Evidence for genetic variation in Natterer’s bats (Myotis nattereri) across three regions in Germany but no evidence for co-variation with their associated astroviruses

Halczok et al. BMC Evolutionary Biology (2017) 17:5 DOI 10.1186/s12862-016-0856-0 RESEARCH ARTICLE Open Access Evidence for genetic variation in Natterer’s bats (Myotis nattereri) across three regions in Germany but no evidence for covariation with their associated astroviruses Tanja K. Halczok1*, Kerstin Fischer2, Robert Gierke1, Veronika Zeus1, Frauke Meier3, Christoph Treß4, Anne Balkema-Buschmann2, Sébastien J. Puechmaille1 and Gerald Kerth1 Abstract Background: As bats have recently been described to harbor many different viruses, several studies have investigated the genetic co-variation between viruses and different bat species. However, little is known about the genetic co-variation of viruses and different populations of the same bat species, although such information is needed for an understanding of virus transmission dynamics within a given host species. We hypothesized that if virus transmission between host populations depends on events linked to gene flow in the bats, genetic co-variation should exist between host populations and astroviruses. Results: We used 19 nuclear and one mitochondrial microsatellite loci to analyze the genetic population structure of the Natterer’s bat (Myotis nattereri) within and among populations at different geographical scales in Germany. Further, we correlated the observed bat population structure to that of partial astrovirus sequences (323–394 nt fragments of the RNA-dependent RNA polymerase gene) obtained from the same bat populations. Our analyses revealed that the studied bat colonies can be grouped into three distinct genetic clusters, corresponding to the three geographic regions sampled. Furthermore, we observed an overall isolation-by-distance pattern, while no significant pattern was observed within a geographic region. Moreover, we found no correlation between the genetic distances among the bat populations and the astrovirus sequences they harbored. Even though high genetic similarity of some of the astrovirus haplotypes found in several different regions was detected, identical astrovirus haplotypes were not shared between different sampled regions. Conclusions: The genetic population structure of the bat host suggests that mating sites where several local breeding colonies meet act as stepping-stones for gene flow. Identical astrovirus haplotypes were not shared between different sampled regions suggesting that astroviruses are mostly transmitted among host colonies at the local scale. Nevertheless, high genetic similarity of some of the astrovirus haplotypes found in several different regions implies that occasional transmission across regions with subsequent mutations of the virus haplotypes does occur. Keywords: Genetic, Population structure, Myotis nattereri, Astrovirus, Host, Gene flow * Correspondence: 1 Ernst-Moritz-Arndt Universität Greifswald, Zoological Institute and Museum, Soldmannstr. 14, 17489 Greifswald, Germany Full list of author information is available at the end of the article © The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Halczok et al. BMC Evolutionary Biology (2017) 17:5 Background With their particular social, ecological, physiological and immunological traits, bats provide unique hosts for many viruses to co-evolve with (e.g. [1, 2]). Indeed, bats are increasingly recognized as reservoirs for a wide range of viruses, some of which carry a zoonotic potential, for example rabies and other viruses of the genus Lyssavirus, SARS-like, MERS-like and other coronaviruses [2–5]. Consequently, several studies have investigated the genetic co-variation between different bat species and their associated viruses [6, 7]. However, much less is known about genetic co-variation of viruses and different populations of the same bat species, although such information is required to gain a better understanding of the transmission dynamics within a given host species (e.g. [8, 9]). The Natterer’s bat (Myotis nattereri Kuhl 1817 sensu lato [10]) is a non-migratory vespertilionid bat that is widespread throughout Europe with the exception of the Iberian and Italian peninsula and the South of France [11]. While this species uses underground sites for hibernation during the winter months, it mostly roosts in trees and buildings during summer forming maternity colonies that consist of female bats and their juveniles as well as occasionally some males [12, 13]. Males typically roost either individually or in small groups in the vicinity of the maternity colonies [14]. Male and female Natterer’s bats have been found to exhibit philopatry even though males leave their natal colony but stay in its vicinity [13]. Mating takes place during autumn at swarming sites that are typically up to 50 km away from the summer colony [13]. Recently, various viruses have been reported to be harbored by M. nattereri [15], including herpes- [16], lyssa[17] and astroviruses (e.g. [18]). The Astroviridae form a large family of non-enveloped, positive-sense, singlestranded RNA viruses [19]. Astroviruses are mostly transmitted via the fecal-oral route [20] and may cause diarrhea in many animal species, including humans [21]. However, the route of transmission in bats has not yet been elucidated. Even though astroviruses have been detected in a variety of species [22], bats have been hypothesized to be a potential reservoir host in Europe and Asia [7, 23]. The high prevalence and diversity of astroviruses harbored by bats is remarkable [18, 21, 23] and their capability to cross species barriers and become adapted to new hosts, including spill-over to other taxa, has been suggested [24]. Due to the occurrence of astroviruses in animals in close contact to humans, e.g. livestock and also bats using human habitation as roosting, it has been argued that astroviruses should be considered as potential candidates for zoonotic infections (e.g. [24]). However, almost nothing is known about the transmission of astrovirus among different populations of their bat hosts. Page 2 of 11 We studied patterns of population genetic structure and dispersal of Myotis nattereri within and among three geographic regions of Germany using both nuclear and mitochondrial microsatellite markers. The population genetic structure of M. nattereri has previously only been investigated in the United Kingdom (UK; [13]). However, the population genetic structure of bats occurring in the UK may be affected by t (...truncated)