Arthropod
Structure
&
Development
43
(2014)
323e340
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Journal logo Review article Gonads and gametogenesis in astigmatic mites (Acariformes: Astigmata) Wojciech Witalinski*
Department of Comparative Anatomy, Institute of Zoology, Jagiellonian University, Gronostajowa 9, 30-387 Krak, Poland article info abstract Article history: Received 13 February 2014 Received in revised form 7 April 2014 Accepted 9 April 2014 Keywords: Ovarian nutritive cell Testicular central cell Intercellular bridges Ovary Oogenesis Vitellogenesis Testis Spermatogenesis Spermatozoa Gonadal somatic cells Astigmatans are a large group of mites living in nearly every environment and exhibiting very diverse reproductive strategies. In spite of an uniform anatomical organization of their reproductive systems, gametogenesis in each sex is highly variable, leading to gamete formation showing many peculiar features and emphasizing the distinct position of Astigmata. This review summarizes the contemporary knowledge on the structure of ovaries and testes in astigmatic mites, the peculiarities of oogenesis and spermatogenesis, as well as provides new data on several species not studied previously. New questions are discussed and approaches for future studies are proposed. 2014 The Author. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/3.0/). 1. Introduction 1.1. Systematics of Astigmata Mites (incl. ticks) consist of a large group of chelicerate arthropods comprising more than 55 000 described species, however, acarologists estimate that many times this number have yet to be described (Walter
and
Proctor,
1999;
Krantz,
2009). In the last de-cades mites (Acari) were considered to be a natural taxon; however, diphyly has also been postulated (Zakhvatkin,
1952;
Van
der
Hammen,
1977,
1979,
1989). Quite recently, a molecular study on the phylogeny of Acari again strongly supported its diphyletic origin (Dabert
et
al.,
2010). Consequently, there are two independent branches (superorders): Parasitiformes (¼Anactinotrichida) and Acariformes (¼Actinotrichida). The latter originated at least in the Early Devonian (Hirst,
1923;
Norton
et
al.,
1988;
Bernini,
1991) and comprises four taxa: the Trombidiformes (order), the Endeostigmata (suborder), the Oribatida (suborder), and the cohort Astigmata (¼ Astigmatina, Acaridida)
(Lindquist
et
al.,
2009). Astigmata is considered a natural group and most likely derived from an early clade (infraorder, acc. to Schatz
et
al.,
2011) of Oribatida, the Desmonomata (OConnor,
1984;
Norton,
1998). * Tel.: þ48 12 664 5047. E-mail address: w.witalinski@gmail.com. As currently recognized (OConnor,
2009), the astigmatic lineage diversiﬁed into 10 superfamilies, 71 families comprising 960 genera and more than 6100 described species (Klimov
and
OConnor,
2013). At present, even at a high taxonomic level the suggested phylogenetic relationships are based on traditional morphological analyses rather than molecular studies, with the exception of a recent molecular study by Klimov
and
OConnor
(2013). A provisional but still temporarily accepted cladogram is presented in Fig. 1 by OConnor
(2009), adopted from earlier work (Norton
et
al.,
1993). It shows the phylogenetic relationships of Astigmata superfamilies and combines Pterolichoidea, Analgoidea and Sarcoptoidea into a monophyletic group Psoroptidia with ca. 3800 species (OConnor,
1982;
Klimov
and
OConnor,
2008), although the composition of Pterolichoidea and Analgoidea is somewhat disputable (for details see: Proctor,
2003). 1.2. Environment of Astigmata Although astigmatan free-living mites are abundant in wet litter and soil, especially in highly decomposed material, they often are the dominant mite group in patchy or ephemeral habitats. They are numerous in decaying organic matter, dung, carrion, sap ﬂows, dry http://dx.doi.org/10.1016/j.asd.2014.04.003
1467-8039/ 2014 The Author. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/3.0/). W. Witalinski / Arthropod Structure & Development 43 (2014) 323e340 Image of Fig. 1 and water-ﬁlled tree holes, phytotelmata and caves (Hughes,
1976;
Evans,
1992;
Fashing,
1994,
1998). The other species are successful in destroying stored food such as cereals, ﬂour, cheese, dried fruits and meat, etc., leading to considerable crop damage (Hughes,
1976). An abundance of Astigmata is associated with other animals, mainly insects and amniotic vertebrates (e.g. all Psoroptidia with the exception of Pyroglyphidae which are free-living), frequently as serious dermicolous parasites (Fain
and
Lukoschus,
1986;
Proctor,
2003;
OConnor,
2009). They can also inhabit bird and mamma-lian nests or such distinct habitat as feathers. Despite a wide range of habitats and a successful adaptive radiation, these mites share many distinct features in reproductive anatomy and reproductive behavior. 2. Materials and methods In this review, original results were obtained through routine transmission electron microscopy (TEM) with a procedure sum-marized as follows. The sex of studied mite species (Histiostomatidae: Histiostoma feroniarum Dufour, Canestriniidae: Canestrinia sellnicki (Samsinák), Carpoglyphidae: Carpoglyphus lactis L., Chaetodactylidae: Chaetodactylus osmiae (Dufour), Glycyphagidae: Glycyphagus domesticus (De Geer), Falculiferidae: Falculifer rostratus (Buhcholz), Sarcoptidae: Notoedres cati Hering, Analgidae: Diplae-gidia columbae (Buhcholz), Proctophyllodidae: Proctophyllodes fuchsi Mironov, Pyroglyphidae: Dermatophagoides farinae Hughes) (Fig.
1) was identiﬁed under a Nikon SMZ1000 stereomicroscope (Nikon Instruments Europe, Amsterdam, Netherlands). After im-mersion into a droplet of Karnovsky’s ﬁxative (Karnovsky,
1965) (mixture containing 2% formaldehyde and 2.5% glutaraldehyde in 0.1 M cacodylate buffer, pH 7.2) on a Paraﬁlm-coated microscopic slide, the anterior part of the body was cut off with a ﬁne razor blade and the remaining rear part was transferred into fresh ﬁxative for 24 h at 4 C. Fixed material was rinsed 4 15 min in 0.1 M cacodylate buffer containing 8% sucrose and postﬁxed with 1.4% osmium tetroxide in 8% sucrose overnight at 4 C. The specimens were then washed and dehydrated in a graded ethanol series fol-lowed by propylene oxide and embedded in Epon 812 substitute (SigmaeAldrich). Semithin cross sections were stained with an Azur II and methylene blue (1:1) mixture, whereas thin sections were collected on formvar coated grids, contrasted with uranyl acetate and lead citrate according to standard protocols (Venable
and
Coggeshall,
1965), and examined under a transmission electron microscope JEOL JEM 100SX (JEOL Ltd., Tokyo, Japan) at 80 kV in the Department of Cell Biology and Imaging, Institute of Zoology, Jagiellonian University. For ﬂuorescent staining with DAPI and Pyronin Y, the females of Rhizoglyphus echinopus were processed as follows: the posterior parts of mite bodies were ﬁxedfor2hat4 Cin ﬁxative containing 4% paraformaldehyde and 2.5% sucrose in 0.01 M PBS. After ﬁxation, the material was washed and dehydrated in a graded ethanol series then embedded in LR-White (Fluka) resin. Semithin sections were stained 30 min with DAPI, washed several seconds in PBS, and stained 20 min with Pyronin Y (SigmaeAldrich)(20 mg/ml). After brief washing in PBS sections were mounted and examined under a ﬂuorescence microscope Olympus BX51 (Olympus Corporation, Tokyo, Japan) ﬁtted with appropriate ﬁlters. 3. Reproduction of Astigmata Both sexual and parthenogenetic species occur in Astigmata, the latter represented by arrhenotokous, thelytokous, and rare deuterotokous organisms. In species possessing both females and males (sexual and arrhenotokous species) the proportion of sexes may be only slightly biased towards females. The males use their intromittent organ, the aedeagus (¼penis) to inseminate females with sperm during copulation. Insemination never occurs through the oviporus, but via a supplementary inseminatory system. Sexual species (with diploid females and diploid males) occur for instance in Acaroidea and Glycyphagoidea, whereas arrhenotokous diplo-haploid species (with diploid females and haploid males) are known in Histiostomatoidea (Histiostomatidae: Histiostoma), Hemisarcoptoidea (Winterschmidtiidae: Kennethiella, Ensliniella, Kurosaia)(Hughes
and
Jackson,
1958;
Heinemann
and
Hughes,
1969;
Cowan,
1984;
Klompen
et
al.,
1987;
Okabe
and
Makino,
2003) and Sarcoptoidea. Thelytokous species occur in Histiostomatoidea (Histiostomatidae), Acaroidea (e.g. Acaridae: Schwiebea) (Okabe
and
OConnor,
2001;
Okabe
et
al.,
2008). Thelytokous pop-ulations are composed of females but extremely rare males can also be occasionally found; such males are non-reproducing as is believed, but their reproductive systems and/or spermatozoa have never been studied. In Knemidocoptes mutans (Analgoidea: Epidermoptidae) the frequency of males in populations is 2e4% (Dubinin,
1953); such strong bias towards males in practically sedentary mites suggests thelytoky rather than the effect of local mate competition, a phenomenon which can also lead to sex ratio distortion (Hamilton,
1967). Deuterotoky, in which both males and females are produced from unfertilized eggs, has been reported in Histiostomatidae
(Heinemann
and
Hughes,
1969). In most cases, the type of reproduction is only suspected and is based mainly on population structure since detailed studies are usually missing. Moreover, some phenomena concerning reproduction can be misinterpreted. For instance, a well-known cosmopolitan species, H. feroniarum (Histiostomatidae), has been for years believed to be comprised of arrhenotokous and thelytokous populations (Hughes
and
Jackson,
1958). Recent unpublished molecular studies (in co-operation with Dr. Miros1awa Dabert, Adam Mickiewicz University, Poznan, Poland) revealed that there are two separate but morphology practically indistinct species, an arrhenotokous species (H. feroniarum) and a thelytokous form (Histiostoma sp.). 4. Reproductive systems The anatomy of reproductive systems in Astigmata has been studied using light-microscopy since the 19th century (Nalepa,
1884,
1885;
Michael,
1901;
Hughes
and
Hughes,
1938;
Dubinin,
1953;
Hughes,
1959;
Popp,
1967;
Rohde
and
Oemick,
1967;
Prasse,
1968,
1970;
Heinemann
and
Hughes,
1970;
Kuo
and
Nesbitt,
1970;
Woodring
and
Carter,
1974;
Vijayambika
and
John,
1975;
Grifﬁths
and
Boczek,
1977;
Baker
and
Krantz,
1985;
Witalinski
and
Walzl,
1995), and has also been studied at the ultrastructural level (Witalinski
et
al.,
1990;
Walzl,
1992;
Desch,
2001;
Walzl
et
al.,
2004;
W. Witalinski / Arthropod Structure & Development 43 (2014) 323e340 Lekimme
et
al.,
2005;
Klien
and
Walzl,
2010;
Witalinski
et
al.,
2014). Some external details of female and male reproductive organs were also described using scanning electron microscopy (SEM) in pyro-glyphid
mites
(Mariana
et
al.,
2008). Finally, it should be emphasized that the most basal astigmatan group, Schizoglyphoidea, has not been studied since only several immature specimens of one species are known (OConnor,
2009), whereas living adult males and females are required for a comprehensive description of reproductive anatomy. Therefore, in this mini-review on anatomical and cytological aspects of reproduction, the superfamily Histiostomatoidea is treated as the most basal in Astigmata. 4.1. The female reproductive system Reproductive systems in female astigmatans studied so far are rather uniform and composed of two parts, the oogenetic (primary) and the inseminatory (secondary) parts (Grifﬁths
and
Boczek,
1977;
Witalinski
et
al.,
1990;
Witalinski
and
Walzl,
1995)(Fig.
2AeD). The oogenetic part comprises paired ovaries and oviducts, an unpaired common oviduct (sometimes also called the uterus, e.g. Prasse,
1970;
Witalinski
et
al.,
1990), a cuticle-lined preoviporal chamber (preoviporal canal of Witalinski
et
al.,
1990), and the oviporus. The oviporus is a complex cuticular structure comprising eugenital lips (internal paragynal folds of Witalinski
et
al.,
1990) covering the eugenital oriﬁce, genital papillae in diachilous slits, anterolateral progenital lips (external paragynal folds of Witalinski
et
al.,
1990), and a medial (epigynal) lip; the progenital chamber (sensu Van
der
Hammen,
1980) is the space between the eugenital lips and ante-rolateral progenital lips (for details see: Prasse,
1970;
Van
der
Hammen,
1980,
1989;
Witalinski
et
al.,
1990;
Evans,
1992;
Alberti
and
Coons,
1999). Spherical or subspherical ovaries are located symmetrically in the rear part of the idiosoma, usually on both sides of the last section of the alimentary tract, i.e. the postcolon, anal atrium and anus. They occupy a considerable part of the idiosoma, but in C. sellnicki are very small, spherical and located directly above the ventral cuticle (unpublished). In Psoroptidia, ovaries are located dorsally as in Sarcoptes scabiei and N. cati e Sarcoptidae (Witalinski
and
Walzl,
1995), Psoroptes spp. e Psoroptidae (Lekimme
et
al.,
2005)(Fig.
2BeD), and F. rostratus e Falculiferidae, but in the latter species they are additionally shifted anteriorly (Fig.
4D). Oviducts emerge at the ventral, anteroventral or lateroventral surface of the ovaries and run forward either straight to the oviporal region of the mite body as in the sarcoptid mites: S. scabiei and N. cati (Witalinski
and
Walzl,
1995), or are S-shaped bending twice to reach the oviporal region as in Acarus siro, Tyrophagus perniciosus,or Sancassania berlesei (Acaridae) (Walzl
et
al.,
2004) Image of Fig. 2 Fig. 2. Schematic representation of reproductive systems in females (AeD) and males (E, F) of Astigmata mites. (A) Acarus siro (Acaridae) dorsal view, (B) Sarcoptes scabiei (Sarcoptidae) axial section, (C, D) Psoroptes ovis (Psoroptidae) female, dorsal (C) and lateral (D) view, (E, F) Psoroptes ovis male, ventral (E) and lateral (F) view. Based on Witalinski
et
al.
(1990)
(A), Desch
(2001)
(B), Lekimme
et
al.
(2005)
(CeF). Abbreviations: asterisk e location of the ovarian nutritive cell (ONC), a e anus, ae e aedeagus, AG e male accessory gland, chg e chorional gland, chg1, 2 e two parts of chorional gland in Sarcoptes, covd e common oviduct, de e ejaculatory duct, ic e inseminatory canal, io e inseminatory opening, mg e midgut, oc e oocyte, op e oviporus, ov e ovary, ovd e oviduct, pch e preoviporal chamber, rs e spermatheca, scc e sperm-conveying cord, sz e spermatozoa in spermatheca, t e testis, vd e deferent duct. Scale bars: 100 mm in (A, B, E, F); 200 mm in (C, D). Image of Fig. 3 Fig. 3. Ovary organization as visible on cross sections of female mites (AeC) and ﬂuorescent staining of cross-sectioned ovary (D). (A) Ovary in Histiostoma spp. showing eccentric ONC with ramiﬁed nucleus and large nucleoli (nu). Oocytes in various developmental stages (oc) are connected with the ONC via intercellular bridges with diaphragm-crossed lumina (arrows). Germinal line cells are embedded in somatic ovarian stroma cells (osc). Thin ovarian wall cells (ow) lying on basal lamina (bm) encompass the ovary. (B) In the ovary of Acaridae and Carpoglyphidae the ONC is located subcentrally and oocytes (oc) are connected with the ONC via funnel-type intercellular bridges ﬁlled by electron-dense material (arrows). Other abbreviations as in (A). (C) The ONC in the ovary of Glycyphagus is in a dorsal position whereas the ventral part of the gonad contains oocytes (oc) in different developmental stages. Other abbreviations as in (A). (D) The LR-White semithin section through the ovary in Rhizoglyphus echinopus stained sequentially with DAPI and pyronine Y. DAPI (blue) reveals DNA whereas pyronine Y counterstains RNA. Note very strong signal for DNA from the ONC nucleus as compared to oocyte (oc) nuclei. oc e oocytes, ONC e the ovarian nutritive cell, ow e ovarian wall cells. Scale bars: 10 mm. W. Witalinski / Arthropod Structure & Development 43 (2014) 323e340 Image of Fig. 4 Fig. 4. Differential interference contrast (A) and conventional light microscopy (BeG). (A) Dissected ovary from Rhizoglyphus echinopus showing the ONC, oogonia/early oocytes (og/ oc) and developmentally advanced oocytes (oc) embedded in ovarian stroma cells (osc). Ovarian wall cells (ow) and intercellular bridges (arrows) are also visible. (B) Semithin cross section through a Histiostoma feroniarum female. Ovaries contain ONCs (asterisks) surrounded at other than abaxial sides by the oocytes (oc). Arrow points to diaphragm-type intercellular bridge. (C) Semithin cross section through Glycyphagus domesticus female. The ONC is located dorsally whereas the rest of the ovary is ﬁlled with oocytes (oc) in different stages of development. Vitellogenic oocytes just before entering the oviducts are also visible (asterisks). Arrow indicates intercellular bridge. (D) Axial semithin section of Falculifer rostratus female; anterior end of the body directed to the left. Spermatheca (rs), ovary (ov), vitellogenic oocyte (voc) in the oviduct, as well as chorional gland (chg) close to oviporus (op) are visible. Note lenticular extensions of perivitelline space in the vitellogenic oocyte. (E) The ovary in F. rostratus sectioned as in (D). The ONC, early oocytes (oc) and W. Witalinski / Arthropod Structure & Development 43 (2014) 323e340 (Fig.
2A). Ovaries in F. rostratus are located both dorsally and more anteriorly, while oviducts emerge to run posteriorly and then turn ventrally toward the oviporal region of the idiosoma. Consequently, in F. rostratus two distinct parts of the oviduct are present: a proximal upper section and a distal lower section. In all species, the oviducts close to the oviporus coalesce to form an unpaired common oviduct (¼uterus or chorion gland in sarcoptid and psoroptid mites e Fig.
4D and F). The common oviduct passes forward into a preoviporal chamber (sometimes incorrectly termed vagina), lined with a thin, usually plicated cuticle. This part can form a short-tube ovipositor by eversion which allows precise egg manipulation during oviposition. The genital aperture, the oviporus, is a longi-tudinal, transversal, or inverted V-shaped slit located in the mid region of the mite venter. Its structure is complex because the cuticular walls are folded and two pairs of ﬁnger-like genital papillae are located between folds (for details see: Witalinski
et
al.,
1990;
Evans,
1992;
Walzl,
1992;
Alberti
and
Coons,
1999). The pregenital sclerite (epigynum) rarely occurs in free-living astigmatans (many Glycyphagidae) but is common in parasitic Astig-mata (Ehrnsberger
et
al.,
2001). Female accessory glands occurring as paired, separate structures connected with the oviducts are absent. Paired accessory glands have been reported in some species (Kuo
and
Nesbitt,
1970;
Baker
and
Krantz,
1985;
Witalinski
et
al.,
1990), but subsequent studies with serial semithin sections have shown that the interpretation of the distal third portion of the oviduct as separate accessory glands was erroneous (Witalinski,
1993;
Witalinski
and
Walzl,
1995). However, in non-psoroptidian species the distal third portion of the oviducts has a thickened glandular wall, whereas in psoroptidians the common oviduct forms dorsally a large, more or less distinct glandular pocket, the chorion gland. In S. scabiei and N. cati the chorion gland comprises only one type of secretory cells, but in F. rostratus it contains two types of cells located in two distinct re-gions (Fig.
4D and F) (Witalinski,
1993). The inseminatory part (Fig.
2AeD) starts with a copulatory or inseminatory opening (bursa copulatrix) located at the rear end of the idiosoma as in Acaridae, Carpoglyphidae and many other stored food pests; the copulatory opening is frequently situated in a shallow depression formed by thickened cuticle (e.g. Acaridae, Suidasiidae, Carpoglyphidae, Falculiferidae and many other Psor-optidia)(Witalinski
et
al.,
1990;
Witalinski
and
Walzl,
1995;
Ahamad
et
al.,
2011). In some groups (e.g. Histiostomatoidea: His-tiostomatidae: H. feroniarum, Histiostoma sp., Hemisarcoptoidea: Chaetodactylidae: C. osmiae) the bursa copulatrix forms a tube or, as in Glycyphagoidea: Glycyphagidae, a cuticular collar protruding from the hind end of the body. An especially long caudal protrusion of the bursa copulatrix/inseminatory canal is present in some Pterolichoidea (Crypturoptidae and some Caudiferidae) (Gaud,
1982;
Proctor,
2003). Instead terminally, an inseminatory opening can be located more dorsally and placed at the apex of conical, several micrometer long cuticular papilla (e.g. Psoroptoidea: Psor-optidae: Psoroptes spp. e Lekimme
et
al.,
2005; Sarcoptoidea: Sar-coptidae: S. scabiei e Desch,
2001,
and
N. cati)(Fig.
2BeD). The type of bursa copulatrix is correlated with the shape of the apex of the aedeagus which is either pointed when matched with a concaved inseminatory opening (Prasse,
1970;
Witalinski
et
al.,
1990;
Ahamad
et
al.,
2011), or is modiﬁed and concaved terminally to ﬁrmly accept the insertion of the copulatory papilla (Sarcoptidae). From the copulatory opening, an inseminatory canal (internal diameter ranges from 0.5 to 0.6 mm to several micrometers e Witalinski
and
Walzl,
1995;
Desch,
2001) leads to the basal part of the spermatheca (seminal receptacle, receptaculum seminis) where sperm is stored before migration to ovaries via sperm-conveying cords (Fig.
2C and D). The inseminatory canal has a cuticular lin-ing, sometimes with additional external taenidia-like strengthening as in A. siro (Witalinski
et
al.,
1990), Pterodectes sp. (Popp,
1967), S. scabiei (Desch,
2001) and Psoroptes spp. (Lekimme
et
al.,
2005), and varies considerably in length. In non-psoroptidians it is short or moderately long (15e20 mmin H. feroniarum e orig., 14 mmin A. siro e Witalinski
et
al.,
1990;62e65 mmin Caloglyphus (¼Sancassania) berlesei and 43e47 mmin G. domesticus e Witalinski
and
Walzl,
1995), but in Psoroptidia it is usually long (70e75 mmin N. cati e Witalinski
and
Walzl,
1995)(ca. 70 mmin S. scabiei e Witalinski
and
Walzl,
1995,50 mmin D. farinae,100 mmin Pterolichus obtusus, Grallolichus proctogamus, 130 mmin Pseudolichus phasiani e Liana,
2004). The inseminatory canal in F. rostratus is extremely long (290e300 mm) and narrow, with a lumen diameter of 0.6 mm. According to Dubinin’s
(1953)
illustration, the inseminatory canal in Trouessartia rosterii is also very long, but it is short in other analgesoid feather mites such as Bdellorhynchus polymorphus and Analges passerinus. Sperm-conveying cords are solid cellular structures, conical in A. siro, but thin and cord-like in most other species in which the spermatheca is placed far from the ovaries, as, for instance, in F. rostratus and P. fuchsi where their diameter is 4.0e4.5 mm and ca. 3.0 mm, respectively. Spermatozoa migrate between conveying cord cells (Fig.
6A) from the basal part of the spermatheca towards the ovaries (A. siro e Witalinski
et
al.,
1990; F. rostratus e unpublished). Syngamy occurs within the ovary with previtellogenic oocytes before they are covered by a vitelline envelope; consequently, in sperm cells of Astigmata the acrosome is absent (Liana
and
Witalinski,
2005). The spermatheca in Astigmata (Figs.
2A,
D
and
4C, D) (Witalinski
et
al.,
1990;
Desch,
2001;
Lekimme
et
al.,
2005)is a complex saccular organ which consists of cellular and cuticular elements. The cuticular lining of the inseminatory canal amalgamates with the solid cuticular basal part of the spermatheca, the main part of the spermatheca visible in mites on microscopical slides examined under a light microscope. The cuticle of the basal part is supported by a thick layer of cells which continue anteriorly to form the saccular part of the spermatheca. The wall of the saccular part is thin and its cells form many long, internally pro-jecting microvilli. The margin of the basal part of the spermatheca protrudes to form two very thin, more or less continuous, ﬁne cuticular lamellae which encompass the internal space of the spermatheca. Thus, the lumen of the spermatheca is divided into two compartments, (1) an external one, penetrated with micro-villi of spermatheca cells, and (2) an internal one, delimited by double lamellae, to which sperm and other male-derived sub-stances are introduced. It is believed that sperm cells leave the spermatheca basis to enter conveying cords and then ovaries via a pair of openings in the basal part of the spermatheca located near two minute V-shaped cuticular appendages visible in light microscopical images. Klien
and
Walzl
(2010)
demonstrated that in S. berlesei, sperm cells aggregate in the spermatheca close to the entrance into such V-shaped appendages. These appendages, advanced previtellogenic oocyte (asterisk) are sequentially distributed from the anterior to posterior end of the ovary. (F) Chorional gland in F. rostratus sectioned as in (D), showing two types of glandular cells (1 and 2), preoviporal chamber (asterisk) and oviporal opening (op) in the ventral cuticle (cu). Vitellogenic oocyte (voc) contains dark yolk spheres and lenticular extensions of perivitelline space (arrow). (G) Sections of two oviductal oocytes in Chaetodactylus osmiae. The right oocyte contains numerous smaller yolk spheres than the left one, much advanced in vitellogenesis. Light proﬁles of lipid droplets occur between the yolk spheres. a e anal slit, aa e anal atrium, col e colon, gu e guanine, rs e spermatheca. Scale bars: 50 mm in (A, C, G); 100 mm in (D), 20 mm in (B, E, F). W. Witalinski / Arthropod Structure & Development 43 (2014) 323e340 Fig. 5. Details of the ovaries in TEM. (A) Dermatophagoides farinae. Funnel-type intercellular bridge ﬁlled with an electron-dense granular material connecting the ONC and oocyte (oc). The ONC contains elongated inclusions of microorganismal appearance surrounding the lipid droplet (L); similar inclusions are abundant in the ovarian stroma cell (osc). (B) Glycyphagus sp. Funnel-type intercellular bridge (sectioned somewhat out of axis) between a protrusion of the ONC and previtellogenic oocyte (oc). Mitochondria (m) in the oocyte are radially aggregated in the vicinity of the electron-dense bridge material and around the nucleus (n). (C) Glycyphagus domesticus. The ONC surrounded by oocytes (oc). Note spherical protrusions of the ONC embedded in the ovarian stroma cell (osc) close to the ONC surface. n e nucleus, nu e nucleolus, osc e ovarian stroma cell. Scale bars: 5 mmin (A, C); 10 mm in (B). named the ducti conjunctivi, consist of a sclerotized part, the funnel, which is ca. 40 mm long. Its diameter varies from 1 mmat the spermatheca to 20 mm at the distal end. These interesting structures, however, are still waiting for precise descriptions at the ultrastructural level. 4.1.1. The ovary The ovaries in Astigmata (Fig.
3) are of nutrimental type and, as in other animals, are composed of two elements: germinal and somatic cells. Oogonia and previtellogenic oocytes belong to germinal cells, as well as one very large and spherical cell of nutritive nature, the so-called ovarian central cell. All these germ-line cells are embedded in only several somatic cells with peripherally positioned nuclei. The ovary is surrounded by a layer of thin epithelium which is difﬁcult to discern under a light microscope and, e.g., is not mentioned in the sarcoptid mite N. cati (Witalinski,
1988). Vitellogenic oocytes occur in the transient zone between the ovary and oviduct and ﬁll the oviductal lumen, in which vitellogenesis is completed and egg envelopes begin to form. Prasse
(1968)
was the ﬁrst to observe the ovarian central cell and later observations conﬁrmed its presence in all studied species (Witalinski
et
al.,
1990;
Walzl,
1992;
Witalinski
and
Walzl,
1995;
Desch,
2001;
Lekimme
et
al.,
2005;
Schwaha
et
al.,
2008;
Witalinski
et
al.,
2014). Indeed, the central cell in many species is located centrally or subcentrally (A. siro, R. echinopus, C. sellnicki) within the ovary (Fig.
3B and D), but in some cases is shifted adaxially, as in H. feroniarum (Figs.
3A
and
4B), Histiostoma sp., abaxially as in C. lactis, abaxially and anteriorly as in Psoroptes spp. (Lekimme
et
al.,
2005), antero-dorsally as in S. scabiei (Desch,
2001), dorsally as in N. cati, or is located either dorsally or sub-centrally as in G. domesticus (Figs.
3C
and
4C). Since it can actually take central or quite eccentric positions, I propose to use the term ovarian nutritive cell (ONC), as a more proper name instead of central cell. W. Witalinski / Arthropod Structure & Development 43 (2014) 323e340 Fig. 6. Sperm-conveying cord in Proctophyllodes fuchsi (A), fragment of the ovary (B) and oviductal vitellogenic oocytes (CeE) in Chaetodactylus osmiae, and oviductal vitellogenic oocyte in Falculifer rostratus (F). (A) Cross-sectioned sperm-conveying cord (scc) containing spermatozoon with chromatin threads (ch). (B) Early oocyte (oc) with mitochondria (m) surrounding nucleus (n), which is connected via a bridge (asterisk) to the ONC. Note many protrusions of the ONC hosted in the ovarian stroma cell (osc). Oocytes are surrounded by ER cisterna of stroma cell (arrows). (C) Periphery of the vitellogenic oocyte containing yolk spheres (Y) in different stages of maturation, lipid droplets (L) and vitelline envelope (ve). (D) Higher magniﬁcation of the vitelline envelope (ve) showing a lamellated structure. Note the different appearance of two yolk spheres (Y); the left one is less mature and contains only several condensed cores in ﬂocculent material, whereas in the more developed, dense right sphere there are paracrystalline cores (asterisk), electron-lucent inclusions (white arrow) and meandering structures (black arrow). (E) Bilayered vitelline envelope (ve) on an oviductal oocyte more developed than those in (C) and (D). Note that the vitelline envelope material is homogenous rather than lamellated and yolk spheres (Y) are well developed. (F) A vitellogenic oviductal oocyte in Falculifer has a well developed roughly spherical yolk (Y), lenticular extensions of vitelline space (asterisk), and very poorly contrasted vitelline envelope (ve). ovd e oviduct wall. Scale bars: 1 mm in (A); 2 mm in (B, D-F); 5 mm in (C). W. Witalinski / Arthropod Structure & Development 43 (2014) 323e340 The ONC (Figs
3
and
4AeC, E) is a very large cell (diameter from ca. 20 mmin Falculifer and Pseudolichus, 25e30 mmin Sarcoptes, Scutulanyssus and Grallolichus,30e35 mmin Canestrinia, Glycyphagus, Notoedres, 40 mmin Pterolichus,up to 50 mmin Histiostoma, Psoroptes and Dermatophagoides)(Desch,
2001;
Liana,
2004;
Lekimme
et
al.,
2005) containing an elaborated nucleus with a number of prominent nucleoli. In most species the ONC has been described as multinucleate (Pyroglyphidae: D. farinae, Dermatophagoides pteronyssinus e Walzl,
1992) or mononucleate with a multilobular nucleus (Acaridae: A. siro e Witalinski
et
al.,
1990), but recent studies with serial sectioning following 3-D reconstruction performed on representatives of three families (Schwaha
et
al.,
2008): S. berlesei (Acaridae), G. domesticus (Glycyphagidae), Cho-rioptes bovis and Otodectes cynotis (Psoroptidae) led to the conclusion that in all Astigmata in ONCs only one extensively branched nucleus is present. DNA-speciﬁc ﬂuorescence after DAPI staining suggests polyploidy (Fig.
3D). The nuclear envelope forms many concavities rich in nuclear pore complexes with frequently adhering ﬁne granular or ﬂocculent nuage material. The rest of the cytoplasm is packed with free ribosomes; it also contains mitochondria and scarce ER and proﬁles of Golgi bodies. Lysosome-like bodies with non-homogenous content (H. feroniarum: Witalinski
et
al.,
2014) as well as crystalline inclusions (S. scabiei: Desch,
2001) can also be found. Eccentrically located ONCs are partly covered by oogonia and previtellogenic oocytes distributed usually in one to several layers; in this area the plasmalemma of the ONC can form many short protrusions described, e.g. in S. scabiei (Desch,
2001), as microvilli. In G. domesticus and C. osmiae the ONC also forms irregular, sometimes terminally expanded protrusions, penetrating the ovarian stroma cells at some distance (Figs.
5C
and
6B). Oogonia and oocytes are connected with the ONC through conspicuous intercellular bridges (Figs.
4A,
C,
5A,
B
and
6B). In general, inter-cellular bridges in all Astigmata except Histiostomatidae are funnel-shaped and ﬁlled with an electron-dense granular material (Fig.
6B) (Witalinski
et
al.,
1990;
Lekimme
et
al.,
2005;
Schwaha
et
al.,
2008;
Florek
and
Witalinski,
2010b;
Klien
and
Walzl,
2010). The bridge opening at the ONC side is ca. 6 mm wide and is smaller than at the oocyte side. Oogonia and small, young oo-cytes have elongated and much thinner bridges, but their diameter increases with the growth of the cells. Recent preliminary studies (Florek
and
Witalinski,
2010b) indicated that in histiostomatid mites (H. feroniarum) a second, unusual type of intercellular bridge is present (Figs.
3A
and
4B). This bridge is practically twodimensional and very large in advanced previtellogenic oocytes (10 mm or more) but its lumen is crossed with a thin diaphragm of electron dense material, hence it has been termed a diaphragmcrossed bridge. At higher magniﬁcation, the dense material is ar-ranged in a rectangular lattice. The same was observed in another undescribed Histiostoma species (Witalinski
et
al.,
2014). In another histiostomatid mite, Bonomoia opuntiae, the bridge has somewhat intermediate structure since the diaphragm dense material is thickened in the center of the bridge lumen (preliminary observations). Oocytes entering meiotic prophase are small roundish cells with a relatively large spherical nucleus in which synaptonemal complexes may be visible (Witalinski
et
al.,
2014). After the ﬁrst meiotic division, the oocytes start to grow at previtellogenic phase. In S. berlesei, meiosis is completed much later in oocytes moving along the second, backward-curved part of the oviduct, whereas the ﬁrst cleavage into two blastomeres occurs at the beginning of the third, forward-curved part of the oviduct (Walzl
et
al.,
2004). Detailed studies on the architecture of the ovary and oocyte pathways within the ovary during their development are absent, but light-microscopical observations of semithin sections suggest that previtellogenic oogenesis occurs generally around the ONC towards the pole where the oviduct emerges. Thus, in most cases oogonia and early previtellogenic oocytes are distributed dorsally or dorso-laterally, whereas the oocytes entering vitellogenesis are distributed ventrally or ventro-laterally in the ovary, i.e. close to the oviduct entrance. 4.1.2. Vitellogenesis Vitellogenesis in Astigmata occurs in oviductal rather than ovarian oocytes (Fig.
4CeG)
(Witalinski,
1995;
Walzl
et
al.,
2004), but this process is known only superﬁcially, since no in-vestigations have dealt with the subject and data are only available from papers focused on other aims (Walzl
et
al.,
2004;
Lekimme
et
al.,
2005;
Witalinski
et
al.,
2014). The nucleus in early vitellogenic oocytes is similar to that in previtellogenic ones but its outline is irregular (Fig.
4E); cytoplasmic organelles accumulate mainly at the oocyte periphery, whereas the rest of the cytoplasm is ﬁlled with two types of inclusions: electron-dense protein yolk spheres and electron-lucent inclusions, which are lipid droplets (Fig.
6CeF). The protein yolk spheres are usually several times larger than the lipid droplets; in Psoroptes (Lekimme
et
al.,
2005) their size is 8 mm and 0.9 mm, respectively. Peripherally located protein yolk spheres are small, ca. 1.6 mmin His-tiostoma and 1.0 in Sancassania. Much larger protein yolk spheres, ca. 5 mmin Histiostoma and up to 15 mmin Sancassania, are packed more centrally in the egg. Large spheres contain several darker roughly spherical cores of crystalline appearance. Lipid spheres comprise small lipid droplets (0.5e0.6 mm) grouped between protein yolk and sometimes surrounding areas of moderate den-sity (Witalinski
et
al.,
2014). The origin of yolk protein (vitellogenin, Vg) varies among mite groups. In mites possessing an arachnid-type ovary (i.e. a hollow, tubular ovary with oocytes protruding outside on stalks and covered with basement membrane only), as in ticks and some Parasitengonina (for further references see Evans,
1992;
Alberti
and
Coons,
1999;
Coons
and
Alberti,
1999), the Vg is either produced by the oocyte itself or, rather, derived from external sources. Fat bodies, midgut cells, and specialized subepidermal cells have been proposed as external sources (for further discussion and references see: Cabrera
et
al.,
2009). Externally produced Vgs are supplied through the hemolymph and absorbed via pinocytosis into oocytes. In many mites, however, the ovary is a compact structure and more or less evidently of nutrimental type (e.g. higher Gamasina: Arc-tacarina e Alberti
and
Krantz,
2007; Parasitina e Alberti
et
al.,
1999; Dermanyssina e Alberti
and
Zeck-Kapp,
1986;
Di
Palma
and
Alberti,
2001;
Nuzzaci
et
al.,
2001;
Di
Palma
et
al.,
2012; or some Para-sitengonina: Erythraeidae e Witte,
1975). In such cases, the oocytes are supplied by nutritive cords from nurse cells with mitochondria, ribosomes and other cytoplasmic components (Steiner
et
al.,
1995), as well as ribonucleoproteins involved in oocyte growth, but Vgs are synthetized and absorbed from hemolymph as above. In Oribatida, nutritive cells/tissues are absent in the ovary (for further references see Liana
and
Witalinski,
2012). In Astigmata, despite their close evolutionary relations to Oribatida, the ovaries are of nutrimental type, but the ONC seems to be a source of ribosome/ ribosome subunits and probably mRNA for Vg authosynthesis rather than of Vg itself, since 1) cytoplasm of previtellogenic oo-cytes is highly saturated with free ribosomes (e.g. Fig.
5), 2) vitellogenesis starts and progresses in oocytes which are no longer connected via bridges with the ONC, and 3) when oocytes are transported along oviducts, they do not show any signs of intensive pinocytotic uptake; moreover, they are coated with a vitelline en-velope (VE) transformed later into an impermeable chorion which can effectively block uptake from the hemolymph. It should be W. Witalinski / Arthropod Structure & Development 43 (2014) 323e340 noted, however, that newly formed VE in S. berlesei is lamellated and contains pores at regular intervals; it was suggested (Walzl
et
al.,
2004) that yolk or yolk precursors can be transported from the oviduct wall into the egg via these pores. A similar lamellated VE also grows on oviductal oocytes in C. osmiae (Fig.
6C and D). The molecular foundations of Vgs and their genes in Astgmata are, as in other mites, fragmentary and are known in only a few species (Blomia tropicalis, D. farinae, D. pteronyssinus, G. domesticus, S. scabiei and Suidasia medanensis)(Cabrera
et
al.,
2009). Equally unexplored is the regulation of vitellogenesis and, in particular, the identiﬁcation and physiological role of ecdysteroids and juvenile hormon (JH) in endocrine regulation of vitellogenesis. In mites, ecdysteroids such as ecdysone, 20E, 2-deoxyecdysone, and maki-sterone A have been identiﬁed in the gamasid mites, Dermanyssus gallinae (Chambers
et
al.,
1996) and Varroa jacobsoni (Feldlaufer
and
Hartfelder,
1997), and an astigmatan, Tyrophagus putrescentiae (Sakagami
et
al.,
1992). Because JH and its analogs have a major role in inﬂuencing oogenesis/vitellogenesis in most insects, in-vestigations aimed at ﬁnding these substances in mites have been conducted. Only farnesol, a precursor of JH, was identiﬁed in deutonymphs of Tetranychus urticae (Regev
and
Cone,
1975,
1976). However, farnesol is present in plants and can be sequestered from food by females which may use this substance as a sex attractant. On the other hand it was shown that exogenous farnesol increase oviposition. In contrast, many studies explored the effects of exogenous JH and its analogs or anti-JHs on mite reproduction (see Cabrera
et
al.,
2009: Table 2), but in the case of Astigmata there was either no effect (farnesol, JH analogs: methoprene and pyriproxyfen on T. putrescentiae) or the effect was negative (JH analogs: fenoxycarb, hydroprene and methoprene on D. farinae; ecdysone analog: halofenozide on T. putrescentiae). The only positive effect was shown by the JH analog, fenoxycarb, on female reproduction in A. siro. In conclusion, studies with JH precursors and anti-JHs were equivocal in establishing that mites have insect JH or they use it to regulate reproduction; thus a new concept for the regulation of female reproduction in mites was proposed in which ecdysteroids instead of JHs play the main role in stimulation of Vg gene expression in the fat body and midgut in ticks, or the midgut and ovaries in other mites (Cabrera
et
al.,
2009). 4.1.3. Egg envelopes Eggs of Astigmata are protected by envelopes of complex origin (Witalinski,
1993). First, an early vitellogenic oocyte entering the oviduct starts to secret a VE, which is therefore of primary origin. TEM studies on VE structure and formation indicated that at the beginning the VE material is either lamellated or coarse-ﬁbrillar (A. siro, Tyrophagus, S. berlesei e Acaridae; Witalinski,
1993;
Walzl
et
al.,
2004), but is not penetrated by oocyte microvilli as suggested by Reger
(1977)
for Caloglyphus anomalus (¼Sancassania anomala) (Acaridae), a species with a VE of the same appearance in TEM as A. siro (Witalinski,
1993) and C. osmiae (Fig.
6C and D). In Psoroptes spp. (Lekimme
et
al.,
2005), the VE is homogenous and electron-lucent, and its thickness is 0.2e0.3 mm. An electron-lucent VE also appears on oocytes in F. rostratus; the oocyte, as in other psoroptid mites, forms many deep concavities (Figs.
4D,
F
and
6F). The early VE in Histiostoma sp. has a variable thickness (0.6e1.5 mm) and its material is electron-dense, but contains ellypsoidal lucent spaces (Witalinski
et
al.,
2014). In S. berlesei the lamellated VE is 1 mm thick (Walzl
et
al.,
2004). As observed in several astigmatans, the thickness of the VE changes: at the beginning of VE formation its thickness increases, but decreases later when the VE lamellae or ﬁbrils disappear, leading to a homogenous VE (see Fig.
6D and E). Interestingly, the disappearance of VE substructure is concomitant with up to a twofold decrease in VE thickness and occurs when the eggs are passing through the distal third portion of the oviduct. Its wall is thick and possibly contains secretory cells. Secretion was not evidenced, but secretory activity was suggested to be a source of VE modiﬁcations in structure and properties (Witalinski,
1993). A modiﬁed, homogenous VE is 0.3e0.4 and 0.7 mm thick in A. siro and T. perniciosus, respectively, and in A. siro it was named the chorion since it was the only layer enveloping a deposited egg. In other species, additional, exochorional material can be deposited on the egg chorion (which therefore is termed the endochorion) prior to laying. In the distal portion of oviducts in T. perniciosus and putatively Tyrophagus longior, an exochorion of three types is secreted: dense patches, granules, and locular chambers. In Aleuroglyphus ovatus, tiny spherical patches were found instead of locular chambers. In psoroptid mites S. scabiei, N. cati, and F. rostratus,a VE of ﬂocculent appearance also transforms into a homogeneous chorion. Chorional glands in sarcoptid mites release exochorion material on the egg surface and form a vesicular monolayer (Witalinski,
1993). In F. rostratus, the chorional gland (Fig.
4D and F)produces a substance which is used to glue the egg on the feather barb of its host (the pigeon). It seems likely that the function of adhesive exochorion material is mainly egg ﬁxation to substratum (Sarcoptes, Notoedres, Falculifer, pterolichoid feather mites e Dubinin,
1953), but additional functions were also proposed, e.g. limited water loss from eggs due to locular chambers in Tyrophagus (Witalinski,
1993). 4.2. The male reproductive system Male reproductive systems in Astigmata were studied on several occasions by light-microscopy (Michael,
1901;
Rohde
and
Oemick,
1967;
Prasse,
1968;
Heinemann
and
Hughes,
1970;
Kuo
and
Nesbitt,
1970;
Vijayambika
and
John,
1975;
Baker
and
Krantz,
1985;
Witalinski
and
Walzl,
1995) and ultrastructurally (Witalinski
et
al.,
1990;
Walzl,
1992;
Lekimme
et
al.,
2005) and are more variable in organization compared to female reproductive systems. They comprise paired spherical or ellypsoidal testes located usually symmetrically in the rear part of the idiosoma, two deferent ducts (vasa deferentia), and one, two or no accessory glands (e.g. Fig.
2E and F). The proximal part of deferent ducts serves as a sperm reservoir, while the distal one has a glandular character (Witalinski
et
al.,
1990). In males of analgesoids A. pass-erinus (Analgidae) and Trouessartia appendiculata (Trouessartiidae), deferent ducts empty into vesicular structure described by Dubinin
(1951)
as a seminal vesicle; however, further studies seem necessary to clarify its structure and function. Both deferent ducts merge together with duct(s) of accessory gland(s), if present, to form a short unpaired deferent duct passing into an ectodermal, cuticlelined ejaculatory duct (ductus ejaculatorius). In Pterodectes (Proctophyllodidae) the ejaculatory duct is an extremely complicated structure functioning during insemination as a sperm pump (Popp,
1967;
Alberti
and
Coons,
1999). The ejaculatory duct enters the aedeagus to terminate at its apex. In acarid mite Caloglyphus (¼Sancassania) berlesei, the testes are situated asymmetrically: the left testis is located dorsally whereas the right one is located ventrally as a result of the occupation of the left side of the body by a very large accessory gland (Witalinski
and
Walzl,
1995). In Lardoglyphus konoi (Acaroidea: Lardoglyphidae), one testis is in front of the other, and two different accessory glands (one of them named a chambered organ) are present (Vijayambika
and
John,
1975). In the hemisarcoptoid mite C. osmiae two testes e each with its own germarium e adhere very tightly to one another ﬁlling the right side of the idiosoma, whereas the left side is occupied by a large accessory gland which opens into the left deferent duct (Fig.
7B). In the glycyphagoid G. domesticus two testes W. Witalinski / Arthropod Structure & Development 43 (2014) 323e340 Fig. 7. (A)Testis organization as visible in cross sections of male mites in case the germarium contains a testicular central cell (TCC) (e.g. Acaridae). The TCC with ramiﬁed nucleus is tightly surrounded by spermatogonia (sg) whereas spermatocytes (sc) and spermatids (sd) in various developmental stages are spread in testicular stroma cells (tsc). The entrance of deferent duct (vd) collects maturing sperm cells (sz). The basement membrane (bm) of testicular stroma cells surrounds the testis. (B) Semithin cross section of Chaetodactylus osmiae male showing two germaria (asterisks) in closely located testes at right side and a large accessory gland (AG) which occupies the left side of the mite body. a e anal opening, vd e deferent duct. Scale bars: 10 mm in (A); 100 mm in (B). are displaced symmetrically (Fig.
8A), but the left one is shorter as a large accessory gland is located anteriorly (Fig.
8B). In Psoroptes ovis (Psoroptidae) (Fig.
2E and F), paired testes are secondarily fused at their proximal parts, thus being actually unpaired (Lekimme
et
al.,
2005). Similarly, in N. cati (Sarcoptidae), testes are interconnected by a narrow bridge which is ﬁlled with an electron-dense, ﬂoccu-lent material (Witalinski,
1988). In D. farinae and D. pteronyssinus (Pyroglyphidae), the testis is unpaired (Walzl,
1992). In the sarcoptid mites S. scabiei and N. cati, testes are situated anteriorly to the aedeagus due to its posterior shifting while short, quickly merging deferent ducts run postero-ventrally rather than anteroventrally (as in most other astigmatans), to empty into the begin-ning of the ejaculatory duct (Witalinski
and
Walzl,
1995). The aedeagus is a sclerotized organ located midventrally, pro-truded by hydrostatic pressure and retracted by muscles attached to sclerites in the genital atrium (Prasse,
1970). Its tip is shaped to ﬁt the female bursa copulatrix opening; in Proctophyllodes males, the aedeagus is extremely long extending far behind the body of the male (OConnor,
2009). 4.2.1. The testis Testes in astigmatans have usually been brieﬂy described in conjunction with studies on spermatogenesis and sperm structure (Alberti,
1980;
Witalinski
et
al.,
1986;
Witalinski
and
Afzelius,
1987;
Witalinski,
1988;
Witalinski
et
al.,
1990;
Walzl,
1992;
Florek
and
Witalinski,
2010a;
Lekimme
et
al.,
2005). They are rather compact organs (Fig.
7A), delimited by a thin amorphous layer (Vijayambika
and
John,
1975) resembling a basal lamina in the light microscope. The membrane surrounds a few somatic cells in which germ cells at different stages are embedded (Witalinski
et
al.,
1990;
Walzl,
1992). In this review, such somatic cells are termed the testicular stroma cells. In some species (D. columbae, F. rostratus), stroma cells are multinucleate and perhaps syncytial (Fig.
9A and B). In S. scabiei two other kinds of somatic cells were found: distal cells and muscle cells (Witalinski
and
Afzelius,
1987). The germinal part (germarium) of the testis can be located dorsally or dorsolaterally (in S. scabiei and N. cati e Witalinski
and
Walzl,1995; C. lactis e Florek
and
Witalinski,
2010a), but if the testis is elongated then the dorsally located germarium may be found either in the anterior or posterior part of the gonad, as in G. domesticus (Witalinski
and
Walzl,
1995)(Fig.
8A) and A. siro (Witalinski
et
al.,
1990), respectively. In C. osmiae the germaria are located less regularly but rather adaxially in both testes adhering closely to each other as mentioned above. The germarium is composed of a compact group of early germ cells, spermatogonia, adhering tightly to one another (Fig.
8C and D) and to the so-called testicular central cell (TCC), if such a cell is present
in
the
adult
gonad.
The
TCC
(Fig.
8C) has been reported in A. siro (Witalinski
et
al.,
1990), Sancassania (¼Caloglyphus) berlesei and S. (¼Caloglyphus) michaeli (Prasse,
1968), Rhizoglyphus robini (Baker
and
Krantz,
1985) and H. feroniarum (Florek
and
Witalinski,
2010a), but is absent in many other species: D. pteronyssinus, D. farinae (Walzl,
1992), G. domesticus, S. scabiei, N. cati (Witalinski
and
Walzl,
1995), C. lactis and F. rostratus (Florek
and
Witalinski,
2010a). The TCCs are of special interest since their origin e germinal or somatic e and function were for a long time enigmatic. The very similar placement of ONCs and TCCs in gonads suggested a germinal origin and, moreover, a nutritive function. However, intercellular bridges connecting spermatogonia with the TCC were not observed, thus the question remained open. Studies performed recently on gonad development in Histiostoma provided evidence that ONCs and TCCs belong to the germinal cell line (Witalinski
et
al.,
2014), because both are connected by bridges with surrounding gonial cells in a quite similar way. The nutritive role of TCCs is rather doubtful; instead, it was postulated (Florek
and
Witalinski,
2010a) that the TCC can “suppress and/or drive the proliferation of adjacent spermatogonia” (for further discussion see Florek
and
Witalinski,
2010a). Indeed, growing and subsequently proliferating spermatogonia lose tight contact with the TCC, as was observed in H. feroniarum (unpublished) and A. siro (Fig.
8C), or separate from a compact mass of germarial earliest spermatogonia in species in which the TCCs in testes are absent (Fig.
8D). The deferent duct entrance is located opposite to the germarium, usually in the ventral area of the testis (Fig.
7A). The entrance of the deferent duct and its vicinity are packed with sperm cells (Figs.
8A
and
9A). Spermatocytes and spermatids disperse after leaving the germarium which disrupts the sequential distribution of spermatogenesis stages (Fig.
9A). They disperse singly or in small clonal groups which do not form wall-encapsulated cysts; rather, they are hosted within large, sometimes multinucleate somatic W. Witalinski / Arthropod Structure & Development 43 (2014) 323e340 Fig. 8. Two semithin sections of Glycyphagus domesticus male in light microscope (A, B) and details of the testis in TEM, in Acarus siro (C) and Carpoglyphus lactis (D, E). (A) Section at anal opening (a) level shows two symmetrically distributed testes, each with dorsally located germarium (white asterisks) and ventrally visible spermatozoa (black asterisks) within or close to the entrance of a deferent duct. (B) section as in (A) but more anteriorly. Anal opening is absent, right testis still occurs, but the left one is replaced by a large accessory gland (AG). Lumen of opisthonotal gland and alimentary tract are indicated by black and white asterisks, respectively. (C) Germarium containing the testicular central cell (TCC) surrounded tightly by early spermatogonia (sg’). Proliferating spermatogonia (sg’’) are separated from the TCC. (D) Early spermatogonia (sg’) in germarium adhere tightly to each other, whereas proliferating ones (sg’’) are distant. Note early spermatogonia nuclei with prominent central nucleoli (nu) and nuage material adhering to nuclear envelope (arrows). (E) Spermatocyte showing formation of spongy layer with participation of Golgi body (arrow). In a more advanced spermatocyte a spongy layer (sl) is formed. n e nucleus, sd e spermatid, tsc e testicular stroma cell. Scale bars: 50 mm in (A, B); 5 mm in (C); 2 mm in (D, E). W. Witalinski / Arthropod Structure & Development 43 (2014) 323e340 Fig. 9. Section through the testis in Falculifer rostratus in TEM. (A) Early spermatogonia (sg’) form the germarium and are electron-dense; proliferating spermatogonia (sg’’) are located at the germarium periphery whereas a spermatocyte (sc’) before division is less dense and enveloped in a thick spongy layer. Dividing spermatocytes (sc’’) and spermatids (sd) show lower density and their nuclei are absent. A spongy layer still occurs. Spermatozoa (sz) are electron-lucent and contain dense lamellae (dl), grouped mitochondria (m), and chromatin threads (arrows). Somatictesticular stroma cells (tsc) are multinucleate and their nuclei (n’) are peripherally distributed. (B) Fragment of the testis. Spermatocyte (sc) containing a nucleus (n) is covered by a spongy layer (asterisk). Several nuclei (n’) of a testicular stroma cell (tsc) are marked. Scale bars: 10 mm in (A); 2 mm in (B). W. Witalinski / Arthropod Structure & Development 43 (2014) 323e340 cells ﬁlling the testis, i.e. the testicular stroma cells (Figs.
8CeE
and
9A, B). 4.2.2. Spermatogenesis As mentioned above, the earliest spermatogonia located in the germarium adhere to the TCC or, if a TCC is absent, they adhere to the other spermatogonia so tightly that their borders can be detected only by TEM (Fig.
8C and D). A relatively large spermatogonial nucleus contains a prominent central nucleolus (Fig.
8D). The nuclear envelope shows shallow concavities with adhering nuage material. Mitochondria are distributed close to the nucleus. Spermatogonia located at the periphery of the germarium are larger and make contact with the germarium one-sidedly (Fig.
8D), eventually to separate and enter the spermatocyte stage. Early spermatocytes (Fig.
8E) are singular spherical cells with a roundish, “empty” nucleus devoid of condensed chromatin, but usually with a nucleolus located peripherally. Nuage material is still present. As the spermatocyte grows, the peripheral cytoplasm hosts many mitochondria and Golgi bodies; the latter participate in the formation of a characteristic superﬁcial spongy layer of anastomosing membranes/cisternae covering the cell (Figs.
8E,
9B
and
10A). The contribution of Golgi bodies to spongy layer formation was observed in many species (Witalinski
et
al.,
1986,
1990;
Liana,
2004;
Florek
and
Witalinski,
2010a), nevertheless, sub-plasmalemmal cisternae of ER were also proposed to be a source of spongy layer membranes in Astigmata spermatocytes (Witalinski
and
Afzelius,
1987;
Lekimme
et
al.,
2005). In general, growing spermatocytes undergo division (Fig.
10B and C), however, division is doubtful in some astigmatic species (see below). During division neither the nuclear envelope nor condensed chromatin with synaptonemal complexes is visible. This suggests that normal meiosis may be absent. Daughter cells remain interconnected by bridges delimited by unthickened cisterns of the spongy layer, thus typical contractile rings lined with electrondense material typical for conventional intercellular bridges or ring canals (permanent intercellular bridges in gametogenesis) are likely absent (Florek
and
Witalinski,
2010a). The number of inter-connected spermatids is no more than four, since in most species, sectioned groups of spermatids contain two (C. lactis e Florek
and
Witalinski,
2010a) or three to four (A. siro, T. putrescentiae e Witalinski
et
al.,
1986, D. columbae e Fig.
10C) cells in section, whereas in some species, e.g. in G. domesticus and C. osmiae, spermatocytes and spermatids are singular. Moreover, the size of spermatids is only somewhat smaller than that of spermatocytes, decreasing progressively. In such cases, male germ cells differentiate, but evidently do not divide. During spermiogenesis many unusual changes occur. Mitochondria in early spermatids can be located peripherally beneath the spongy layer (e.g. in C. lactis e Florek
and
Witalinski,
2010a); later, in many species they transform into more or less modiﬁed mitochondrial derivatives, sometimes vesicular and difﬁcult to distinguish, as in A. siro, T. putrescentiae (Witalinski
et
al.,
1986,
1990), H. feroniarum (Witalinski
et
al.,
2014), D. columbae (Fig.
10B and C), or P. fuchsi (Fig.
10E). In some cases, however, mitochondrial morphology is altered moderately (e.g. S. scabiei and N. cati e Witalinski
and
Afzelius,
1987;
Witalinski,
1988; C. osmiae e Fig.
11B), or only slightly, as in G. domesticus (Fig.
11D and E) or F. rostratus (Liana
and
Witalinski,
2005). In some species, mitochondria have a tendency to aggregate forming large assemblages, as in D. pteronyssinus and D. farinae (Walzl,
1992); in P. obtusus many rod-shaped mitochondria aggregate end-to-end and side-byside forming bundles meandering within the cell (Liana
and
Witalinski,
2005). As spermiogenesis progresses, cisterns of the spongy layer can aggregate to form a spherical spongy body (Fig.
11E, inset) (Florek
and
Witalinski,
2010a); cisterns of the spongy layer sometimes participate in the formation of very conspicuous structures (Fig.
11A and C). In consequence, the spermatid is no longer covered by a spongy layer, but its plasmalemma seems to be thickened. Chromatin appears in spermatid cytoplasm as progressively thickening threads. Electron-dense lamellae (most species) or tu-bules (Sarcoptes and Notoedres) derived from ER also occur. In some cases, a band of granular material (C. sellnicki) or many chains of small vesicles (Scutulanyssus obscurus) occur in the spermatids, but dense lamellae or tubules are absent (Liana,
2004). 4.2.3. Sperm structure Several papers dealing with sperm structure in Astigmata have described their peculiar organization: S. anomala (¼C. anomalus) (Reger,
1971), A. siro (Alberti,
1980;
Witalinski
et
al.,
1986,
1990), T. putrescentiae (Witalinski
et
al.,
1986), D. farinae (Walzl,
1992), Psoroptes equi (Alberti,
1984), S. scabiei (Witalinski
and
Afzelius,
1987), and N. cati (Witalinski,
1988). In the only review dealing with sperm structure in Astigmata (Liana
and
Witalinski,
2005), the number of studied species was substantially enlarged to include H. feroniarum, C. sellnicki, Glycyphagus sp., S. berlesei, P. obtusus, P. phasiani, G. proctogamus, F. rostratus, S. obscurus, Trouessartia minutipes and Myocoptes musculinus. Quite recently, data on the ultrastructure of spermatozoa in C. lactis have become available (Florek
and
Witalinski,
2010a). Sperm structure in four other spe-cies, C. osmiae (Hemisarcoptoidea: Chaetodactylidae), G. domesticus (Glycyphagoidea: Glycyphagidae), D. columbae (Analgoidea: Analgidae), and P. fuchsi (Analgoidea, Proctophyllodidae), are described in this review and thereby increase the number of studied species to 23. Representatives of 8 superfamilies from 9 available for investigation were studied and only spermatozoon structure in Hypoderatoidea is still unknown. Spermatozoa in astigmatic mites are multiform cells (Figs.
9A
and
10D,
E
and
11B, D, E) making their dimensions difﬁcult to precisely determine. As calculated from TEM micrographs, sperm cell size varies considerably from ca. 2 mmin H. feroniarum, 3e4 mm in M. musculinus, N. cati and S. scabiei, 5 mmin G. proctogamus, 6 mm in A. siro, 6e7 mmin F. rostratus and D. farinae,7e8 mmin Glycyphagus sp., 8e10 mmin P. phasiani,8e11 mmin P. obtusus and 12 mm in T. minutipes, but reaching ca. 18 mmin C. sellnicki and 22e27 mm in S. obscurus (Liana
and
Witalinski,
2005). Sperm diameter in the newly studied species D. columbae is ca. 1.4e2.9 mm, 2.9e4.5 mmin P. fuchsi, whereas in C. osmiae and G. domesticus spermatozoon size isca.4 11 mmandin7 15 mm, respectively. The most striking feature of sperm cells is the lack of a nucleus; instead, chromosomal material is visible as threads embedded directly in the cytoplasm and located more or less centrally in the cell (e.g. Alberti,
1980;
Lekimme
et
al.,
2005;
Liana
and
Witalinski,
2005;
Florek
and
Witalinski,
2010a). Chromatin has a star-like appearance in two of three genera in the Pterolichidae family, suggesting that several threads cross at some sites. The diameter of chromatin threads varies from 40 to 60 nm in most species up to 170e190 nm in H. feroniarum. Other peculiarities of Astigmata sperm are electron-dense lamellae derived from ﬂat ER cisternae which are present in spermatids. In C. lactis there is only one lamella partly surrounding the chromatin threads (Florek
and
Witalinski,
2010a). In the Histiostoma spermatozoon (Liana
and
Witalinski,
2005;
Witalinski
et
al.,
2014) two lamellae run parallel to each other and this tandem is located laterally to the chromatin threads. Two to several lamellae occur in the vicinity of chromatin threads in Tyrophagus (Witalinski
et
al.,
1986). In several other species shorter or longer proﬁles of lamellae, frequently in parallel arrangement, are placed mostly around the chromatin (Acarus, Glycyphagus, Dermatophagoides, Falculifer, Grallolichus, Psoroptes, Myocoptes), whereas in Pterolichus W. Witalinski / Arthropod Structure & Development 43 (2014) 323e340 W. Witalinski / Arthropod Structure & Development 43 (2014) 323e340 Fig. 11. Spermatogenesis and sperm structure in Chaetodactylus osmiae (A, B) and Glycyphagus domesticus (CeE), TEM. (A) Spermatid with chromatin (ch) and area of anastomosing membranes (asterisk) separated by electron-dense lamella (dl). Anastomosing membranes are surrounded by arcuate cisterns (arrows); their external membranes show periodic densities (inset). (B) Several sperm cells at different levels of condensation (1e4): less condensed spermatozoon (1) shows an electron-dense lamella (dl) which separates chromatin threads (ch) from circular proﬁles (arrows). Mitochondrial derivatives (m) are also present. (C) Spermatid fragment containing a conspicuous cisternal arrangement which later transforms into a spongy body of the spermatozoon. There are also electron-dense lamellae (dl) and mitochondria (m). (D) Several spermatozoa in a deferent duct (vd) containing chromatin (ch), dense lamellae (dl), and mitochondria (m). Material ﬁlling the deferent duct is highly electron-dense. (E) Spermatozoon at higher magniﬁcation showing chromatin (ch), dense lamellae (dl), and mitochondria. In the lower spermatozoon a ﬁbrillar bundle (arrow) is present. Inset shows a spongy body. Scale bars: 1 mmin (AeC); 5 mmin (D, E); 1 mmin (Einset). W. Witalinski / Arthropod Structure & Development 43 (2014) 323e340 they are visible in between chromatin threads; in Pseudolichus lamellae are scarce and curved showing circular proﬁles. Spermatozoa in Trouessartia are packed with stacks of parallel and short lamellae. In contrast, lamellae are absent in Canestrinia and Scutulanyssus sperm; in the former species sperm contains a band of granular material, whereas the Scutulanyssus sperm cell is ﬁlled with branching chains of vesicles (Liana
and
Witalinski,
2005). In sarcoptid mites (Notoedres and Sarcoptes), ramifying electrondense tubules distributed within the cell are visible in place of lamellae; these tubules originate during spermiogenesis from tubular proﬁles of ER rather than ﬂat
ER
cisternae
(Witalinski
and
Afzelius,
1987). Psoroptes sperm shows intermediate lamellar structures since spermatozoa contain many parallel lamellae organized in groups and electron-dense tubules which seem to grow out from the lamellae margins (Alberti,
1984;
Liana
and
Witalinski,
2005). As was mentioned earlier, mitochondria during spermiogenesis in Astigmata either persist e at least to some degree e in their normal structure, or they transform into mitochondrial derivatives of variable appearance and distribution within the cell. Nearly unmodiﬁed mitochondria have been found in sperm of P. obtusus (Liana
and
Witalinski,
2005), in which they form large assemblages with rod-shaped mitochondria aggregating end-to-end and side-by-side in a bundle meandering within the cell. Distinct and large assemblages of mitochondria are also present in Dermatophagoides sperm. In other studied species mitochondrial derivatives are more or less altered and their internal structures, especially cristae, are no longer discernible; such poorly visible vesicular structures occur, for instance, in Acarus and Tyrophagus sperm (Witalinski
et
al.,
1986,
1990). Thus, in most cases the function of mitochondrial derivatives as energy (ATP) donors for spermatozoon movement seems unlikely; their deeply disintegrated structure is in accor-dance with the uniparental theory of maternal mitochondrial in-heritance (e.g. Giles
et
al.,
1980;
Sutovsky
et
al.,
1999). Sperm structure in the currently studied species also shows some special characters. In C. osmiae (Fig.
11B) the spermatozoon contains only one meandering lamella which separates chromatin threads (40e45 nm thick) and circular proﬁles likely derived from spermatid arcuate cisterns present around a large spongy area (Fig.
11A). The latter is putatively a remnant of the spermatocyte superﬁcial spongy layer. Spermatozoa in G. domesticus (Fig.
11D and E) contain many electron-dense lamellae surrounding chromatin threads (70e80 nm thick), as well as many globular mitochondria with frequent incisions. In the sperm cell of P. fuchsi (Fig.
10E) centrally located, tightly packed chromatin threads (27e33 nm thick) are surrounded by radially oriented groups of lamellae ar-ranged in parallel. Most remarkable is the sperm of D. columbae (Fig.
10D), since this is the only case of astigmatic spermatozoon without chromatin threads; instead, there are many granules of variable size (90e125 nm) and density surrounded by moderately dense, elongated or circular proﬁles derived from a short electrondense lamella visible in spermatids (Fig.
10C). The acrosome is absent in sperm of Astigmata. This is the consequence of early syngamy, since sperm penetrates ovaries (Prasse,
1968;
Witalinski
et
al.,
1986;
Witalinski,
1988) and en-counters naked oocytes before the vitelline envelope/chorion is formed. Interestingly, spermatozoa found within the female show ﬁne ﬁlaments regularly distributed under the cell membrane; their role in sperm motion have been suggested (Alberti,
1980;
Witalinski
et
al.,
1986). 4.2.4. Testicular somatic cells Germinal cells in testis are embedded in a few somatic cells (Figs.
7A
and
8C,
D
and
9), termed the testicular stroma cells in this review. The number of stroma cells is difﬁcult to determine; their irregularly shaped nuclei located peripherally are scarcely visible, suggesting a low number of these cells in the testis (e.g. Sarcoptidae: N. cati e Witalinski,
1988). In some species, e.g. C. lactis, stroma cells are distinct and connected by adherent junctions, at least close to the testis-deferent duct transition (Florek
and
Witalinski,
2010a). However, in F. rostratus (Fig.
9) and S. scabiei, stroma cells (originally named the main somatic cells; Witalinski
and
Afzelius,
1987) contain many nuclei and their syncytial nature is possible. In the latter species, two additional kinds of somatic cells were found: the so-called distal somatic cells and muscle cells. The distal somatic cells are located close to the beginning of the deferent duct, thus may be considered as an element of the deferent duct wall. More interesting are muscle cells embedded in stroma cells, with con-tractile ﬁlaments containing appendages penetrating stroma cells and observable between germ cells in testis regions rather distant from the entrance of the deferent duct. 5. Conclusions and perspectives Studies on the reproduction of Astigmata are fragmentary and focused mostly on some aspects of reproduction and reproductive behavior having implications in the evolution of reproductive strategies (Tilszer
et
al.,
2006;
Radwan,
2009) rather than gonad structure, details of gametogenesis and functioning of reproductive systems. For example, very little is known on the functioning of the spermatheca in Astigmata females (Radwan
and
Witalinski,
1991), as well as on events during sperm storage, migration to ovaries and details of fertilization. The same deﬁciency of information pertains to the role of the TCC in spermatogenesis. Recent studies on gonad development in Histiostoma (Witalinski
et
al.,
2014) conﬁrmed earlier suggestions (Witalinski
et
al.,
1990) on TCC origin from the germinal line. However, the role of the TCC during the early stages of gametogenesis and reasons, why TCCs are absent in adult testes in some species whereas they remain in others, are still enigmatic. Further conclusions may stem from studies on species with adult testes devoid of TCC to evidence whether TCCs are present in developing gonads and, if so, when and how they disappear. A very intriguing problem concerns oogenesis, in particular the structure of the unique intercellular bridges connecting previtellogenic oocytes with the ONC. In all studied Astigmata except Histiostomatidae, funnel shaped bridges ﬁlled tightly with some electron-dense material are present. The function of such structures as a gate controlling the in-and-out ﬂow between the ONC and oocytes is only suggested; the same concerns the even more conspicuous and enigmatic diaphragm-crossed bridges found in Histiostoma species. The reasons for such profund modiﬁcations of ordinary intercellular bridges and mechanisms involved in their function should be studied in the future. Moreover, studies on ovaries in Histiostomatoidea other than Histiostoma could clarify whether the funnel-shaped intercellular bridges evolved from diaphragm-crossed bridges or vice versa, or both types appeared independently. A different body of information should be collected and considered in the light of the evolution of gonads and reproduction in Astigmata. If we accept the idea that Astigmata evolved from within early Oribatida (Desmonomata: Trhypochthoniidae) (Norton
et
al.,
1993) a number of problems must be considered. First, the gonads in contemporary Oribatida are quite different than in Astigmata (further literature: Alberti
and
Coons,
1999;
Liana,
2004;
Bergmann
et
al.,
2008;
Liana
and
Witalinski,
2012). For instance, oribatid ovaries are unpaired and composed of oocyte clusters connected via microtubule-rich protrusions with one or several enucleate centers (medullae). Such ovaries are evidently not of nutrimental type. Oribatid testes are usually paired, but consist of germinal and glandular parts. Second, sperm W. Witalinski / Arthropod Structure & Development 43 (2014) 323e340 organization in both taxa is completely different, showing peculiarities in each group (e.g. oribatid sperm contains compact, highly condensed chromatin containing mitochondrial derivatives, whereas in astigmatic spermatozoa separate chromatin threads are freely embedded in cytoplasm). Third, differences in reproductive behavior are also striking and not easy to explain: Oribatida are inseminated through stalked spermatophores deposited on the substrate, whereas Astigmata females are inseminated during copulation via an accessory inseminatory system. Moreover, the-lytokous parthenogenesis is a main reproductive strategy in Des-monomata, whereas in Astigmata thelytoky seems to be secondarily evolved in some taxa only. It is necessary to emphasize, however, that in fact we know practically nothing on the reproduction of the ancestors of Astigmata since we can only study living oribatid taxa and it is at least theoretically possible that oribatid progenitors of Astigmata were much different from contemporary Desmonomata/Trhypochthoniidae. Acknowledgements This study was partly supported by grant number N N303 799940 from the Ministry of Science and Higher Education, Poland. The author wishes to thank Dr. Marcin Liana, National Centre of Science, Krak, Poland), who prepared and partly studied using TEM the material of Proctophyllodes fuchsi, and made it available for this review, as well as to Dr. Roberto Nannelli (Istituto Sperimentale per la Zoologia Agraria, Florence, Italy) and Prof. Dr. Micha1 Woyciechowski (Institute of Environmental Sciences, Jagiellonian University) for supplying the author with Glycyphagus domesticus and Chaetodactylus osmiae, respectively. Finally, English correction of the MS was kindly done by Dr. Maciej Pabijan, Institute of Zoology, Jagiellonian University. TEM observations were done in the Department of Cell Biology and Imaging, Institute of Zoology, Jagiellonian University. References Ahamad,
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