Ticks and Tick-borne Diseases 6 (2015) 334–343 Contents lists available at ScienceDirect Ticks and Tick-borne Diseases j ourna l ho me pa ge: www.elsevier.com/locate/ttbdis Original article Genetic variation in transmission success of the Lyme borreliosis pathogen Borrelia afzelii Nicolas Tonetti a,1 , Maarten J. Voordouw b,*,1 , Jonas Durand b , Séverine Monnier a , Lise Gern a a Institute of Biology, Laboratory of Eco-Epidemiology of Parasites, University of Neuchâtel, Neuchâtel, Switzerland b Institute of Biology, Laboratory of Ecology and Evolution of Parasites, University of Neuchâtel, Neuchâtel, Switzerland a r t i c l e i n f o Article history: Received 24 September 2014 Received in revised form 27 December 2014 Accepted 16 February 2015 Available online 4 March 2015 Keywords: Borrelia afzelii Co-feeding transmission Ixodes ricinus Lyme borreliosis Reproductive number Vector-borne pathogen a b s t r a c t The vector-to-host and host-to-vector transmission steps are the two critical events that define the life cycle of any vector-borne pathogen. We expect negative genetic correlations between these two trans- mission phenotypes, if parasite genotypes specialized at invading the vector are less effective at infecting the vertebrate host and vice versa. We used the tick-borne bacterium Borrelia afzelii, a causative agent of Lyme borreliosis in Europe, to test whether genetic trade-offs exist between tick-to-host, systemic (host-to-tick), and a third mode of co-feeding (tick-to-tick) transmission. We worked with six strains of B. afzelii that were differentiated according to their ospC gene. We compared the three components of transmission among the B. afzelii strains using laboratory rodents as the vertebrate host and a laboratory colony of Ixodes ricinus as the tick vector. We used next generation matrix models to combine these transmission components into a single estimate of the reproductive number (R 0 ) for each B. afzelii strain. We also tested whether these strain-specific estimates of R 0 were correlated with the strain-specific frequencies in the field. We found significant genetic variation in the three transmission components among the B. afzelii strains. This is the first study to document genetic variation in co-feeding transmis- sion for any tick-borne pathogen. We found no evidence of trade-offs as the three pairwise correlations of the transmission rates were all positive. The R 0 values from our laboratory study explained 45% of the variation in the frequencies of the B. afzelii ospC strains in the field. Our study suggests that laboratory estimates of pathogen fitness can predict the distribution of pathogen strains in nature. © 2015 Elsevier GmbH. All rights reserved. Introduction The ability to establish an infection in a naive host and transmis- sion to secondary hosts are the critical fitness components of the parasite life cycle. Parasite populations often exhibit genetic vari- ation in life history traits despite the fact that these characters are expected to be under strong selection. Life history theory suggests that negative genetic correlations (trade-offs) between different components of the parasite life cycle can influence the evolution of the optimal parasite phenotype (Stearns, 1992). Previous work has shown trade-offs among a variety of parasite life history traits * Corresponding author at: Institute of Biology, University of Neuchâtel, Rue Emile-Argand 11, CH-2000 Neuchâtel, Switzerland. Tel.: +41 32 718 3114; fax: +41 32 718 3001. E-mail addresses: nicolas.tonetti@icloud.com (N. Tonetti), maarten.voordouw@unine.ch (M.J. Voordouw), jonas.durand@unine.ch (J. Durand), severine.monnier@unine.ch (S. Monnier), lise.gern@unine.ch (L. Gern). 1 These two authors contributed equally to this work. including within- and among-host transmission, ability to avoid clearance by the host immune system, and parasite life expectancy (de Roode et al., 2008; Ebert, 1998; Fraser et al., 2007; Mackinnon et al., 2008; Mackinnon and Read, 1999). These trade-offs are of considerable interest because they drive the evolution of virulence, which is the level of parasite-induced harm to the host (Ebert and Bull, 2003). Life history trade-offs might be particularly prevalent in vector- borne pathogens that are adapted to live in two very different environments: an arthropod vector and a vertebrate host. The life cycle of all vector-borne pathogens contains two critical transmission events: vector-to-host transmission and host-to- vector transmission (Randolph, 1998). Vector-to-host transmission requires the pathogen to colonize the transmission tissues of the vector (often the salivary glands) and avoid clearance by the vertebrate immune system. Host-to-vector transmission requires ingestion of the pathogen by the vector from the host tissues (blood, skin) and resistance against the arthropod immune system. The genetic and physiological mechanisms underlying these two http://dx.doi.org/10.1016/j.ttbdis.2015.02.007 1877-959X/© 2015 Elsevier GmbH. All rights reserved.