Nuttalliella namaqua: a living fossil and closest relative to the ancestral tick lineage: implications for the evolution of blood-feeding in ticks

Abstract

Ticks are monophyletic and composed of the hard (Ixodidae) and soft (Argasidae) tick families, as well as the Nuttalliellidae, a family with a single species, Nuttalliella namaqua. Significant biological differences in lifestyle strategies for hard and soft ticks suggest that various blood-feeding adaptations occurred after their divergence. The phylogenetic relationships between the tick families have not yet been resolved due to the lack of molecular data for N. namaqua. This tick possesses a pseudo-scutum and apical gnathostoma as observed for ixodids, has a leathery cuticle similar to argasids and has been considered the evolutionary missing link between the two families. Little knowledge exists with regard to its feeding biology or host preferences. Data on its biology and systematic relationship to the other tick families could therefore be crucial in understanding the evolution of blood-feeding behaviour in ticks. Live specimens were collected and blood meal analysis showed the presence of DNA for girdled lizards from the Cordylid family. Feeding of ticks on lizards showed that engorgement occurred rapidly, similar to argasids, but that blood meal concentration occurs via malpighian excretion of water. Phylogenetic analysis of the 18S nuclear and 16S mitochondrial genes indicate that N. namaqua grouped basal to the main tick families. The data supports the monophyly of all tick families and suggests the evolution of argasid-like blood-feeding behaviour in the ancestral tick lineage. Based on the data and considerations from literature we propose an origin for ticks in the Karoo basin of Gondwanaland during the late Permian. The nuttalliellid family almost became extinct during the End Permian event, leaving N. namaqua as the closest living relative to the ancestral tick lineage and the evolutionary missing link between the tick families.

Figure 1. Localities where N. namaqua has been collected in southern Africa.

Biome data are indicated for Namibia , and South Africa and collection sites by black dots and names.

Figure 2. Collection and morphology of N. namaqua.

A) The crevice from which specimens were collected. B) A specimen concealed on a rock obtained from within the crevice. C) A dorsal view of an unfed female that shows the pseudo-scutum and ventral mouthparts. D) The same tick shown as an engorged female still attached to a lizard. E) Size range and general morphology of the collected live specimens. The black arrow indicates the tick selected for dissection from which lizard DNA was extracted. F) A dissected female with midgut that indicates it's recently fed status. G) A Giemsa stained smear obtained from the gut contents of the dissected female.

Figure 3. Phylogenetic analysis of the cordylid lizard family and sequences obtained from the gut content of N. namaqua.

Consensus sequences obtained from N. namaqua are indicated with black dots. Clades and genera are labelled according to Stanley et al. . Genbank accession numbers are indicated within brackets.

Figure 4. Bayesian analysis of the 18S rRNA gene for the parasitiformes.

Nodal support is indicated by posterior probability values. Genbank accession numbers are indicated in brackets.

Figure 5. Phylogenetic analysis of the concatenated 18S-16S rRNA dataset.

Indicated is the 50% majority consensus tree obtained with Bayesian as well as maximum parsimony analysis. Posterior probability and bootstrap support values are indicated above and below the nodes, respectively. Genbank accession numbers are indicated in brackets as 18S_16S.