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Reproduction in a Metastriata Tick, Haemaphysalis Longicornis (Acari: Ixodidae)

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Reproduction in a Metastriata Tick, Haemaphysalis Longicornis (Acari: Ixodidae) J. Acarol. Soc. Jpn., 22(1): 1-23. May 25, 2013 © The Acarological Society of Japan http://www.acarology-japan.org/ 1 [REVIEW] Reproduction in a Metastriata Tick, Haemaphysalis longicornis (Acari: Ixodidae) 1 2 3 4 Tomohide MATSUO *, Nobuhiko OKURA , Hiroyuki KAKUDA and Yasuhiro YANO 1Laboratory of Parasitology, Department of Pathogenetic and Preventive Veterinary Science, Faculty of Agriculture, Kagoshima University, Kagoshima 890-0065, Japan 2Department of Anatomy, School of Medicine, University of the Ryukyu, Nishihara, Okinawa 903-0215, Japan 3Fukuoka Joyo High School, Chikushi 901, Chikushino, Fukuoka 818-0025, Japan 4Division of Immunology and Parasitology, Department of Pathological Sciences, Faculty of Medical Sciences, University of Fukui, Fukui 910-1193, Japan (Received 20 June 2012; Accepted 29 December 2012) ABSTRACT The superfamily Ixodoidea includes two major families: the Ixodidae called “hard tick” and Argasidae called “soft tick”. Furthermore, Ixodidae is classified into Prostriata (Ixodidae: Ixodes), and Metastriata (Ixodidae except for Ixodes) based on their reproductive strategies. That is, species in each group have characteristic reproductive organs and systems. Ticks are important as vectors of various pathogens. Haemaphysalis longicornis belonging to the Metastriata is characterized by having both the parthenogenetic and bisexual races, and is widely distributed in Australia, New Zealand, New Caledonia, the Fiji Islands, Japan, the Korean Peninsula and northeastern areas of both China and Russia. This species is known as a vector of rickettsiae causing Q fever, viruses causing Russian spring-summer encephalitis, and protozoa causing theileriosis and babesiosis. H. longicornis, the most dominant tick in Japanese pastures, is very important in agricultural and veterinary sciences because this species also transmits piroplasmosis caused by Theileria and Babesia parasites among grazing cattle. We present here an overview reproduction in the bisexual race of H. longicornis. Key words: Metastriata, tick, reproduction, bisexual race, vector INTRODUCTION A taxonomic group referred to as “tick” in the subclass Acari, which includes over 35,000 species (Oliver, 1989) is classified as Ixodoidea of the Metastigmata (Ixodida). The superfamily Ixodoidea includes two major families: the Ixodidae called “hard tick” and Argasidae called “soft * Corresponding author: e-mail: [email protected] DOI: 10.2300/acari.22.1 2 Tomohide MATSUO et al. tick”. A third family Nuttalliellidae is minor and consists of only a single species for which reproductive strategies are unknown. Furthermore, Ixodidae is classified into Prostriata (Ixodidae: Ixodes) and Metastriata (Ixodidae except for Ixodes) based on their reproductive strategies. It is known that the valid genus and species names of ticks are more than 850 (Baker and Murrell, 2004; Guglielmone et al., 2009). Ticks cause severe toxic conditions, e.g. tick paralysis, various tick toxicoses, irritation, tick bite allergies, immune responses and economic losses due to blood sucking (Sonenshine, 1991). Haemaphysalis longicornis Neumann, 1901 belonging to the Metastriata is widely distributed in Australia, New Zealand, New Caledonia, the Fiji Islands, Japan, the Korean Peninsula and northeastern areas of both China and Russia. This species is known as a vector of the rickettsiae causing Q fever, viruses causing Russian spring-summer encephalitis, and protozoa causing theileriosis and babesiosis, respectively (Hoogstraal et al., 1968). H. longicornis is the most dominant tick in Japanese pastures and transmits piroplasmosis by Theileria sergenti / buffeli / orientalis group (Fujisaki, 1992; Fujisaki et al., 1994) and Babesia ovata among grazing cattle (Ishihara 1968). Additionally, reproduction of H. longicornis is very interesting because the species includes both pathenogenetic and bisexual races (Kitaoka, 1961). Our research group has studied reproduction in the bisexual race for more than 10 years. Recently, numerous studies on vector ticks have reported and elucidated roles of reproduction in the transmission of pathogens such as the transovarial transmission of protozoans. Therefore, studies on the reproduction of this species need to be summarized in order to not only understand their life cycles for control but also to assist in investigations on the relationship between ticks and pathogens. Therefore, in this review we describe reproduction in the bisexual race of H. longicornis in hopes the information will assist the progress of research on ticks as vectors of various pathogens. MALE REPRODUCTION Reproduction in male H. longicornis is described: 1) the development of the testes during feeding (Matsuo et al., 1997a) and 2) the turnover of the spermatogenic cells (Matsuo and Mori, 2000), 3) the external shape and histological changes of the male accessory genital glands during a feeding (Matsuo and Mori, 2000; Matsuo et al., 1997b) and after a copulation (Matsuo, 2000), 4) ultrastructure of the spermatophore which play an important role in the transfer of male germ cells from a male to a female and action of the spermatophore in vitro (Matsuo et al., 1998) and 5) the derivation of the spermatophore components from the accessory glands (Matsuo, 2000; Matsuo et al., 1997b). 1) Testes and Spermatogenesis The adult male H. longicornis has a paired tubular testes similar to other ticks, and the testes increased approximately twice in length and five times in thickness during feeding (Fig. 1). The testes are fused posteriorly (Argasidae), broadly joined (most Prostriata), or connected only by an extremely thin filamentous strand of tissue (Metastriata) (Oliver, 1982). At each feeding stage the testes contain spermatogenic cells in various stages of spermatogenesis with more advanced spermatogenesis in the posterior region of the testes than the anterior region connected to the vas deferens. The spermatogenic cells are arranged in reverse order as usually found in the tubular Reproduction in Haemaphysalis longicornis 3 testes of most invertebrates (Oliver, 1982). Spermatogonia and early primary spermatocytes are contained in the anterior region of the testes of unfed males, and slightly enlarged primary spermatocytes in the posterior region. Spermatogonia, primary spermatocytes during their growth phase, and early spermatids just after maturation division are found in the testes of 3-day fed males. Spermatogenesis is completed within the testes, and spermatogenic cells at all stages from spermatogonia to elongated spermatids were contained in the testes of completely (5-day) fed males. Furthermore, the spermatogenic cells are packed in cysts composed of cyst cells as seen in other ticks (Oliver, 1982) (Fig. 1). Cysts arranged radially form the central lumen as a passage extending the length of testes for elongated spermatids to move to the vas deferens. The cyst cells face the lumen and contain microvilli, so are also called ‘nutritive cells’ (Reger, 1961) or ‘interstitial cells’ (Raikhel, 1983). The development of all cells within a particular cyst is synchronous, and the number of spermatogenic cells appears to be species specific (Khalil, 1969, 1970). Spermatogonia and early primary spermatocytes are contained in the anterior part of the testes of unfed males. These cells are small and have a large nucleus. Polysomes and mitochondria are found in the cytoplasm, and intercellular bridges have already formed. Subsequently, the main growth phase of primary spermatocytes has begun, and these cells gradually increase in size. The polysomes disappear and the Golgi complex emerges in the primary spermatocytes after the beginning of this phase. The subplasmalemmal cisternae (SC) that become cellular processes on the surface of spermatozoa begin to be formed, and are also called ‘subsurface cisternae’ (Reger, 1962) or ‘cortical alveoli’ (Raikhel, 1983). Although the origin of the SC is uncertain, the endoplasmic reticulum (Reger, 1961, 1962, 1963), Golgi complex (Reger, 1974) and plasma membrane (Oliver and Brinton, 1972; Suleiman and Brown, 1978) are suggested as origins. In H. longicornis, the timing of the emergence and disappearance of the Golgi complex is synchronized with the addition of SC initiation and completion. Therefore, we conclude the SC originates from the Golgi complex. The size of the cells reduced by meiosis after the main growth phase is completed at this time. Early spermatids that formed the largest SC are found immediately after the reduction in size. Thereafter, the cells in which the relocation of the nucleus and SC, and the formation of the cisternal cavity have occurred are early rounded spermatids. However, the second reduction of cell size is also observed as reduction in area of sections with a change in shape during the formation of the cisternal cavity in H. longicornis. Oliver (1982) also indicated that the spermatogenic cell where the nucleus is located centrally and the periphery remains surrounded by a cup-shaped SC is the early spermatid. These cells in which the cisternal cavity has formed begin to elongate, and finally the elongated spermatids or prospermia (Till, 1961) consisting of an outer sheath and inner cord are completed. The cellular processes originating from the SC are arranged on the outer surface of the inner cord and the inner surface of the outer sheath. Detailed studies on tick spermatogenesis have particularly observed the structure of the elongated spermatids, cellular processes called ‘motile processes’, and the
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