Bartonella species in bat flies (Diptera: Nycteribiidae) from western Africa

Article (PDF Available)inParasitology 139(3):324-9 · March 2012with150 Reads
DOI: 10.1017/S0031182011002113 · Source: PubMed
Abstract
Bat flies are obligate ectoparasites of bats and it has been hypothesized that they may be involved in the transmission of Bartonella species between bats. A survey was conducted to identify whether Cyclopodia greefi greefi (Diptera: Nycteribiidae) collected from Ghana and 2 islands in the Gulf of Guinea harbour Bartonella. In total, 137 adult flies removed from Eidolon helvum, the straw-coloured fruit bat, were screened for the presence of Bartonella by culture and PCR analysis. Bartonella DNA was detected in 91 (66·4%) of the specimens examined and 1 strain of a Bartonella sp., initially identified in E. helvum blood from Kenya, was obtained from a bat fly collected in Ghana. This is the first study, to our knowledge, to report the identification and isolation of Bartonella in bat flies from western Africa.
Bartonella species in bat ies (Diptera: Nycteribiidae)
from western Africa
S. A. BILLETER
1
,D.T.S.HAYMAN
2,3,4
,A.J.PEEL
3,4
,K.BAKER
3,4
,J.L.N.WOOD
3
,
A. CUNNINGHAM
4
,R.SUU-IRE
5
,K.DITTMAR
6
and M. Y. KOSOY
1
*
1
Centers for Disease Control and Prevention, Division of Vector Borne Diseases, Fort Collins, Colorado, USA
2
Rabies and Wildlife Zoonoses Group, Veterinary Laboratories Agency-Weybridge, Surrey, UK
3
Cambridge Infectious Diseases Consortium, Department of Veterinary Medicine, University of Cambridge, Cambridge, UK
4
Institute of Zoology, Zoological Society of London, London NW1 4RY, UK
5
Wildlife Division of the Forestry Commission, Accra, Ghana
6
State University of New York at Bualo, Department of Biological Sciences, Bualo, New York, USA
(Received 20 July 2011; revised 14 October and 24 October 2011; accepted 27 October 2011; first published online 6 February 2012)
SUMMARY
Bat ies are obligate ectoparasites of bats and it has been hypothesized that they may be involved in the transmission of
Bartonella species between bats. A survey was conducted to identify whether Cyclopodia gree gree (Diptera:
Nycteribiidae) collected from Ghana and 2 islands in the Gulf of Guinea harbour Bartonella. In total, 137 adult ies
removed from Eidolon helvum, the straw-coloured fruit bat, were screened for the presence of Bartonella by culture and PCR
analysis. Bartonella DNA was detected in 91 (66·4%) of the specimens examined and 1 strain of a Bartonella sp., initially
identied in E. helvum blood from Kenya, was obtained from a bat y collected in Ghana. This is the rst study, to our
knowledge, to report the identication and isolation of Bartonella in bat ies from western Africa.
Key words: Bartonella, Cyclopodia bat y, Eidolon helvum, bat, Africa, PCR, culture.
INTRODUCTION
Bartonella species are gram-negative bacteria that
infect erythrocytes of their respective hosts and most
are believed to be transmitted by arthropod vectors
(Billeter et al. 2008). There are currently more
than 20 recognized Bartonella species and many of
those are known or suspected zoonotic pathogens
(Breitschwerdt et al. 2010). Bartonella DNA has also
been detected in a wide variety of biting arthropods
including ticks, eas, lice, mites, ies, and keds
(Billeter et al. 2008). The detection of DNA,
however, does not demonstrate viability of the
organism or vector competency of the arthropod.
To date, only 6 Bar tonella species have been
conrmed to be transmitted by an arthropod exper-
imentally; B. bacilliformis istransmitted by Lutzomyia
verrucarum sandies, B. quintana is transmitted by
Pediculus humanus body lice, B. birtlesii is trans-
mitted by Ixodes ricinus ticks, B. henselae is trans-
mitted by Ctenocephalides felis eas, and B. grahamii
and B. taylorii are transmitted by Ctenophthalmus
nobilis eas (Swift, 1920; Battistini, 1931; Chomel
et al. 1996; Bown et al. 2004; Billeter et al. 2008; Reis
et al. 2011).
Eidolon helvum, the straw-coloured fruit bat, is
distributed throughout much of sub-Saharan Africa
and feeds on owers, leaves, and fruits. These bats
tend to roost in colonies of over 100 000, often in
urban areas, and are used as a human food source in
Central and West Africa. Bats are known reservoirs
of zoonotic viruses including rabies, Nipah virus,
coronaviruses, and others, but their role in the
transmission of human pathogenic bacteria has not
been explored in detail (Wong et al. 2007). Results
from our laboratory have shown that some bats,
including E. helvum, are carriers for several unique
Bartonella species but their ability to transmit these
organisms to humans and other animals is unknown
(Kosoy et al. 2010). It is also unknown whether any
arthropod vectors are responsible for the trans-
mission of Bartonella species between bats.
Bat ies (Diptera) are obligate, blood-sucking
ectoparasites often found living in the fur and on
wing membranes of the bat host (Dick and Patterson,
2006). Bat ies are most closely related to tse-tse ies
(Glossinidae) and Hippoboscid ies and all belong to
the same super family, Hippoboscoidea (Dittmar
et al. 2006). Bat ies are divided into 2 families:
Streblidae, most commonly found in the Western
Hemisphere, and Nycteribiidae, predominantly in
the Eastern Hemisphere (Dick and Patterson, 2006).
Although Bartonella DNA was detected in a bat
y, Trichobius major (Diptera: Streblidae) collected
from a Myotis austroriparius in Florida (Reeves et al.
* Corresponding author: Centers for Disease Control and
Prevention, Department of Vector Borne Diseases, 3150
Rampart Road, Fort Collins, CO 80521, USA. Tel:
+ 970 266 3522. Fax: + 970 225 4257. E-mail: mck3@cdc.
gov
324
Parasitology (2012), 139, 324329. © Cambridge University Press 2012
doi:10.1017/S0031182011002113
2005), no surveys have been performed to screen
Nycteribiidae ies for the presence of Bartonella or
demonstrate viability of the organism in these ies.
Because of this, a study was performed to examine
bat ies from western Africa for the presence of
Bartonella using culture and PCR analysis.
MATERIALS AND METHODS
Bat y collection and identication
Bat ies were collected from E. helvum in Ghana and
on 2 islands in the Gulf of Guinea, Annobón and
Bioko; in total 137 ies were examined (Fig. 1). From
the study site in Accra, Ghana, 46 adult ies were
collected, placed into pots, and transferred to 80 °C
shortly thereafter. From the island of Annobón, a
total of 32 ies was collected: 16 were suspended in
70% ethanol and 16 were placed at 80 °C. A total of
59 bat ies was collected from E. helvum on the
island of Bioko and all samples were placed in tubes
containing 70% ethanol. Samples were subsequently
shipped overnight on dry ice (those samples frozen at
80 °C) or ice packs (samples suspended in ethanol)
to the Ft. Collins CDC, Bartonella Laboratory.
Upon arrival, all samples were placed at 80 °C
until further analysis. After DNA extraction, exo-
skeletons were kept as DNA vouchers and were
subsequently slide mounted in PVA (BioQuip
Products, Rancho Dominguez, CA, USA). Bat ies
were sexed and identi ed using the species keys of
Theodor (1967). All specimens keyed to Cyclopodia
gree gree, based on the characteristic setation of the
fore-tibiae, the presence of a quadratic patch of long
dorsal abdominal setae on the female, characteristic
head morphology, a broad, open haltere groove, and a
single dorsal thoracic seta. Specimens collected from
Annobón were slightly heavier sclerotized, but
otherwise adhered to the key.
Culturing of Barton ella spp. from ies
All frozen bat y specimens were thawed, subjected
to surface sterilization using a Wescodyne wash
(20 min) followed by a 70% ethanol wash (5 min),
and were then rinsed in sterile 1x PBS (0·15 M, pH:
7·50, Atlanta, CDC). Flies were cut in half long-
itudinally using a sterile scalpel blade so that half
could be used for DNA extraction and half for culture
analysis. For culture, ies were suspended in 500 μlof
Brain Heart Infusio n (BHI) broth (CDC) containing
20% fungizone; 300 μl was aliquoted onto a BHI agar
plate containing 5 or 10% debrinated rabbit blood
(CDC). Plates were placed at 35 °C, 5% CO
2
and
examined daily for up to 4 weeks. Any Bartonella-like
colonies were subcultured by streaking onto a fresh
rabbit blood agar plate.
DNA extraction and PCR amplication
DNA extraction of 137 adult bat ies and second
passage colonies was performed using a Qiagen
Fig. 1. Map of western Africa, including the sites of bat y collection. A total of 137 adult Cyclopodia gree gree ies
were collected from Eidolon helvum:46ies from Accra, Ghana, 32 ies from the island of Annobón, and 59 ies from
the island of Bioko.
325Bartonella species in African bat ies
QIAamp tissue kit (QIAGEN, Valencia, CA, USA)
according to the manufacturers instructions. Prior
to DNA extraction, the bat ies in ethanol were
triturated using a sterile scalpel blade. For the
cultured Bartonella, 6 individual colonies from 1
isolate were picked using a sterile loop and suspended
in 200 μl of BHI broth. Bat ies were examined for
the presence of Bartonella DNA by conventional
PCR. Primers 443f (5 GCT ATG TCT GCA TTC
TAT CA) (Birtles and Raoult, 1996) and 1210r
(5 GAT CYT CAA TCA TTT CTT TCC A) were
designed to amplify a portion of the citrate synthase
gene, gltA. Each 50 μl PCR reaction contained
28·75 μl of nuclease-free water, 5x PCR buer
containing MgCl
2
, 0·2 mM dNTPs, 15 pmol of
each primer, and 1·25 U of GoTaq DNA polymerase
(Promega, Madison, WI, USA). PCR was performed
using a Bio-Rad Laboratories iCycler (Hercules, CA,
USA) with the following cycling conditions: 94 °C
for 2 min followed by 45 cycles of 94 °C for 30 sec,
48 °C for 1 min, 72 °C for 1 min, and 1 cycle of 72 °C
for 7 min.
PCR products were separated using electro-
phoresis in a 1·5% agarose gel containing ethidium
bromide and were visualized under UV light.
The positive control consisted of B. doshiae
DNA and nuclease-free water was used as a negative
control.
Gene sequencing and analysis
Amplicons were puried using the QIAquick PCR
purication kit (QIAGEN) and sequenced using an
Applied Biosystems Model 3130 Genetic Analyzer
(Applied Biosystems, Foster City, CA, USA). DNA
sequences were analysed using the Lasergene v8
sequence analysis software (DNASTAR, Madison,
WI, USA) to determine a consensus sequence for the
PCR product from each bat y. All sequences from
this study were subsequently cropped, *307 bp, for
further phylogenetic analysis. Sequences obtained in
this study were considered similar to validated
Bartonella species if similarity over the gltA fragment
was >96·0% (La Scola et al. 2003). The Clustal W
program in Megalign (Lasergene) was used to
compare sequences obtained from this study to
Bartonella sequences available in GenBank. GltA
sequences from 5 novel Bartonella species, isolated
from E. helvum in Kenya, were also included in
the phylogenetic analyses. Five species, identied
as E1, E2, E3, Ew (GenBank number:
HM363765 HM363768) and E-124 (GenBank
number: JN190887), represent bat specic
Bartonella.
The neighbor-joining (N-J) method based on
the Kimura 2-parameter model and the boot-
strap calculations were carried out with 1000 re-
samplings.
Nucleotide sequence Accession numbers
Sequences, representative of each genotype obtained
from this study, were deposited in GenBank under
Accession numbers JN172035 JN172074.
RESULTS
Prevalence of Bartonella DNA in bat ies
Of the 137 adult bat ies examined, 66·4% were PCR
positive for the presence of Bartonella DNA using
gltA specic primers (Table 1). Positivity from each
location ranged from 56·5% in Ghana to 71·9% on the
island of Annobón.
Genetic heterogeneity
Of 82 sequences examined, a total of 39 genotypes
( genotype consisting of 1 or more nucleotide dier-
ences) were found (Table 2). Eight genotypes were
represented by 230 identical sequences. The
sequence similarity among Bartonella sequences
detected in bat ies ranged between 71·4 and 100%,
while similarity among Bartonella sequences ob-
tained from bat ies and those identied previously
from E. helvum ranged from 71·9 to 100%. Fifty-
ve of the 82 sequences were 596% similar to
Bartonella previously isolated from E. helvum
or other Bartonella species, suggesting that the
remaining 27 sequences may represent novel species
(Fig. 2).
Isolation of a Bartonella sp. from a bat y
Although attempts to culture Bartonella spp. from
bat ies were largely unsuccessful due to overgrowth
of contaminants, a single isolate from a bat ywas
obtained. A Bartonella sp. isolate, 98·4% identical
to Bartonella sp. E1-105 isolated from bats in
Kenya based on gltA sequence analysis (GenBank
Accession: HM363765), was cultured from 1 bat y
collected in Ghana (y Cg 23 Q22-1). Further
molecular characterization was performed by se-
quence analysis of the 16S rRNA gene, ftsZ,
and rpoB using methods described previously
Table 1. Prevalence of Bartonella DNA in adult
bat ies from western Africa
Location of
collection
Total number of
adult bat ies
examined
% PCR positive
per location
Ghana 46 56·5% (26)
Annobón
island
32 71·9% (23)
Bioko island 59 71·2% (42)
TOTAL 137 66·4% (91)
326S. A. Billeter and others
(Marchesi et al. 1998; Renesto et al. 2001; Zeaiter
et al. 2002). Comparison of sequence data from
Bartonella E1-105 demonstrated sequence simi-
larity of 100%, 100%, and 99·8% within the 16S
rRNA gene, ftsZ, and rpoB genes, respectively
(GenBank Accession numbers for Bartonella
E1-105: HM363785, HM363770 and HM363775).
DISCUSSION
Within the current study, we demonstrated (1) the
presence of Bartonella DNA in bat ies from western
Africa and (2) the successful culture of Bartonella
from a bat y collected in Ghana. Bartonella
DNA has previously been detected in bat ectopar-
asites, specically in a T. major bat y, Cimex
adjunctus (Hemiptera: Cimicidae) bat bug, Carios
kelleyi (Acari: Argasidae) tick, Sternopsylla
texanus (Siphonaptera: Ischnopsyllidae) ea, and a
Steatonyssus sp. mite (Acari: Mesostigmata) (Loftis
et al. 2005; Reeves et al. 2005, 2006a, 2007). Our
data, unlike previous surveys, reveals that a large
percentage (up to 66·4%) of C. gree gree harboured
Bartonella DNA and, in at least 1 case, viability of the
bacteria could be conrmed. More than half (65·9%
of 82) of the sequences obtained were identical or
similar to Bartonella species previously isolated from
E. helvum (Kosoy et al. 2010), suggesting a potential
role of bat ies in the transmission of Bartonella
between bats. When compared with Bartonella
species isolated from other bat species in Kenya, the
bat y Bartonella genotypes detected in this study
appear to be very host specic (data not shown).
Interestingly, 27 (32·9%) Bartonella sequences did
appear to be unique to bat ies. It is unclear, at this
point, whether Bartonella species may circulate
among bat ies outside of the host or whether these
27 sequences represent potential symbionts.
Previous investigations have also pointed to the
likely potential of Bartonella transmission by other
hippoboscid ies. Lipoptena cervi, or the deer ked, is
the suspected vector of B. schoenbuchensis in deer.
Dehio et al. (2004) successfully isolated B. schoenbu-
chensis from deer ked collected in Germany
and demonstrated the presence of the bacteria in the
mid-gut of the ies. Bartonella DNA has also been
detected in L. cervi from Massachusetts and
L. maza mae collected in South Carolina (Reeves
et al. 2006b; Matsumoto et al. 2008). Halos et al.
(2004) detected Bartonella DNA in a large percentage
of L. cervi (94% of 48 adults) , Hippobosca equina (71%
of 17 adults), and Melophagus ovinus (100% of 20
adults) collected from 4 dierent ruminant spe cies.
Bartonella DNA was also found in 100% (10 total) of
the M. ovinus pupae screened suggesting the bacteria
may be vertically transmitted in this species.
Further investigation is warranted to decipher
what role, if any, bat ies or other bat ectoparasites
might play in the transmission of Bartonella spp.
between bats. Future studies will be performed to
screen bat ies from other bat species and locations
for the presence of Bartonella. Attempts will also be
made to isolate viable Bartonella from pupae to
ascertain whether vertical transmission of the bacteria
may occur, as suggested by Halos et al.(2004). Bat
ies undergo adenotrophic vivaparity (i.e. the com-
plete development of 3 larval stages inside the adult
female) and deposition of a single pre-pupae. This
unique reproductive ability may facilitate vertical
transmission of parasites, including Bartonella spp.
(Dittmar et al. 2006). Importantly, eorts also are on-
going to determine whether these agents are respon-
sible for human illnesses.
Table 2. The total number of 39 Bartonella genotypes, from 82 sequences examined, detected in bat ies
from western Africa
(Genotypes with identical sequences were given identication numbers of 18. All remaining
genotypes were unique.)
Genotype
designation
Total number of sequences detected per genotype
(representative GenBank Accession number)
Total number of sequences
from each location
Ghana Annobón Bioko
1 30 (JN172039) 6 8 16
2 3 (JN172056) 0 3 0
3 3 (JN172072) 0 0 3
4 3 (JN172044) 1 1 1
5 3 (JN172040) 1 1 1
6 4 (JN172035) 2 1 1
7 3 (JN172048) 1 2 0
8 2 (JN172052) 0 1 1
Unique
sequences
31 10 6 15
TOTAL 82 21 23 38
327Bartonella species in African bat ies
ACKNOWLEDGEMENTS
S. A. Billeter is supported through the American Society of
Microbiology/Centers for Disease Control and Prevention
Post-Doctoral Associates Program in Infectious Diseases
and Public Health Microbiology. D. T. S. Hayman
is supported by a Wellcome Trust Research Training
Fellowship, J. L. N. Wood is supported by the Alborado
Trust, and both are supported by the RAPIDD program of
the Science & Technology, Directorate, Department of
Fig. 2. Tree topology displaying similarity of Bartonella DNA detected in Cyclopodia gree gree with known
Bartonella sequences based upon partial citrate synthase gene, gltA. The topology was constructed by the
neighbor-joining method based on the Kimura-2 parameter model of nucleotide substitution. Bootstrap values are based
on 1000 replicates. The tree was rooted by the use of Brucella melitensis 16M
T
as the out-group. Bartonella sequences
obtained from 5 Eidolon helvum , collected in Kenya (Kosoy et al. 2010), are included in the tree (GenBank Accession
numbers: HM363765 HM363768 and JN190887). Unique Bartonella sequences identied in bat ies from Annobón
are represented by GenBank Accession numbers JN172049 JN172057, Bartonella sequences obtained from bat ies
from Bioko are represented by GenBank Accession numbers JN172058 JN172074, and Bartonella sequences obtained
from Ghana bat ies are represented by GenBank Accession numbers JN172035 JN172048.
328S. A. Billeter and others
Homeland Security. K. Baker is supported by a Wellcome
Trust Research Training Fellowship. A. A. Cunningham
is supported by a Royal Society Wolfson Research Merit
award.
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329Bartonella species in African bat ies
    • "We first compiled sequence data for this study from a previous analysis of bat-bartonella codivergence by Lei and Olival (2014) and then expanded by searching Web of Science and Google Scholar using the terms " bat* bartonella " . This compiled data from the literature included partial citrate synthase gene sequences (gltA) for Bartonella genotypes from bats and ectoparasites (bat flies and fleas) from the UK, Guatemala, Peru, Taiwan, Finland, Puerto Rico, multiple countries in Africa, Costa Rica, and Vietnam (Anh et al., 2015; Bai et al., 2015 Bai et al., , 2012 Bai et al., , 2011 Billeter et al., 2012; Brook et al., 2015; Concannon et al., 2005; Judson et al., 2015; Kamani et al., 2014; Kosoy et al., 2010; Lin et al., 2012; Morse et al., 2012; Olival et al., 2015; Veikkolainen et al., 2014). The gltA gene has been shown to provide good phylogenetic resolution among known Bartonella species and subspecies (Norman et al., 1995) and is widely used for detection of bartonella infections. "
    [Show abstract] [Hide abstract] ABSTRACT: The influence of factors contributing to parasite diversity in individual hosts and communities are increasingly studied, but there has been less focus on the dominant processes leading to parasite diversification. Using bartonella infections in bats as a model system, we explored the influence of three processes that can contribute to bartonella diversification and lineage formation: (1) spatial correlation in the invasion and transmission of bartonella among bats (phylogeography); (2) divergent adaptation of bartonellae to bat hosts and arthropod vectors; and (3) evolutionary codivergence between bats and bartonellae. Using a combination of global fit techniques and ancestral state reconstruction, we found that codivergence appears to be the dominant process leading to diversification of bartonella in bats, with lineages of bartonellae corresponding to separate bat suborders, superfamilies, and families. Furthermore, we estimated the rates at which bartonellae shift bat hosts across taxonomic scales (suborders, superfamilies, and families) and found that transition rates decrease with increasing taxonomic distance, providing support for a mechanism that can contribute to the observed evolutionary congruence between bats and their associated bartonellae. While bartonella diversification is associated with host sympatry, the influence of this factor is minor compared to the influence of codivergence and there is a clear indication that some bartonella lineages span multiple regions, particularly between Africa and Southeast Asia. Divergent adaptation of bartonellae to bat hosts and arthropod vectors is apparent and can dilute the overall pattern of codivergence, however its importance in the formation of Bartonella lineages in bats is small relative to codivergence. We argue that exploring all three of these processes yields a more complete understanding of bat-bartonella relationships and the evolution of the genus Bartonella, generally. Application of these methods to other infectious bacteria and viruses could uncover common processes that lead to parasite diversification and the formation of host-parasite relationships.
    Full-text · Article · Jul 2016
    • "Bacteria within the genus Bartonella are Gram-negative, fastidious, aerobic, oxidase-negative, slow-growing in vitro, pleiomorphic organisms, belonging to the alpha-2 subgroup of the class Proteobacteria on the basis of their 16S rDNA sequences. To date, 31 Bartonella species have been officially validated [1,2], and many isolates have yet to be described [3,4]. These bacteria are specifically adapted to distinct mammalian reservoir hosts where they cause intra-erythrocytic infections [5]. "
    [Show abstract] [Hide abstract] ABSTRACT: Abstract The bacterial genus Bartonella is classified in the alpha-2 Proteobacteria on the basis of 16S rDNA sequence comparison. The Bartonella two-component system feuPQ is found in nearly all bacterial species. We investigated the usefulness of the response regulator feuP gene sequence in the classification of 18 well characterized Bartonella species. Phylogenetic relationships were inferred using parsimony neighbour-joining and maximum-likelihood methods. Reliable classifications of most of the studied species were obtained. Bartonella were divided into two supported clades containing two supported clusters each. These results were similar to our previous data obtained with groEL ftsZ and ribC genes sequences. The wide range of feuP DNA sequence similarity 78.6 to 96.5 among Bartonella species makes it a promising candidate for multi-locus sequence typing MLST of clinical isolates. This is the first report proving the usefulness of feuP sequences in bartonellae classification at the species level.
    Full-text · Article · Nov 2015
    • "Whether bat flies impose significant direct fitness costs on their hosts is largely unknown, but costs are generally considered minor (Zahn & Rupp 2004; Dick & Patterson 2006). However, bat flies can serve as vectors for more costly endoparasites, including Haemosporidia and Bartonella (Megali et al. 2011; Billeter et al. 2012). Regardless of the exact cost of infection, Bechstein's bats employ several behaviours that limit B. nana transmission and infection intensity (Reckardt & Kerth 2007), suggesting that infection may be costly in some way. "
    [Show abstract] [Hide abstract] ABSTRACT: Host-parasite interactions are ubiquitous in nature. However, how parasite population genetic structure is shaped by the interaction between host and parasite life history remains understudied. Studies comparing multiple parasites infecting a single host can be used to investigate how different parasite life history traits interplay with host behaviour and life history. In this study, we used 10 newly developed microsatellite loci to investigate the genetic structure of the parasitic bat fly (Basilia nana). Its host, the Bechstein's bat (Myotis bechsteinii), has a social system and roosting behaviour that restrict opportunities for parasite transmission. We compared fly genetic structure to that of the host and another parasite, the wing-mite, Spinturnix bechsteini. We found little spatial or temporal genetic structure in B. nana, suggesting a large, stable population with frequent genetic exchange between fly populations from different bat colonies. This contrasts sharply with the genetic structure of the wing-mite, which is highly sub-structured between the same bat colonies as well as temporally unstable. Our results suggest that although host and parasite life history interact to yield similar transmission patterns in both parasite species, the level of gene flow and eventual spatio-temporal genetic stability is differentially affected. This can be explained by the differences in generation time and winter survival between the flies and wing-mites. Our study thus exemplifies that the population genetic structure of parasites on a single host can vary strongly as a result of how their individual life history characteristics interact with host behaviour and life history traits. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
    Article · Mar 2015
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