Abstract
The astigmatid family Hypoderatidae includes over 80 mite species exhibiting peculiar life cycle. Deutonymphs are parasitic instars inhabiting subcutaneous or visceral tissues of birds and rodents, while all other instars are nidicolous forms. In this study we investigated genetic diversity of deutonymphs of two hypoderatid species, Neottialges evansi and Phalacrodectes gaudi, collected from 16 individuals of the great cormorant Phalacrocorax carbo in SW Poland during host post-breeding dispersal. The initial alternative hypotheses were: (1) populations of deutonymphs in both mite species found in tissues of particular bird individuals form genetically distinct populations, (2) mites are panmictic among hosts. The topologies of NJ phylogenetic trees and median-joining haplotype networks reconstructed for COI haplotypes revealed lack of hostdependent genetic structure in populations of N. evansi and P. gaudi. Furthermore, high haplotype diversity (Hd) and low nucleotide diversity (Pi) prove high genetic differentiation of both mite species. We concluded, that unlimited dispersal of mites among cormorant specimens could be explained by host specific breeding behavior: free mating between cormorants originating from different European populations and low contribution of reunited pairs in breeding colonies in subsequent breeding seasons, reuse of the same nest material by different members of the colony, and host behavior called prospecting.
Acknowledgements
We would like to express our deep gratitude to Eberhard Wurst, Senckenberg Gesellschaft für Naturforschung, Frankfurt, Germany for making it possible for us to cite his unpublished observations concerning the life cycle of Neottialges evansi and Phalacrodectes gaudi. We thank Miroslawa Dabert, Molecular Biology Techniques Laboratory, AMU, Poznan, Poland for her help in molecular analyses and valuable comments on the MS. We would like also to show our gratitude to Przemyslaw Chylarecki, Museum and Institute of Zoology, Polish Academy of Sciences, Warsaw, Poland for providing us with important information about breeding behavior of cormorants.
References
Alberti G., Kanarek G., Dabert J. 2016. Unusual way of feeding by the deutonymph of Neottialges evansi (Actinotrichida, Astigmata, Hypoderatidae), a subcutaneous parasite of cormorants, revealed by fine structural analyses. Journal of Morphology, 277, 1368–1389. 10.1002/jmor.20584Search in Google Scholar PubMed
Bandelt H-J., Forster P., Röhl A. 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37–48. 10.1093/oxfordjournals.molbev.a026036Search in Google Scholar PubMed
Bzoma S., Mokwa T., Gromadzki M. 2005. Recoveries of Great Cormorant (Phalacrocorax carbo) in Poland. 7th International Conference on Cormorants, 4th Meeting of Wetlands International Cormorants Research Group, 23–26 November 2005, Villeneuve, Switzerland. Programme and abstracts, pp. 23Search in Google Scholar
Cadiou B., Monnat J-Y., Danchin E. 1994. Prospecting in the kittiwake, Rissa tridactyla: different behavioural patterns and the role of prospecting in recruitment. Animal Behaviour, 47, 847–856. 10.1006/anbe.1994.1116Search in Google Scholar
Calabuig G., Ortego J., Aparicio J.M., Cordero P.J. 2010. Intercolony movements and prospecting behaviour in the colonial lesser kestrel. Animal Behaviour, 79, 811–817. 10.1016/j.anbehav.2009.12.007Search in Google Scholar
Dabert J., Ehrnsberger R., 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, 41–52Search in Google Scholar
Dabert M., Coulson S.J., Gwiazdowicz D.J., Moe B., Hanssen S.A., Biersma E.M., Pilskog H.E., 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, 163–179. 10.1007/s10493-014-9856-1Search in Google Scholar PubMed PubMed Central
Danchin E. 1992. The incidence of the tick parasite Ixodes uriae in kittiwake Rissa tridactyla colonies in relation to the age of the colony and the mechanism of infecting new colonies. Ibis, 134, 134–14110.1111/j.1474-919X.1992.tb08390.xSearch in Google Scholar
de Jong M.A., Wahlberg N., van Eijk M., Brakefield P.M., Zwaan B.J. 2011. Mitochondrial DNA signature for range-wide populations of Bicyclus anynana suggests a rapid expansion from recent refugia. PloS One, 6, e21385. 10.1371/journal.pone.0021385Search in Google Scholar PubMed PubMed Central
Dewey T. 2009. “Phalacrocorax carbo” (On-line), Animal Diversity Web. Accessed August 11, 2016 at http://animaldiversity.org/accounts/Phalacrocorax_carbo/Search in Google Scholar
Dittmann T., Zinsmeister D., Becker P.H. 2005. Dispersal decisions: common terns, Sterna hirundo, choose between colonies during prospecting. Animal Behaviour, 70, 13–20. 10.1016/j.anbehav.2004.09.015Search in Google Scholar
Fain A. 1967. Les hypopes parasites des tissus cellulaires des oiseaux (Hypodectidae: Sarcoptifonnes). Bulletin de L’Institut Royal des Sciences Naturelles de Belgique, Biologie, 43, 1–139 (In French)Search in Google Scholar
Fain A. 1966. Note sur les acariens nidicoles à deutonymphe parasite tissulaire des oiseaux (Hypodectidae: Sarcoptifonnes) (note preliminaire). Revue de Zoologie et de Botanique Africaines, 74, 324–330. (In French)Search in Google Scholar
Fain A., Bafort J. 1967. Cycle évolutif et morphologie de Hypodectes (Hypodectoides) propus (Nitzsch) acarien nidicole a deutonymphe parasite tissulaire des pigeons. Bulletin de la Classe des Sciences Academie Royale de Belgique, 53, 501–533 (In French)Search in Google Scholar
Fain A., Beaucournu J. 1972. Observations sur le cycle evolutif de Pelecanectes evansi Fain et description d’une espece nouvelle du genre Phalacrodectes Fain (Hypoderidae: Sarcoptiformes). Acarologia, 13, 374–382Search in Google Scholar
Fain A., Clark J.M. 1994. Description and life cycle of Suladectes hughesae antipodus subspc.nov. (Acari: Hypoderatidae) associated with Sula bassana serretor Gray (Aves: Pelecaniformes) in New Zealand. Acarologia, 35, 361–371Search in Google Scholar
Fain A., Lawrence B.R. 1986. Two new species of Neottialges Fain (Acari, Hypoderatidae) under the skin of birds, with a key to the hypopi of this genus. Journal of Natural History, 20, 849–85610.1080/00222938600770621Search in Google Scholar
Fain A., Lukoschus F.S. 1986. Observations on the life cycle of Neottialges (Pelecanectes) evansi Fain, 1966 and Phalacrodectes whartoni Fain, 1967 with descriptions of new taxa (Acari, Hypoderatidae). Systematic Parasitology, 8, 291–31610.1007/BF00009738Search in Google Scholar
Felsenstein J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39, 783–791 Ferreri M., Qu W., Han B. 2011. Phylogenetic networks: A tool to display character conflict and demographic history. African Journal of Biotechnology, 10, 12799–12803. 10.5897/ AJB11.010Search in Google Scholar
Ferreri M., Qu W., Han B. 2011. Phylogenetic networks: A tool to display character conflict and demographic history. African Journal of Biotechnology, 10, 12799–12803. 10.5897/ AJB11.010Search in Google Scholar
Goodall-Copestake W.P., Tarling G.A., Murphy E.J. 2012. On the comparison of population-level estimates of haplotype and nucleotide diversity: a case study using the gene cox1 in animals. Heredity, 109, 50–56. 10.1038/hdy.2012.12Search in Google Scholar PubMed PubMed Central
Hall T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98Search in Google Scholar
Janssen-Duijghuijsen G. H. S., Lukoschus F. S., Fain A. 1979. Parasites of Western Australia. 1. Hypopi of the family Hypoderidae Murray, 1877. Records of the Western Australian Museum 7, 1–8Search in Google Scholar
Kimura M. 1980. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111–12010.1007/BF01731581Search in Google Scholar PubMed
Levin I.I., Parker P.G. 2013. Comparative host–parasite population genetic structures: obligate fly ectoparasites on Galapagos seabirds. Parasitology, 140, 1061–1069. 10.1017/S0 031182013000437Search in Google Scholar
Librado P, Rozas J. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452. 10.1093/bioinformatics/btp187Search in Google Scholar PubMed
McCoy K.D., Boulinier T., Tirard C. 2005. Comparative host-parsite population structures: disentangling prospecting and dispersal in the black-legged kittiwake Rissa tridactyla. Molecular Ecology, 14, 2825–2838. 10.1111/j.1365-294X.2005.02631.xSearch in Google Scholar PubMed
Mironov S.V., Kivganov D.A. 2010. Descriptions of adult instars of new and little known mite species of family Hypoderatidae (Acari: Astigmata) from nests of aquatic birds. Acarina, 18, 37–59Search in Google Scholar
Mironov S.V., OConnor B.M. 2013. Two new genera of mites of the family Hypoderatidae (Acari: Astigmata) from swifts and their nests (Apodiformes: Apodidae) from the Philippines. International Journal of Acarology, 39, 209–23410.1080/01647954.2012.758654Search in Google Scholar
OConnor B.M. 1985. Hypoderatid mites (Acari) associated with cormorants (Aves: Phalacrocoracidae) with description of a new species. Journal of Medical Entomology, 22, 324–33110.1093/jmedent/22.3.324Search in Google Scholar
Pence D.B., Bergan J.F. 1996. Hypopi (Acari: Hypoderatidae) from owls (Aves: Strigiformes: Strigidae). Journal of Medical Entomology, 33, 828–83410.1093/jmedent/33.5.828Search in Google Scholar PubMed
Pence D.B., Duncan M. 1995. Hypopi (Acari: Hypoderatidae) from subcutaneous tissues of the African spoonbill (Aves: Ciconiiformes: Threskiornithidae). Journal of Medical Entomology, 32, 166–17310.1093/jmedent/32.2.166Search in Google Scholar
Pence D.B., Spalding M.G. 1996. Hypopi (Acari: Hypoderatidae) from the roseate spoonbill (Aves: Ciconiiformes; Threskiornithidae). Journal of Medical Entomology, 33, 244–24910.1093/jmedent/33.2.244Search in Google Scholar
Pence D.B., Spalding M.G., Bergan J.F., Cole R.A., Newman S., Gray P.N. 1997. New records of subcutaneous mites (Acari: Hypoderatidae) in birds, with examples of potential host colonization events. Journal of Medical Entomology, 34, 411–610.1093/jmedent/34.4.411Search in Google Scholar
Polzin T., Daneschmans V. 2003. On Steiner trees and minimum spanning trees in hypergraphs. Operations Research Letters, 31, 12–20. 10.1016/S0167-6377(02)00185-2Search in Google Scholar
Rambaut A. 2009. FigTree v 1.4.2. University of Edinburgh, Edinburgh, UK. (http://tree.bio.ed.ac.uk/software/figtree/).Search in Google Scholar
Saitou N., Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4, 406–425Search in Google Scholar
Schj⊘rring S. 2001. Ecologically determined natal philopatry within a colony of great cormorants. Behavioral Ecology, 12, 287–294. 10.1093/beheco/12.3.287Search in Google Scholar
Schj⊘rring S., Gregersen J., Bregnballe T. 1999. Prospecting enhances breeding success of first-time breeders in the great cormorant, Phalacrocorax carbo sinensis. Animal Behaviour, 57, 647–654. 10.1006/anbe.1998.0993Search in Google Scholar PubMed
Slatkin M., Hudson R.R. 1991. Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics, 129, 555–56210.1093/genetics/129.2.555Search in Google Scholar PubMed PubMed Central
Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729. 10.1093/molbev/mst197Search in Google Scholar PubMed PubMed Central
Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. 1997. The ClustalX windows interface. Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25, 4876–488210.1093/nar/25.24.4876Search in Google Scholar PubMed PubMed Central
van Schaik J., Kerth G., Bruyndonckx N., Christe P. 2014. The effect of host social system on parasite population genetic structure: comparative population genetics of two ectoparasitic mites and their bat hosts. BMC Evolutionary Biology, 14. 10.1186/1471-2148-14-18Search in Google Scholar PubMed PubMed Central
Wurst E., Havelka P. 1997. Redescription and life history of Tytodectes strigis (Acari: Hypoderatidae), a parasite of the barn owl Tyto alba (Aves: Strigidae). Stuttgarter Beiträge zur Naturkunde, 554A, 1–39Search in Google Scholar
© 2016 W. Stefański Institute of Parasitology, PAS