Comparative phylogeography of a vulnerable bat and its ectoparasite reveals dispersal of a non-mobile parasite among distinct evolutionarily significant units of the host
Knowledge about phylogeographical structuring and genetic diversity is of key importance for the conservation of endangered species. Comparative phylogeography of a host and its parasite has the potential to reveal cryptic dispersal and behaviour in both species, and can thus be used to guide conservation management. In this study, we investigate the phylogeographic structure of the Bechstein’s bat, Myotis bechsteinii, and its ectoparasitic bat fly, Basilia nana, at 12 sites across their entire distribution. For both species, a mitochondrial sequence fragment (ND1 and COI respectively) and nuclear microsatellite genotypes (14 and 10 loci respectively) were generated and used to compare the phylogeography of host and parasite. Our findings confirm the presence of three distinct genetic subpopulations of the Bechstein’s bat in (1) Europe, (2) the Caucasus and (3) Iran, which remain isolated from one another. The genetic distinctiveness of host populations in the Caucasus region and Iran emphasize that these populations must be managed as distinct evolutionarily significant units. This phylogeographical pattern is however not reflected in its parasite, B. nana, which shows evidence for more recent dispersal between host subpopulations. The discordant genetic pattern between host and parasite suggest that despite the long-term genetic isolation of the different host subpopulations, long-range dispersal of the parasite has occurred more recently, either as the result of secondary contact in the primary host or via secondary host species. This indicates that a novel pathogenic threat to one host subpopulation may be able to disperse, and thus have important consequences for all subpopulations.
KeywordsMyotis bechsteinii Basilia nana Nycteribiidae Co-phylogeography Parasite biogeography
This project was funded by a grant from the Volkswagen Foundation (Az 84959). We thank Ina Römer for her assistance in the lab. We are indebted to the following people for providing samples: Petr Benda, Andrej Conti, Christian Dietz, Peter Estok, Tamas Görföl, Lena Grosche, Frauke Meier, Markus Melber, Collin Morris, Maria Napal, Beytullah Özkan, Serbüllent Pakzus, Boyan Petrov, Sébastien Puechmaille.
Compliance with ethical standards
Sampling of Bechstein’s bats was carried out under license from the responsible nature conservancy departments.
Conflict of interest
The authors declare that they have no conflict of interest.
- Hafner MS, Demastes JW, Spradling TA, Reed DL (2003) Cophylogeny between pocket gophers and chewing lice. In:Page RDM (ed) Tangled trees: phylogeny, cospeciation, and coevolution. University of Chicago Press, Chicago, pp 195–220Google Scholar
- Hutson AM, Aulagnier S, Spitzenberger F (2008) Myotis nattereri. The IUCN Red List of Threatened Species 2008; e.T14135A4405996Google Scholar
- Kerth G, Petrov B, Conti A, Anastasov D, Weishaar M, Gazaryan S, Jaquiery J, Konig B, Perrin N, Bruyndonckx N (2008) Communally breeding Bechstein’s bats have a stable social system that is independent from the postglacial history and location of the populations. Mol Ecol 17:2368–2381CrossRefPubMedGoogle Scholar
- Nagy ZT, Sonet G, Mortelmans J, Vandewynkel C, Grootaert P (2013) Using DNA barcodes for assessing diversity in the family Hybotidae (Diptera, Empidoidea). ZooKeys 365:263–278Google Scholar
- Nieberding CM, Morand S (2007) Comparative phylogeography: the use of parasites for insights into host history. In:Krasnov BR, Morand S, Poulin R (eds) Micromammals and macroparasites: from evolutionary ecology to management. Springer, Tokyo, 277–293Google Scholar
- Paunovíc M (2016) Myotis bechsteinii. The IUCN Red List of Threatened Species 2016; e.T14123A22053752Google Scholar
- Rambaut A, Suchard M, Xie W, Drummond A (2014) Tracer v1.6. Institute of Evolutionary Biology, University of Edinburgh, EdinburghGoogle Scholar
- Ruedi M, Stadelmann B, Gager Y, Douzery EJ, Francis CM, Lin LK, Guillen-Servent A, Cibois A (2013) Molecular phylogenetic reconstructions identify East Asia as the cradle for the evolution of the cosmopolitan genus Myotis (Mammalia, Chiroptera). Mol Phylogenet Evol 69:437–449CrossRefPubMedGoogle Scholar
- Theodor O (1967) An Illustrated Catalogue of the Rothschild Collection of Nycteribiidae (Diptera) in the British Museum (Natural History). Publication 655. London: Trustees of the British Museum (Natural History), 8, 5Google Scholar
- Topál G (1983) New and rare fossil mouse-eared bats from the Middle Pliocene of Hungary (Mammalia, Chiroptera). Fragmenta Mineralogica et Palaeontologica 11:43–54Google Scholar
- Wang J (2017) The computer program structure for assigning individuals to populations: easy to use but easier to misuse. Mol Ecol Resour 17:981–990Google Scholar
- Witsenburg F, Clement L, Lopez-Baucells A, Palmeirim J, Pavlinic I, Scaravelli D, Sevcik M, Dutoit L, Salamin N, Goudet J, Christe P (2015) How a haemosporidian parasite of bats gets around: the genetic structure of a parasite, vector and host compared. Mol Ecol 24:926–940CrossRefPubMedGoogle Scholar
- Yavruyan E, Rakhmatulina I, Bukhnikashvili A, Kandaurov A, Natradze I, Gazaryan S (2008) Bats conservation action plan for the Caucasus. Publishing House Universal, TbilisiGoogle Scholar