Molecular evidence for host–parasite co-speciation between lizards and Schellackia parasites

Current and past parasite transmission may depend on the overlap of host distributions, potentially affecting parasite specificity and co-evolutionary processes. Nonetheless, parasite diversification may take place in sympatry when parasites are transmitted by vectors with low mobility. Here, we test the co-speciation hypothesis between lizard final hosts of the Family Lacertidae, and blood parasites of the genus Schellackia, which are potentially transmitted by haematophagous mites. The effects of current distributional overlap of host species on parasite specificity are also investigated. We sampled 27 localities on the Iberian Peninsula and three in northern Africa, and collected blood samples from 981 individual lizards of seven genera and 18 species. The overall prevalence of infection by parasites of the genus Schellackia was ∼35%. We detected 16 Schellackia haplotypes of the 18S rRNA gene, revealing that the genus Schellackia is more diverse than previously thought. Phylogenetic analyses showed that Schellackia haplotypes grouped into two main monophyletic clades, the first including those detected in host species endemic to the Mediterranean region and the second those detected in host genera Acanthodactylus, Zootoca and Takydromus. All but one of the Schellackia haplotypes exhibited a high degree of host specificity at the generic level and 78.5% of them exclusively infected single host species. Some host species within the genera Podarcis (six species) and Iberolacerta (two species) were infected by three non-specific haplotypes of Schellackia, suggesting that host switching might have positively influenced past diversification of the genus. However, the results supported the idea that current host switching is rare because there existed a significant positive correlation between the number of exclusive parasite haplotypes and the number of host species with current sympatric distribution. This result, together with significant support for host–parasite molecular co-speciation, suggests that parasites of the genus Schellackia co-evolved with their lizard hosts.Ministerio de Economía y Competitividad and European Regional Development Fund (MINECO/FEDER) provided financial support (CGL2012-40026-C02-01 and CGL2015-67789-C2-1-P to SM; CGL2012-40026-C02-02 to J. Martínez; CGL2015-64086-P to JGP; CGL2014-53523-P to J. Martín; CGL2008-01522, CGL2012-32459, and CGL2016-76918 to PSF). Partial support to sample in the Guadarrama Mountains was provided to OJR by project CGL2011-30393 conceded to I. de la Riva. Ministerio de Educación, Cultura y Deporte and the European Regional Development Fund (MEC/FEDER) funded JJC and JB (grant CGL2008-00137/BOS). MEC also funded RM-P (BES-2010-038427).Peer reviewe