The Mitochondrial Genomes of Nuttalliella namaqua (Ixodoidea: Nuttalliellidae) and Argas africolumbae (Ixodoidae: Argasidae): Estimation of Divergence Dates for the Major Tick Lineages and Reconstruction of Ancestral Blood-Feeding Characters

Abstract

Ixodida are composed of hard (Ixodidae), soft (Argasidae) and the monotypic Nuttalliellidae (Nuttalliella namaqua) tick families. Nuclear 18S rRNA analysis suggested that N. namaqua was the closest extant relative to the last common ancestral tick lineage. The mitochondrial genomes of N. namaqua and Argas africolumbae were determined using next generation sequencing and de novo assembly to investigate this further. The latter was included since previous estimates on the divergence times of argasids lacked data for this major genus. Mitochondrial gene order for both was identical to that of the Argasidae and Prostriata. Bayesian analysis of the COI, Cytb, ND1, ND2 and ND4 genes confirmed the monophyly of ticks, the basal position of N. namaqua to the other tick families and the accepted systematic relationships of the other tick genera. Molecular clock estimates were derived for the divergence of the major tick lineages and supported previous estimates on the origins of ticks in the Carboniferous. N. namaqua larvae fed successfully on lizards and mice in a prolonged manner similar to many argasids and all ixodids. Excess blood meal-derived water was secreted via the salivary glands, similar to ixodids. We propose that this prolonged larval feeding style eventually gave rise to the long feeding periods that typify the single larval, nymphal and adult stages of ixodid ticks and the associated secretion of water via the salivary glands. Ancestral reconstruction of characters involved in blood-feeding indicates that most of the characteristics unique to either hard or soft tick families were present in the ancestral tick lineage.

The host preferences of Nuttalliella namaqua (Ixodoidea: Nuttalliellidae): a generalist approach to surviving multiple host-switches

“…If eggs were laid in these environments, larvae would probably parasitize lizards. Even so, reports of larvae feeding on mice were reported even though it is not clear what the prevalence is on mice in general (Horak et al 2012;Mans et al 2012). It is furthermore intriguing that a number of females were found on burrowing mammals, such as meerkat and Brant's Karoo rat (Keirans et al 1976), given that females feed fast (Mans et al 2011).…”

“…Given the molecular clock age estimations for the Nuttalliella genus (>280 MYA) it would be clear that this genus fed on reptiles long before the origin of mammals (Mans et al 2011;Mans et al 2012). It is therefore likely that the host preference of N. namaqua changed over temporal time so that extant mammals and lizards would be current preferred hosts.…”

“…In contrast, numerous larval ticks were found on a variety of small murid rodents (Micaelamys namaquensis, Aethomys chrysophilus and Acomys spinosissimus), suggesting that these were the natural hosts of larval N. namaqua (Horak et al 2012). Larvae could also be successfully fed on both mice and lizards and moulted to nymphs Mans et al 2012). The question was raised whether the female analysed in the previous study (Mans et al 2011), could have incidentally fed on a lizard and that reptiles would not be natural hosts for female ticks, even if successful feeding could be completed in the laboratory.…”

Tick attachment cement – reviewing the mysteries of a biological skin plug system

“…There are no reports of cement production in Nuttalliella namaqua Bedford, 1931, the single species in the family Nuttalliellidae (Mans et al ., 2012). The presence of cement seems to be related to different tick feeding habits; nymphs and females of Nuttalliella namaqua (Mans et al ., 2011) and most life stages in the Argasidae complete their blood meal within minutes to hours (Oliver, 1989; Apanaskevich & Oliver, 2014) and therefore may not need additional anchorage.…”

“…Furthermore, the Argasidae enter the host skin deeply (Sauer et al ., 1995) with well‐developed mouthparts (Binnington & Kemp, 1980) and usually become active when their host animals are resting or sleeping in their nests or burrows (Oliver, 1989), perhaps making cement production unnecessary. Exceptions might be found in larval stages of some genera in Argasidae and the larvae of Nuttalliella namaqua (Mans et al ., 2012) , which take blood meals over several days (Oliver, 1989; Mans et al ., 2012; Apanaskevich & Oliver, 2014). However, to date, cement has only been reported for feeding larvae of Argas pusillus Kohls, 1950 (Stiller & Ranchitham, 1975), although this observation is not undisputed (Kemp et al ., 1982).…”