Comparative phylogeography of a vulnerable bat and its ectoparasite reveals dispersal of a non-mobile parasite among distinct evolutionarily significant units of the host

Abstract

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

Genetic structure and diversity of a rare woodland bat, Myotis bechsteinii: comparison of continental Europe and Britain

“…Our finding of little diversity across the whole of Europe confirms a recent population range expansion which coincides with post-glacial colonisation as observed in multiple bat species (Moussy et al 2015;Petit et al 1999;van Schaik et al 2017). Kerth et al (2008) analysed the HV2 and ND1 mitochondrial genes of M. bechsteinii from the Balkans and suggested that this population may have been the unique glacial refugium for the species as genetic diversity was higher than in Europe.…”

Global warming leads to larger bats with a faster life history pace in the long-lived Bechstein’s bat (Myotis bechsteinii)

“…After DNA extraction, samples were genotyped using 13 polymorphic microsatellite loci, 12 of which had been previously established 59 , 60 . The last marker (GD7VI) was developed following the procedure described in van Schaik et al (2018) 60 . The sequence and primer information have been submitted to GenBank and are available under ascension no.…”

“…A detailed description of all markers and multiplexes used for PCR-amplification is given in the Supplementary Information (see Supplementary Table S6 ). PCR protocols followed van Schaik et al 2018 60 . PCR products were run on a 3130 Genetic Analyzer (Applied Biosystems).…”

Host Phylogeny, Geographic Overlap, and Roost Sharing Shape Parasite Communities in European Bats

“…It is also possible that host and ectoparasite phylogenetic structure in geographically separate populations may influence microevolutionary patterns in associated microbes. Historical processes, such as the postglacial recolonization of regions of Europe by bats (Flanders et al, 2009;Dool et al, 2013), or patterns of host and ectoparasite dispersal across distant locations (Bruyndonckx et al, 2009;Witsenburg et al, 2015;van Schaik et al, 2018) may lead to the formation of distinct microbial lineages. These types of analyses demand additional genetic data to detect fine distinctions between related lineages and are thus beyond the scope of this current work but would be fruitful avenues for future research on vector-borne microorganisms like Bartonella.…”

“…All these forces may combine to generate complex host-vector-microbe communities over evolutionary time but may be predictable given sufficient data and appropriate analytical methods. Moreover, bats are a highly threatened group of wildlife species, play central roles in ecosystems, and deliver valuable ecosystem services such as pollination and pest control (Boyles et al, 2011;Kunz et al, 2011); thus, ecological and evolutionary information on parasites could be informative for bat conservation and ecosystem sustainability (Whiteman and Parker, 2005;van Schaik et al, 2018). In addition to these factors, there are outstanding questions regarding the forces that drive Bartonella evolution in bats.…”