The embryogenesis of the Tick Rhipicephalus (Boophilus) microplus: The establishment of a new chelicerate model system

Abstract

Chelicerates, which include spiders, ticks, mites, scorpions, and horseshoe crabs, are members of the phylum Arthropoda. In recent years, several molecular experimental studies of chelicerates have examined the embryology of spiders; however, the embryology of other groups, such as ticks (Acari: Parasitiformes), has been largely neglected. Ticks and mites are believed to constitute a monophyletic group, the Acari. Due to their blood-sucking activities, ticks are also known to be vectors of several diseases. In this study, we analyzed the embryonic development of the cattle tick, Rhipicephalus (Boophilus) microplus (Acari: Ixodidae). First, we developed an embryonic staging system consisting of 14 embryonic stages. Second, histological analysis and antibody staining unexpectedly revealed the presence of a population of tick cells with similar characteristics to the spider cumulus. Cumulus cell populations also exist in other chelicerates; these cells are responsible for the breaking of radial symmetry through bone morphogenetic protein signaling. Third, it was determined that the posterior (opisthosomal) embryonic region of R. microplus is segmented. Finally, we identified the presence of a transient ventral midline furrow and the formation and regression of a fourth leg pair; these features may be regarded as hallmarks of late tick embryogenesis. Importantly, most of the aforementioned features are absent from mite embryos, suggesting that mites and ticks do not constitute a monophyletic group or that mites have lost these features. Taken together, our findings provide fundamental common ground for improving knowledge regarding tick embryonic development, thereby facilitating the establishment of a new chelicerate model system.

Ancestral reconstruction of tick lineages

“…In the Acari, the mouthparts are beared by the capitulum, while the prosoma and opisthosoma are fused into a non-segmented idiosoma . However, segmentation in embryos, body pattern of setae, fissures, folds and festoons, support a more ancient arthropod segmentation plan in ticks (Klompen et al 2015(Klompen et al , 1996bSantos et al 2013). Further, opisthosomal segmentation during the germ band stage is observed in ticks (and other Parasitiformes?…”

Chelicerata

“…However, Itow et al claim that the posterior cumulus (i.e., the structure most likely homologous to the spider cumulus) has no effect on axis formation in the horseshoe crab (Itow 1990 ;Itow et al 1991 ). Migrating cumuli have also been noted in Amblypygi (Weygoldt 1975 ), Opiliones (Holm 1947 ;Juberthie 1964 ), possibly in a solifuge (Heymons 1904 ;Holm 1947 ) and most recently in a tick (Santos et al 2013b ). The cumulus has therefore been suggested as belonging to the ground pattern in Chelicerata (Hilbrant et al 2012 ).…”

“…This has allowed comparisons of the sequences of important developmental genes to be made between this tick and other metazoans (e.g., Janssen et al 2010 ). Furthermore, embryonic development has been described for Rhipicephalus ( Boophilus ) microplus , which involved using antibody stainings (Santos et al 2013b ). However, gene expression and function during tick development has not been studied to the best of our knowledge, although reports of the successful application of parental RNAi (e.g., la Fuente et al 2007 ) might change this in the future.…”

“…The initial germ anlage commonly forms all prosomal segments (pre-cheliceral lobe, cheliceral, pedipalpal, and the four walking leg segmentsPl, Ch, Pp, L1-L4), and a differing number of opisthosomal segments are added sequentially segmentation is found in spiders, harvestmen (Juberthie 1964 ), whip scorpions (Anderson 1973 ), Amblypygi (Weygoldt 1975 ), ticks (Anderson 1973 ;Santos et al 2013b ), and pseudoscorpions (Yoshikura 1975 ). However, horseshoe crabs, scorpions and pycnogonids form only pre-cheliceral lobes and cheliceral and pedipalpal segments as well as a SAZ from their embryonic primordium, while walking leg segments and opisthosomal segments are then sequentially added from the SAZ (Anderson 1973 ;Itow and Sekiguchi 1980 ;Farley 2001 ;Brenneis et al 2011b ).…”

Post-embryonic development in the mite suborder Opilioacarida, with notes on segmental homology in Parasitiformes (Arachnida)

“…Wolff and Hilbrant 2011), and it is unclear whether the above study followed embryogenesis until hatching. In this context, it is worth noting that molecular embryology of the tick Rhipicephalus (Boophilus) microplus (Canestrini) showed indicators of at least eight opisthosomal segments based on DAPI and antennapedia (Antp) antibody staining (Santos et al 2013). Redrawn and modified from Klompen et al (1996).…”