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Sperm Structure in Parasitidae Mites (Parasitiformes: Mesostigmata: Gamasina)

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Sperm Structure in Parasitidae Mites (Parasitiformes: Mesostigmata: Gamasina) Acarologia A quarterly journal of acarology, since 1959 Publishing on all aspects of the Acari All information: http://www1.montpellier.inra.fr/CBGP/acarologia/ [email protected] Acarologia is proudly non-profit, with no page charges and free open access Please help us maintain this system by encouraging your institutes to subscribe to the print version of the journal and by sending us your high quality research on the Acari. Subscriptions: Year 2020 (Volume 60): 450 € http://www1.montpellier.inra.fr/CBGP/acarologia/subscribe.php Previous volumes (2010-2018): 250 € / year (4 issues) Acarologia, CBGP, CS 30016, 34988 MONTFERRIER-sur-LEZ Cedex, France ISSN 0044-586X (print), ISSN 2107-7207 (electronic) The digitalization of Acarologia papers prior to 2000 was supported by Agropolis Fondation under the reference ID 1500-024 through the « Investissements d’avenir » programme (Labex Agro: ANR-10-LABX-0001-01) Acarologia is under free license and distributed under the terms of the Creative Commons-BY-NC-ND which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original author and source are credited. Acarologia 56(1):3–32 (2016) DOI: 10.1051/acarologia/20162190 Sperm structure in Parasitidae mites (Parasitiformes: Mesostigmata: Gamasina) Wojciech WITALINSKI´ * and Dagmara PODKOWA (Received 22 September 2015; accepted 29 October 2015; published online 07 March 2016) Department of Comparative Anatomy, Institute of Zoology, Jagiellonian University, Gronostajowa 9, 30-387 Kraków, Poland. [email protected] (*Corresponding author); [email protected]. ABSTRACT — This contribution reviews the ultrastructure of ribbon-type sperm in 14 genera of both subfamilies (7 in Pergamasinae and 7 in Parasitinae) of the Parasitidae family (Parasitiformes: Mesostigmata: Gamasina); in total 27 species were considered, of which sperm ultrastructure was studied for the first time in 17 species and 9 genera. We found a wide range of sperm dimensions and nucleus lengths, but basic external and internal structures were substantially constant across genera. Spermatozoa are rod- or club-shaped cells with an elongated nucleus. The chromatin granules are focused in the middle zone of the nucleus. The cytoplasm around the nucleus and in the adjoining postnuclear region is filled with inclusion bodies with striated content (striated inclusion bodies, sIBs), whereas in the distant postnuclear region they are replaced by larger granular inclusion bodies (gIBs) usually containing a striated core surrounded by granular material. Mitochondria are distributed mostly subplasmalemmally in the nuclear region and between gIBs in the postnuclear region of the sperm cell. The most variable feature of the spermatozoa is the number of compound longitudinal ribbons of plasmalemmal origin alternating with subplasmalemmal cisterns: 9 (Leptogamasus anoxygenellus) to 21 (Pergamasus barbarus) in Pergamasinae and 5 (Parasitus berlesei and Paracarpais loricatus) to 30 (Paracarpais lunulata) in Parasitinae. In general, ribbons are electron-dense in the nuclear region but more lucent in the postnuclear region. The variation in sperm structure was not reflected in the taxonomic arrangement of genera and subfamilies within Parasitidae, but it must be emphasized that the taxonomy of Parasitidae is still awaiting a comprehensive modern revision. KEYWORDS — mites; spermatozoa morphology; variability; ultrastructure; taxonomy INTRODUCTION second pair of legs to fix ventrally to the female, firmly holding her last legs of the 4th pair. Then, Parasitid mites, despite their name, are predomi- the male produces a sac-like spermatophore from nantly free-living and predatory inhabitants of hu- the genital opening located at the anterior mar- mid litter and decaying matter, feeding on imma- gin of the sternum and by manipulating the che- ture stages and eggs of microhexapods, as well as licerae it transfers the spermatophore into the fe- small soil oligochaets and nematodes (Micherdz- male genital opening located in a mid-ventral po- i´nski1969; Tichomirov 1977; Hyatt 1980; Karg 1993; sition. This mode of insemination was termed to- Blackman 1997; Szafranek et al. 2013). Males and cospermy by Athias-Henriot and later specified as females are usually equally represented in collected neotocospermy by Alberti (Athias-Henriot 1968; Al- material. During mating, the male uses its enlarged berti 2002). Parasitid spermatozoa (Figures 1, 2) http://www1.montpellier.inra.fr/CBGP/acarologia/ 3 ISSN 0044-586-X (print). ISSN 2107-7207 (electronic) Witali´nskiW. and Podkowa D. FIGURE 1: General organisation of parasitid spermatozoon (left) showing superficial and internal organization, as well as spermatozoon internal structure (right) as shown on cross sections through nuclear, postnuclear and posterior regions (based on Witali´nski1975). Abbreviations: ca – canaliculus running in longitudinal crest, ch – chromatin, cr – longitudinally running crest, gIB – granular inclu- sion body, m – mitochondrion, n – nucleus, rb – subplasmalemmal longitudinal ribbon, sc – subplasmalemmal cistern, sIB – striated inclusion body 4 Acarologia 56(1):3–32 (2016) FIGURE 2: Schematic drawings of Parasitidae spermatozoa with outlined nucleus and anterior tip upwards. Abbreviations: Acs – Aclerogamasus similis, Ant – Anidogamasus teutonicus, Cl – Cornigamasus lunaris (asterisk marks anterior end), Gs – Gamasodes spiniger, Hc – Holoparasitus calcaratus, La – Leptogamasus anoxygenellus, Pac – Parasitus coleoptratorum, Pck – Paracarpais kraepelini, Pclo – Paracarpais loricatus, Pclu – Paracarpais lunulata, Pem – Pergamasus mediocris (sperm of P. barbarus, P. brevicornis and P. crassipes have similar proportions), Phf – Phorytocarpais fimetorum, Psp – Paragamasus sp., Tsp – Trachygamasus sp. 5 Witali´nskiW. and Podkowa D. were observed as early as the 19th century (Win- subgenera elevated to the genus level mainly due kler 1888; Michael 1892). They are easily recog- to the contributions of Athias-Henriot and Juvara- nizable due to their club- or rod-shape appearance Bals (e.g. Athias-Henriot 1969; Juvara-Bals 1972, and unusual, very characteristic internal structure 1977; Juvara-Bals and Athias-Henriot 1972; Athias- occasionally observable under a light microscope Henriot 1979, 1980, 1981) are still not accepted as (Sokolov 1934), but obviously better illustrated genera by some acarologists preferring the more using a transmission electron microscope (TEM). simple "traditional" taxonomy as presented in e.g. They are classified as ribbon-type spermatozoa (Al- Bhattacharyya 1963, Micherdzi´nski 1969, Holz- berti 1980) since there are complicated systems of mann 1969, Karg 1971, 1993, Evans and Till 1979, plasmalemmal infoldings forming so-called ribbons and Hyatt 1980. For example, three species recently which are double rows of saccular structures run- included in Paracarpais (P. loricatus, P. kraepelini and ning longitudinally along the spermatozoon from P. lunulata) are still traditionally located in different its anterior to posterior end (Sokolov 1934; Wital- genera (Parasitus loricatus, Vulgarogamasus kraepelini i´nski1975, 1976, 1979). The plasmalemma above and Porrhostaspis lunulata). Furthermore, the phylo- each ribbon evaginates forming a longitudinal ridge genetic relationships within Parasitidae, even at the or crest containing the canaliculus. Electron-dense generic level, were never tested with modern phy- subplasmalemmal cisterns run longitudinally along logenetic methods. Since it is commonly accepted and between ribbons. The sperm nucleus is elon- that the structure of spermatozoa can provide a new gated and occupies more or less half of the length set of characters useful for phylogenetic considera- of the spermatozoon. The nucleus-containing part tions (e.g. Afzelius 1979; Baccetti 1979; Wirth 1984; is considered to be the anterior one, but for con- Jamieson 1987), the aim of our paper was to review venience rather than due to any physiological (e.g. the main modifications in sperm structure in 27 rep- movement) evidence. Around and just behind the resentatives of 14 parasitid mite genera (7 in Perga- nucleus there are many inclusion bodies with a masinae and 7 in Parasitinae), in 17 species and 9 characteristic, striated appearance (striated inclu- genera for the first time at the ultrastructural level. sion bodies, sIBs). The posterior part of the cell It could also trace some evolutionary routes within contains larger, granular inclusion bodies (gIBs) family. On the other hand, future molecular taxo- which are apparently derived from the striated nomic studies could be used to track general trends ones (Witali´nski1975). Crista-type mitochondria in sperm evolution within Parasitidae and, possibly, are usually located between ribbons below subplas- to allow a better understanding of the complicated malemmal cisterns in the nuclear region, but in the sperm structures in the light of their function. postnuclear region they are scattered between gIBs. Typical acrosome, flagellum, axoneme and centri- oles have never been observed in parasitid sperm; MATERIALS AND METHODS an acrosomal vesicle reported in Pergamasus sperm (Witali´nski1975) is a result of misinterpretation. We considered sperm structure in 27 species (Table 1) of parasitid mites from both subfamilies, Perga- The Parasitidae is one of the most species-rich masinae (16 species from 7 genera) and Parasiti- families of mesostigmatic mites comprising at least nae (11 species from 7 genera). Free-living
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