The integration of multiple independent data reveals an unusual response to Pleistocene climatic changes in the hard tick Ixodes ricinus

Department of Ecological and Biological Sciences, Tuscia University, Viterbo, Italy.
Molecular Ecology (Impact Factor: 6.49). 02/2013; 22(6). DOI: 10.1111/mec.12203
Source: PubMed


In the last few years, improved analytical tools and the integration of genetic data with multiple sources of information have shown that temperate species exhibited more complex responses to ice ages than previously thought. In this study, we investigated how Pleistocene climatic changes affected the current distribution and genetic diversity of European populations of the tick Ixodes ricinus, an ectoparasite with high ecological plasticity. We first used mitochondrial and nuclear genetic markers to investigate the phylogeographic structure of the species and its Pleistocene history using coalescent-based methods; then we used species distribution modelling to infer the climatic niche of the species at last glacial maximum; finally, we reviewed the literature on the I. ricinus hosts to identify the locations of their glacial refugia. Our results support the scenario that during the last glacial phase, I. ricinus never experienced a prolonged allopatric divergence in separate glacial refugia, but persisted with interconnected populations across Southern and Central Europe. The generalist behaviour in host choice of I. ricinus would have played a major role in maintaining connections between its populations. Although most of the hosts persisted in separate refugia, from the point of view of I. ricinus, they represented a continuity of 'bridges' among populations. Our study highlights the importance of species-specific ecology in affecting responses to Pleistocene glacial-interglacial cycles. Together with other cases in Europe and elsewhere, it contributes to setting new hypotheses on how species with wide ecological plasticity coped with Pleistocene climatic changes.

1 Follower
18 Reads
  • Source
    • "The importance of adding genetic data in deciphering the taxonomy of fleas cannot be disputed and this approach has the added advantage of also providing novel insights into the evolutionary history of the species concerned (see, for example, Whiting, 2002; Luchetti et al., 2005, 2007; Whiting et al., 2008; Lawrence et al., 2014). Although cryptic divergence as a result of host vicariance has recently been implicated as a contributing factor towards diversification among generalist flea lineages (van der Mescht , Matthee & Matthee, 2015), most evolutionary studies to date show very limited or complex relationships between parasite and host genetic structures (Criscione, Poulin & Blouin, 2005; G omez-D ıaz et al., 2007; Barrett et al., 2008; Hoberg & Brooks, 2008; Nieberding et al., 2008; Cangi et al., 2013; Du Toit et al., 2013; Fermino et al., 2013; Porretta et al., 2013; Martin u et al., 2014). Given the wide host range, the previous description of two species (D. ellobius and D. abaris by Hopkins & Rothschild, 1966) based on a morphological character, and the potential effect of host and habitat vicariance on the evolution of fleas in the region, we predict that D. ellobius (as described by De Meillon et al., 1961; Segerman, 1995) may contain cryptic diversity in the region. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Dinopsyllus ellobius is considered a common and widespread flea in southern Africa and can act as a vector for plague. Due to differences in the interpretation of geographical variation in male sternite VIII, the taxonomy of the species is characterized by uncertainty. In an attempt to provide a better understanding of the systematics of D. ellobius, and also to provide new insights into the mechanisms that play a role in the diversification of the taxon, we sampled 830 small mammals at 31 localities throughout the distribution range of the parasite. Mitochondrial cytochrome c oxidase subunit II (COII) sequence data were generated for 151 D. ellobius specimens from 19 positive localities and this data set was supplemented with partial data derived from an elongation factor 1 alpha (EF1-a) intron. A parsimony haplotype network of the mtDNA and a Splitstree analyses revealed the existence of two genetic clades that were separated by 5.53% (� 1.78) sequence divergence. Although the nuclear DNA data were unresolved, significant size differences were detected between head, coxa, femur and tibia lengths of male individuals belonging to the two mtDNA lineages. The exact mechanisms that could have caused the diversification among lineages are not clear but the two lineages seem to be geographically separated and may have different ecological requirements. The present study strongly supports the notion that the two lineages are representative of D. ellobius (probably more associated with the host body and better adapted to mesic conditions) and Dinopsyllus abaris (probably more associated with the host nest and diverse climatic conditions) as originally proposed based on the single morphological character confined to male sternite VIII.
    Biological Journal of the Linnean Society 07/2015; 116(3). DOI:10.1111/bij.12615 · 2.26 Impact Factor
  • Source
    • "In the last decades advances in molecular techniques have greatly improved our tools to investigate the dynamics of vector populations and of pesticide resistance insurgence [43, 49–53]. More recently, next-generation sequencing technologies have offered unprecedented opportunities to investigate the molecular basis of the interaction between cellular defenses and insecticides [54]. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Background: Proteins from the ABC family (ATP-binding cassette) represent the largest known group of efflux pumps, responsible for transporting specific molecules across lipid membranes in both prokaryotic and eukaryotic organisms. In arthropods they have been shown to play a role in insecticide defense/resistance. The presence of ABC transporters and their possible association with insecticide transport have not yet been investigated in the mosquito Anopheles stephensi, the major vector of human malaria in the Middle East and South Asian regions. Here we investigated the presence and role of ABCs in transport of permethrin insecticide in a susceptible strain of this mosquito species. Methods: To identify ABC transporter genes we obtained a transcriptome from untreated larvae of An. stephensi and then compared it with the annotated transcriptome of Anopheles gambiae. To analyse the association between ABC transporters and permethrin we conducted bioassays with permethrin alone and in combination with an ABC inhibitor, and then we investigated expression profiles of the identified genes in larvae exposed to permethrin. Results: Bioassays showed an increased mortality of mosquitoes when permethrin was used in combination with the ABC-transporter inhibitor. Genes for ABC transporters were detected in the transcriptome, and five were selected (AnstABCB2, AnstABCB3, AnstABCB4, AnstABCmember6 and AnstABCG4). An increased expression in one of them (AnstABCG4) was observed in larvae exposed to the LD50 dose of permethrin. Contrary to what was found in other insect species, no up-regulation was observed in the AnstABCB genes. Conclusions: Our results show for the first time the involvement of ABC transporters in larval defense against permethrin in An. stephensi and, more in general, confirm the role of ABC transporters in insecticide defense. The differences observed with previous studies highlight the need of further research as, despite the growing number of studies on ABC transporters in insects, the heterogeneity of the results available at present does not allow us to infer general trends in ABC transporter-insecticide interactions.
    Parasites & Vectors 07/2014; 7(1):349. DOI:10.1186/1756-3305-7-349 · 3.43 Impact Factor
  • Source
    • "In some cases, the trade movements of livestock introduced and spread species far away from the original ranges [51]. We demonstrated that the covariates derived from the harmonic regression better captured the abiotic niche of several species of ticks than did the monthly raw set of descriptors or interpolated gridded climate, which have been traditionally used for this purpose [52-54]. We are aware that the nominal spatial resolution of 0.1° may be too coarse for some applications focusing on local or regional issues, which could require a higher resolution. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Background Correlative modelling combines observations of species occurrence with environmental variables to capture the niche of organisms. It has been argued for the use of predictors that are ecologically relevant to the target species, instead of the automatic selection of variables. Without such biological background, the forced inclusion of numerous variables can produce models that are highly inflated and biologically irrelevant. The tendency in correlative modelling is to use environmental variables that are interpolated from climate stations, or monthly estimates of remotely sensed features. Methods We produced a global dataset of abiotic variables based on the transformation by harmonic regression (time series Fourier transform) of monthly data derived from the MODIS series of satellites at a nominal resolution of 0.1°. The dataset includes variables, such as day and night temperature or vegetation and water availability, which potentially could affect physiological processes and therefore are surrogates in tracking the abiotic niche. We tested the capacities of the dataset to describe the abiotic niche of parasitic organisms, applying it to discriminate five species of the globally distributed tick subgenus Boophilus and using more than 9,500 published records. Results With an average reliability of 82%, the Fourier-transformed dataset outperformed the raw MODIS-derived monthly data for temperature and vegetation stress (62% of reliability) and other popular interpolated climate datasets, which had variable reliability (56%–65%). The transformed abiotic variables always had a collinearity of less than 3 (as measured by the variance inflation factor), in contrast with interpolated datasets, which had values as high as 300. Conclusions The new dataset of transformed covariates could address the tracking of abiotic niches without inflation of the models arising from internal issues with the descriptive variables, which appear when variance inflation is higher than 10. The coefficients of the harmonic regressions can also be used to reconstruct the complete original time series, being an adequate complement for ecological, epidemiological, or phylogenetic studies. We provide the dataset as a free download under the GNU general public license as well as the scripts necessary to integrate other time series of data into the calculations of the harmonic coefficients.
    Parasites & Vectors 07/2014; 7(1):302. DOI:10.1186/1756-3305-7-302 · 3.43 Impact Factor
Show more