Nuttalliella

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Nuttalliella
Temporal range: Cenomanian–Recent
Nuttalliella namaqua cropped.png
Scientific classification OOjs UI icon edit-ltr.svg
Kingdom: Animalia
Phylum: Arthropoda
Subphylum: Chelicerata
Class: Arachnida
Order: Ixodida
Family: Nuttalliellidae
Schulze, 1935  [1]
Genus: Nuttalliella
Bedford, 1931  [2]
Type species
Nuttalliella namaqua
Bedford, 1931
Fossil species
  • Nuttalliella gratae
  • Nuttalliella tuberculata
  • Nuttalliella placaventrala
  • Nuttalliella odyssea
  • Nuttalliella tropicasylvae

Nuttalliella is genus of tick. It contains a single living species, Nuttalliella namaqua found in southern Africa, having been reported from Tanzania, Namibia and South Africa, [3] with fossil species of the genus having been reported from the mid-Cretaceous (~100 million years ago) Burmese amber of Myanmar. [4] It is the only living member of the family Nuttalliellidae. [5] It can be distinguished from ixodid ticks and argasid ticks by a combination of characteristics including the position of the stigmata, lack of setae, strongly corrugated integument, and form of the fenestrated plates. [6] Known as a 'living fossil', it is the most basal lineage of extant ticks. [7] [8]

Contents

History of research

The first description by G.A.H. Bedford in 1931 was based upon a single female collected under a stone at Kamieskroon, in Little Namaqualand, by Dr R.F. Lawrence in October 1930. [9] The genus and family honours bacteriologist George Nuttall, a specialist in diseases transmitted by ticks, while the species is named for Little Namaqualand, the origin of the first specimen described. [9] [7] The species was recognised as distinctive enough to warrant its own family in two publications in 1935 and 1936. [4] As of 1980, only eighteen specimens had been collected. [7] In a 2011 study, that number was increased to fifty-one total specimens. They were collected in three locations in South Africa including two new sites: Springbok, Graaff-Reinet, and Heuningvleipan. [7]

Recently, fossil species described from Burmese amber have begun to clarify the basal phylogenies of early tick families. The specimens, dating to the mid-Cretaceous, around 100 million years ago, have included species in newly described genera Deinocroton, Khimaira and Legionaris, in addition to fossil Nuttalliella. [4]

Description and systematics

Nuttalliella, and the Nuttalliellidae more broadly, are regarded as the evolutionary 'link' between the hard ticks (Ixodidae) and the soft ticks (Argasidae). [7] Nuttalliella spp. possess a partly sclerotized pseudo-scutum and anterior, albeit short, mouthparts. In adults, the dorsal pseudoscutum appears like that of the Ixodidae, however the cuticle texture is not shell-like as in the hard ticks, rather it is a leathery, wrinkled surface, with elevations and pits as in the Argasidae. [10] [7] N. namaqua larvae possess true scuta, unlike the other life stages of the species; larvae also exhibit a dentate anal plate and pores on the legs, which are not seen in subsequent lifestages or in the Ixodidae or Argasidae. [11] Nuttalliella spp., like the Argasidae, can use their stomach as a storage organ for unmetabolised blood cells and haemoglobin. [12]

The Deinocrotonidae, formerly positioned as a sister family to the Nuttalliellidae, [13] [14] are now considered part of the Nuttalliellidae, as they share many of the unique morphological features of the family. [4] Namely, the shared pseudoscutum and hypostome features, but especially the 'ball-and-socket-like' leg joints common to Nuttalliella, Deinocroton and Legionaris species. [4] As such, there are currently four families in the order Ixodida.

Of modern tick lineages, Nutalliella is likely most related to the Ixodidae genus Ixodes , which, as the sole Prostriata genus, is known to be a basal lineage. [15] This relation was recognised by Bedford in the species' description, who noted the anterior anal groove and character of the pseudoscutum as most similar to Ixodes. [9] However, the nuttalliellids are no longer considered the last common ancestral lineage to the two primary modern tick families, the Ixodidae and Argasidae, following the discovery of the fossil species Khimaira fossus gen. et sp. nov. The newly recognised family, the Khimairidae, feature a much more distinct 'chimaeric fusion' of argasid and ixodid characters: a soft, integumented body together with a well-developed terminal gnathosoma and scutum. As such, the fossil family Khimairidae fam. nov. is now considered to be the last common ancestral lineage of the Argasidae and Ixodidae. [13]

Cladogram after Chitimia‐Dobler et al. 2022 and 2024: [13] [4]

Ixodida (ticks)

Distribution and ecology

Nuttalliella namaqua has been observed in southern Africa, including Botswana, Mozambique, [16] Namibia, Tanzania [17] and South Africa, [18] particularly the Karoo. [10] The species' usual habitat is xeric shrubland, often being found in rock crevices or on the ground. [7] [10]

N. namaqua is believed to have generalist host preferences, potentially weighted depending on life-stage [19] The species been collected from mammals, reptiles and birds' nests. [7] Genetic sequencing of blood found in N. namaqua show a wide diversity of lizard hosts. [19] Larvae may feed more commonly on murid rodents, [20] which is common to a number of African ixodid ticks. [21] Nymphs and adults may more readily parasitise lizards, including geckoes, skinks and particularly girdled lizards ( Karusasaurus and Cordylus spp.). [22] [19] Resolving the species life-cycle is challenging due to the elusive nature of the tick, in addition to the factor that the females feed rapidly, such that they are rarely found on-host. The species is also known from meerkats, hares and jackals, among others. [10]

Tick host preferences are fundamentally determined by ecological factors, and flexibility in host selection over time is an attribute of most tick lineages. [23] Given that Nuttalliella predate the origin of mammals, a generalist strategy of parasitism is likely a major driving force in the longevity of the species, which has seen the species adopt mammalian hosts as necessary. [19]

References

  1. Schulze-Rostock, P. (1935). "ZUR VERGLEICHENDEN ANATOMIE DER ZECKEN. (DAS STERNALE, DIE MUNDWERKZEUGE, ANALFURCHEN UND ANALBESCHILDERUNG, IHRE BEDEUTUNG, URSPR+£NGLICHKEIT UND LUXURIEREN)" [ON THE COMPARATIVE ANATOMY OF TICKS.]. Zeitschrift für Morphologie und Ökologie der Tiere (in German). 30 (1): 1–40. doi:10.1007/BF00418067. JSTOR   43261572. S2CID   28473817.
  2. G. A. H. Bedford (1931). "Nuttalliella namaqua, a new genus and species of tick". Parasitology . 23 (2): 230–232. doi:10.1017/S0031182000013573. S2CID   83785631.
  3. James E. Keirans; Carleton M. Clifford; Harry Hoogstraal; Emmett R. Easton (1976). "Discovery of Nuttalliella namaqua Bedford (Acarina: Ixodoidea: Nuttalliellidae) in Tanzania and redescription of the female based on scanning electron microcopy". Annals of the Entomological Society of America . 69 (5): 926–932. doi:10.1093/aesa/69.5.926.
  4. 1 2 3 4 5 6 Chitimia-Dobler, Lidia; Handschuh, Stephan; Dunlop, Jason A.; Pienaar, Ronel; Mans, Ben J. (2024-04-16). "Nuttalliellidae in Burmese amber: implications for tick evolution". Parasitology. 151 (9): 891–907. doi: 10.1017/S0031182024000477 . ISSN   0031-1820. PMC   11770530 . PMID   38623697.
  5. Alberto A. Guglielmone; Richard G. Robbins; Dmitry A. Apanaskevich; Trevor N. Petney; Agustín Estrada-Peña; Ivan G. Horak; Renfu Shao; Stephen C. Barker (2010). "The Argasidae, Ixodidae and Nuttalliellidae (Acari: Ixodida) of the world: a list of valid species names" (PDF). Zootaxa . 2528: 1–28. doi:10.11646/zootaxa.2528.1.1. hdl:11336/97869.
  6. Mohamed A. Roshdy; Harry Hoogstraal; Abdulelah A. Banaja; Samir M. El Shoura (1983). "Nuttalliella namaqua (Ixodoidea: Nuttalliellidae): spiracle structure and surface morphology". Parasitology Research . 69 (6): 817–821. doi:10.1007/BF00927431. S2CID   33872322.
  7. 1 2 3 4 5 6 7 8 Ben J. Mans; Daniel de Klerk; Ronel Pienaar & Abdalla A. Latif (2011). Oliveira, Pedro Lagerblad (ed.). "Nuttalliella namaqua: a living fossil and closest relative to the ancestral tick lineage: implications for the evolution of blood-feeding in ticks". PLoS ONE . 6 (8) e23675. Bibcode:2011PLoSO...623675M. doi: 10.1371/journal.pone.0023675 . PMC   3157464 . PMID   21858204.
  8. Mans, Ben J.; Klerk, Daniel de; Pienaar, Ronel; Latif, Abdalla A. (2011-08-17). "Nuttalliella namaqua: A Living Fossil and Closest Relative to the Ancestral Tick Lineage: Implications for the Evolution of Blood-Feeding in Ticks". PLOS ONE. 6 (8) e23675. Bibcode:2011PLoSO...623675M. doi: 10.1371/journal.pone.0023675 . ISSN   1932-6203. PMC   3157464 . PMID   21858204.
  9. 1 2 3 Bedford, G.A.H. (1931): "Nuttalliella namaqua, a new genus and species of tick". Parasitology23 (2): 230-232. doi : 10.1017/S0031182000013573
  10. 1 2 3 4 Ledwaba, Maphuti Betty; Malatji, Dikeledi Petunia (2024). "Nuttalliella namaqua Bedford, 1931, a sole extant species of the genus Nuttalliella - a scoping review". Frontiers in Parasitology. 3 1401351. doi: 10.3389/fpara.2024.1401351 . ISSN   2813-2424. PMC   11731621 . PMID   39817164.
  11. Latif, A. A., Putterill, J. F., de Klerk, D. G., Pienaar, R., and Mans, B. J. (2012). Nuttalliella namaqua (Ixodoidea: Nuttalliellidae): First description of the male, immature stages and re-description of the female. PloS One 7, e41651. doi: 10.1371/journal.pone.0041651
  12. Sonenshine, D. E., and Roe, R. M. (2014). Biology of Ticks Vol. 2 (Cambridge: Oxford University Press).
  13. 1 2 3 Chitimia-Dobler, Lidia; Mans, Ben J.; Handschuh, Stephan; Dunlop, Jason A. (2022). "A remarkable assemblage of ticks from mid-Cretaceous Burmese amber". Parasitology. 149 (6): 820–830. doi:10.1017/S0031182022000269. ISSN   0031-1820. PMC   10090602 . PMID   35241194.
  14. Peñalver E, Arillo A, Delclòs X, Peris D, Grimaldi DA, Anderson SR, Nascimbene PC and Pérez-de la Fuente R (2017) Ticks parasitized feathered dinosaurs as revealed by Cretaceous amber assemblages. Nature Communications 8, 1024.
  15. Nava, Santiago; Guglielmone, Alberto A.; Mangold, Atilio J. (2009-01-01). "An overview of systematics and evolution of ticks". Frontiers in Bioscience (Landmark Edition). 14 (8): 2857–2877. doi:10.2741/3418. ISSN   2768-6698. PMID   19273240.
  16. Apanaskevich, Dmitry A. (2021-01-15). "New larval host records and locality data for Nuttalliella namaqua Bedford, 1931 (Acari: Nuttalliellidae)" . Systematic and Applied Acarology: 317–319. doi:10.11158/saa.26.1.18. ISSN   2056-6069.
  17. Keirans, James E.; Clifford, Carleton M.; Hoogstraal, Harry; Easton, Emmett R. (1976-09-01). "Discovery of Nuttalliella namaqua Bedford (Acarina: Ixodoidea: Nuttalliellidae) in Tanzania and Redescription of the Female Based on Scanning Electron Microcopy1" . Annals of the Entomological Society of America. 69 (5): 926–932. doi:10.1093/aesa/69.5.926. ISSN   1938-2901.
  18. Stevens, L.; Stekolnikov, A. A.; Ueckermann, E. A.; Horak, I. G.; Matthee, S. (2022). "Diversity and distribution of ectoparasite taxa associated with Micaelamys namaquensis (Rodentia: Muridae), an opportunistic commensal rodent species in South Africa". Parasitology. 149 (9): 1229–1248. doi:10.1017/S0031182022000750. ISSN   0031-1820.
  19. 1 2 3 4 Mans, Ben J.; de Klerk, Daniel G.; Pienaar, Ronel; Latif, Abdalla A. (2013-09-21). "The host preferences of Nuttalliella namaqua (Ixodoidea: Nuttalliellidae): a generalist approach to surviving multiple host-switches". Experimental and Applied Acarology. 62 (2): 233–240. doi:10.1007/s10493-013-9737-z. hdl: 2263/33541 . PMID   24057095. S2CID   17797303.
  20. Horak, Ivan G.; Lutermann, Heike; Medger, Katarina; Apanaskevich, Dmitry A.; Matthee, Conrad A. (2012-02-02). "Natural hosts of the larvae of Nuttalliella sp. (N. namaqua?) (Acari: Nuttalliellidae)". The Onderstepoort Journal of Veterinary Research. 79 (1): E1–2. doi: 10.4102/ojvr.v79i1.405 . ISSN   2219-0635. PMID   23327328.
  21. Matthee, S.; Horak, I.G.; Mescht, L. van der; Ueckermann, E.A.; Radloff, F.G.T (2010). "Ectoparasite Diversity on Rodents at De Hoop Nature Reserve, Western Cape Province" . African Zoology. 45 (2): 213–224. doi:10.3377/004.045.0222. ISSN   1562-7020.
  22. El Shoura, S. M. (1991). Nuttalliella namaqua (Acarina: Ixodoidea: Nuttalliellidae) redescription of the female morphology in relation to the families Argasidae and Ixodidae. Acarologia 31, 349–355
  23. Klompen JS, Black WC 4th, Keirans JE, Oliver JH Jr (1996) Evolution of ticks. Annu Rev Entomol 41:141–161