Amblyomma cajennense (Fabricius, 1787) (Acari: Ixodidae), the Cayenne tick: phylogeography and evidence for allopatric speciation

Abstract

BackgroundAmblyomma cajennense F. is one of the best known and studied ticks in the New World because of its very wide distribution, its economical importance as pest of domestic ungulates, and its association with a variety of animal and human pathogens. Recent observations, however, have challenged the taxonomic status of this tick and indicated that intraspecific cryptic speciation might be occurring. In the present study, we investigate the evolutionary and demographic history of this tick and examine its genetic structure based on the analyses of three mitochondrial (12SrDNA, d-loop, and COII) and one nuclear (ITS2) genes. Because A. cajennense is characterized by a typical trans-Amazonian distribution, lineage divergence dating is also performed to establish whether genetic diversity can be linked to dated vicariant events which shaped the topology of the Neotropics.ResultsTotal evidence analyses of the concatenated mtDNA and nuclear + mtDNA datasets resulted in well-resolved and fully congruent reconstructions of the relationships within A. cajennense. The phylogenetic analyses consistently found A. cajennense to be monophyletic and to be separated into six genetic units defined by mutually exclusive haplotype compositions and habitat associations. Also, genetic divergence values showed that these lineages are as distinct from each other as recognized separate species of the same genus. The six clades are deeply split and node dating indicates that they started diverging in the middle-late Miocene.ConclusionsBehavioral differences and the results of laboratory cross-breeding experiments had already indicated that A. cajennense might be a complex of distinct taxonomic units. The combined and congruent mitochondrial and nuclear genetic evidence from this study reveals that A. cajennense is an assembly of six distinct species which have evolved separately from each other since at least 13.2 million years ago (Mya) in the earliest and 3.3 Mya in the latest lineages. The temporal and spatial diversification modes of the six lineages overlap the phylogeographical history of other organisms with similar extant trans-Amazonian distributions and are consistent with the present prevailing hypothesis that Neotropical diversity often finds its origins in the Miocene, after the Andean uplift changed the topology and consequently the climate and ecology of the Neotropics.

Amblyomma parvum Aragão, 1908 (Acari: Ixodidae): Phylogeography and systematic considerations

“…The tested calibrations were: outgroup node set to 15 + 4 million of years ago (Mya); A. cajennense -A. mixtum node set to 6 + 2 Mya; A. cajennense -A. mixtum -sculptum node set to 9 + 2 Mya. These calibrations corresponded to the estimated divergence dates within our outgroup taxa as previously reported (Beati et al, 2013).…”

“…Because the main lineages identified in this study, A. pseudoparvum, CA, and BA correspond roughly, in terms of geographical distribution, to clades identified within the A. cajennense species complex (Beati et al, 2013), we hypothesized that the evolution of the A. parvum group might have followed a similar phylogeographical temporal pattern. The decision of using only mitochondrial gene sequences was not only justified by the results of the partition homogeneity test, but also by the visible topological contrast observed between the ITS2 and the mitochondrial reconstructions, and by the fact that mitochondrial DNA, with its lower population size, putative neutrality, and elevated mutation rate, is considered to be a robust marker for developing hypotheses on population history and phylogeographical evolutionary patterns (Zink and Barrowclough, 2008).…”

“…FigTree v.1.4.2 was used to visualize tree topology, with mean divergence times and 95% confidence intervals. Node calibration was based on biogeographical information used in a recent publication on the biogeography of a closely related group of ticks, the A. cajennense complex (Beati et al, 2013). Species of that complex were purposely selected as outgroups in this study, because their previously evaluated divergence times can constitute additional calibration points for dating nodes within A. parvum.…”

“…Increasing evidence shows that tick species with wide geographic distributions may in fact be clusters of more or less cryptic species (Szabo et al, 2005;Labruna et al, 2009;Mastropaolo et al, 2011;Beati et al, 2013;Nava et al, 2014).…”

“…If samples from Brazil and Argentina are genetically different enough to suggest incipient speciation, samples from Central America are more likely to have diverged earlier and to constitute a different species. This would be particularly meaningful, if we consider that another tick taxon, Amblyomma cajennense Fabricius sensu lato, with a similar geographical distribution and also associated with relatively drier areas, was found to represent six different species, one of them with a distribution extending from southern Texas to Ecuador (Amblyomma mixtum Koch, 1844) and five confined to continental South America (Beati et al, 2013;Nava et al, 2014).…”