of host specificity: genetic differentiation in dove lice (Insecta: Phthiraptera). Molecular Ecology 11, 2538.CrossRefGoogle Scholar
Jovani, R and Serrano, D (2004) Fine-tuned distribution of feather mites (Astigmata) on the wing of birds: the case of blackcaps Sylvia atricapilla. Journal of Avian Biology 35, 1620.CrossRefGoogle Scholar
Jovani, R, Tella, JL, Sol, D and Ventura, D (2001) Are hippoboscid flies a major mode of transmission of feather mites? Journal of Parasitology 87, 11871189.CrossRefGoogle Scholar
Keller, LF and Waller, DM (2002) Inbreeding effects in wild populations. Trends in Ecology and Evolution 17, 230241.CrossRefGoogle Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 18701874.CrossRefGoogle ScholarPubMed
Lenormand, T (2002) Gene flow and the limits to natural selection. Trends in Ecology & Evolution 17, 183189.CrossRefGoogle Scholar
Martinu, J, Sychra, O, Literák, I, Capek, M, Gustafsson, DL and Stefka, J (2015) Host generalists and specialists emerging side by side: an analysis of evolutionary patterns in the cosmopolitan chewing louse genus Menacanthus. International Journal for Parasitology 45, 6373.CrossRefGoogle ScholarPubMed
McCoy, KD, Boulinier, T, Tirard, C and Michalakis, Y (2003) Host-dependent genetic structure of parasite populations: differential dispersal of seabird tick host races. Evolution 57, 288296.CrossRefGoogle ScholarPubMed
Mideo, N (2009) Parasite adaptations to within-host competition. Trends in Parasitology 25, 261268.CrossRefGoogle ScholarPubMed
Nadler, SA (1995) Microevolution and the genetic structure of parasite populations. Journal of Parasitology 81, 395403.CrossRefGoogle ScholarPubMed
Pérez-Tris, J and Tellería, JL (2002 a) Migratory and sedentary blackcaps in sympatric non-breeding grounds: implications for the evolution of avian migration. Journal of Animal Ecology 71, 211224.CrossRefGoogle Scholar
Pérez-Tris, J and Tellería, JL (2002 b) Regional variation in seasonality affects migratory behaviour and life-history traits of two Mediterranean passerines. Acta Oecologica-International Journal of Ecology 23, 1321.CrossRefGoogle Scholar
Pérez-Tris, J, Bensch, S, Carbonell, R, Helbig, AJ and Tellería, JL (2004) Historical diversification of migration patterns in a passerine bird. Evolution 58, 18191832.CrossRefGoogle Scholar
Poulin, R (2007) Evolutionary Ecology of Parasites. Princeton, NJ: Princeton University Press.Google Scholar
Proctor, HC (2003) Feather mites (Acari: Astigmata): ecology, behavior, and evolution. Annual Review of Entomology 48, 185209.CrossRefGoogle ScholarPubMed
Rigaud, T, Perrot-Minnot, M-J and Brown, MJF (2010) Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence. Proceedings of the Royal Society of London B: Biological Sciences 277, 36933702.CrossRefGoogle ScholarPubMed
Santana, FJ (1976) A review of the genus Trouessartia. Journal of Medical Entomology 1, S1S128.CrossRefGoogle Scholar
Slatkin, M (1987) Gene flow and the geographic structure of natural populations. Science 236, 787792.CrossRefGoogle ScholarPubMed
Szudarek, N, Kanarek, G and Dabert, J (2017) The genetic structure of hypoderatid mites (Actinotrichida: Astigmata) parasitizing great cormorant (Phalacrocorax carbo) during host post-breeding dispersal in Milicz, SW Poland. Acta Parasitologica 62, 7689.CrossRefGoogle ScholarPubMed
Whiteman, NK, Kimball, RT and Parker, PG (2007) Co-phylogeography and comparative population genetics of the threatened Galapagos hawk and three ectoparasite species: ecology shapes population histories within parasite communities. Molecular Ecology 16, 47594773.CrossRefGoogle ScholarPubMed
Supplementary material: File

Fernández-González et al. supplementary material

Figure S1 and Table S1

Download Fernández-González et al. supplementary material(File)
File 1 MB