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Gonads and Gametogenesis in Astigmatic Mites

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Gonads and Gametogenesis in Astigmatic Mites ASD565_proof ■ 7 May 2014 ■ 1/18 Arthropod Structure & Development xxx (2014) 1e18 55 Contents lists available at ScienceDirect 56 57 Arthropod Structure & Development 58 59 60 journal homepage: www.elsevier.com/locate/asd 61 62 63 64 65 1 Gonads and gametogenesis in astigmatic mites (Acariformes: 66 2 67 3 Astigmata) 68 4 69 * 5 Q1 Wojciech Witalinski 70 6 71 Department of Comparative Anatomy, Institute of Zoology, Jagiellonian University, Gronostajowa 9, 30-387 Kraków, Poland 7 72 8 73 9 article info abstract 74 10 75 11 76 Article history: Astigmatans are a large group of mites living in nearly every environment and exhibiting very diverse 12 Received 13 February 2014 reproductive strategies. In spite of an uniform anatomical organization of their reproductive systems, 77 13 Received in revised form gametogenesis in each sex is highly variable, leading to gamete formation showing many peculiar fea- 78 7 April 2014 14 tures and emphasizing the distinct position of Astigmata. This review summarizes the contemporary 79 Accepted 9 April 2014 15 knowledge on the structure of ovaries and testes in astigmatic mites, the peculiarities of oogenesis and 80 16 spermatogenesis, as well as provides new data on several species not studied previously. New questions 81 Keywords: 17 are discussed and approaches for future studies are proposed. 82 Ovarian nutritive cell Ó 18 Testicular central cell 2014 The Author. Published by Elsevier Ltd. This is an open access article under the CC BY license 83 19 Intercellular bridges (http://creativecommons.org/licenses/by/3.0/). 84 20 Ovary 85 Oogenesis 21 86 22 Vitellogenesis Testis 87 23 Spermatogenesis 88 24 Spermatozoa 89 25 Gonadal somatic cells 90 26 91 27 92 28 93 1. Introduction 1.1. Systematics of Astigmata 29 94 30 95 Mites (incl. ticks) consist of a large group of chelicerate arthro- As currently recognized (OConnor, 2009), the astigmatic lineage 31 96 pods comprising more than 55 000 described species, however, diversified into 10 superfamilies, 71 families comprising 960 genera 32 97 acarologists estimate that many times this number have yet to be and more than 6100 described species (Klimov and OConnor, 2013). 33 98 described (Walter and Proctor, 1999; Krantz, 2009). In the last de- At present, even at a high taxonomic level the suggested phyloge- 34 99 cades mites (Acari) were considered to be a natural taxon; however, netic relationships are based on traditional morphological analyses 35 100 diphyly has also been postulated (Zakhvatkin, 1952; Van der rather than molecular studies, with the exception of a recent mo- 36 101 Hammen, 1977, 1979, 1989). Quite recently, a molecular study on lecular study by Klimov and OConnor (2013). A provisional but still 37 102 the phylogeny of Acari again strongly supported its diphyletic temporarily accepted cladogram is presented in Fig. 1 by OConnor 38 103 origin (Dabert et al., 2010). Consequently, there are two indepen- (2009), adopted from earlier work (Norton et al., 1993). It shows 39 104 dent branches (superorders): Parasitiformes (¼Anactinotrichida) the phylogenetic relationships of Astigmata superfamilies and 40 105 and Acariformes (¼Actinotrichida). The latter originated at least in combines Pterolichoidea, Analgoidea and Sarcoptoidea into a 41 106 the Early Devonian (Hirst, 1923; Norton et al., 1988; Bernini, 1991) monophyletic group Psoroptidia with ca. 3800 species (OConnor, 42 107 and comprises four taxa: the Trombidiformes (order), the 1982; Klimov and OConnor, 2008), although the composition of 43 108 Endeostigmata (suborder), the Oribatida (suborder), and the cohort Pterolichoidea and Analgoidea is somewhat disputable (for details 44 109 Astigmata (¼ Astigmatina, Acaridida) (Lindquist et al., 2009). see: Proctor, 2003). 45 110 Astigmata is considered a natural group and most likely derived 46 111 from an early clade (infraorder, acc. to Schatz et al., 2011) of Ori- 1.2. Environment of Astigmata 47 112 batida, the Desmonomata (OConnor, 1984; Norton, 1998). 48 113 Although astigmatan free-living mites are abundant in wet litter 49 114 and soil, especially in highly decomposed material, they often are 50 115 * þ the dominant mite group in patchy or ephemeral habitats. They are 51 Tel.: 48 12 664 5047. 116 E-mail address: [email protected]. numerous in decaying organic matter, dung, carrion, sap flows, dry 52 117 53 http://dx.doi.org/10.1016/j.asd.2014.04.003 118 54 1467-8039/Ó 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/). 119 Please cite this article in press as: Witalinski, W., Gonads and gametogenesis in astigmatic mites (Acariformes: Astigmata), Arthropod Structure & Development (2014), http://dx.doi.org/10.1016/j.asd.2014.04.003 ASD565_proof ■ 7 May 2014 ■ 2/18 2 W. Witalinski / Arthropod Structure & Development xxx (2014) 1e18 1 parts of mite bodies were fixed for 2 h at 4 Cinfixative containing 66 2 4% paraformaldehyde and 2.5% sucrose in 0.01 M PBS. After fixation, 67 3 the material was washed and dehydrated in a graded ethanol series 68 4 then embedded in LR-White (Fluka) resin. Semithin sections were 69 5 stained 30 min with DAPI, washed several seconds in PBS, and 70 6 stained 20 min with Pyronin Y (SigmaeAldrich)(20 mg/ml). After 71 7 brief washing in PBS sections were mounted and examined under a 72 8 fluorescence microscope Olympus BX51 (Olympus Corporation, 73 9 Tokyo, Japan) fitted with appropriate filters. 74 10 75 11 3. Reproduction of Astigmata 76 12 77 13 Fig. 1. Cladogram of Astigmata superfamilies (adopted from Norton et al. (1993) by Both sexual and parthenogenetic species occur in Astigmata, the 78 14 OConnor (2009) showing families and species studied originally for this review. latter represented by arrhenotokous, thelytokous, and rare deu- 79 15 terotokous organisms. In species possessing both females and 80 16 males (sexual and arrhenotokous species) the proportion of sexes 81 fi 17 and water- lled tree holes, phytotelmata and caves (Hughes, 1976; may be only slightly biased towards females. The males use their 82 18 Evans, 1992; Fashing, 1994, 1998). The other species are successful intromittent organ, the aedeagus (¼penis) to inseminate females 83 fl 19 in destroying stored food such as cereals, our, cheese, dried fruits with sperm during copulation. Insemination never occurs through 84 20 and meat, etc., leading to considerable crop damage (Hughes, 1976). the oviporus, but via a supplementary inseminatory system. Sexual 85 21 An abundance of Astigmata is associated with other animals, species (with diploid females and diploid males) occur for instance 86 22 mainly insects and amniotic vertebrates (e.g. all Psoroptidia with in Acaroidea and Glycyphagoidea, whereas arrhenotokous diplo- 87 23 the exception of Pyroglyphidae which are free-living), frequently as haploid species (with diploid females and haploid males) are 88 24 serious dermicolous parasites (Fain and Lukoschus, 1986; Proctor, known in Histiostomatoidea (Histiostomatidae: Histiostoma), 89 25 2003; OConnor, 2009). They can also inhabit bird and mamma- Hemisarcoptoidea (Winterschmidtiidae: Kennethiella, Ensliniella, 90 26 lian nests or such distinct habitat as feathers. Despite a wide range Kurosaia)(Hughes and Jackson, 1958; Heinemann and Hughes, 91 27 of habitats and a successful adaptive radiation, these mites share 1969; Cowan, 1984; Klompen et al., 1987; Okabe and Makino, 92 28 many distinct features in reproductive anatomy and reproductive 2003) and Sarcoptoidea. Thelytokous species occur in Histiosto- 93 29 behavior. matoidea (Histiostomatidae), Acaroidea (e.g. Acaridae: Schwiebea) 94 30 (Okabe and OConnor, 2001; Okabe et al., 2008). Thelytokous pop- 95 31 2. Materials and methods ulations are composed of females but extremely rare males can also 96 32 be occasionally found; such males are non-reproducing as is 97 33 In this review, original results were obtained through routine believed, but their reproductive systems and/or spermatozoa have 98 34 transmission electron microscopy (TEM) with a procedure sum- never been studied. In Knemidocoptes mutans (Analgoidea: Epi- 99 35 marized as follows. The sex of studied mite species (Histiostoma- dermoptidae) the frequency of males in populations is 2e4% 100 36 tidae: Histiostoma feroniarum Dufour, Canestriniidae: Canestrinia (Dubinin, 1953); such strong bias towards males in practically 101 37 sellnicki (Samsinák), Carpoglyphidae: Carpoglyphus lactis L., Chae- sedentary mites suggests thelytoky rather than the effect of local 102 38 todactylidae: Chaetodactylus osmiae (Dufour), Glycyphagidae: Gly- mate competition, a phenomenon which can also lead to sex ratio 103 39 cyphagus domesticus (De Geer), Falculiferidae: Falculifer rostratus distortion (Hamilton, 1967). Deuterotoky, in which both males and 104 40 (Buhcholz), Sarcoptidae: Notoedres cati Hering, Analgidae: Diplae- females are produced from unfertilized eggs, has been reported in 105 41 gidia columbae (Buhcholz), Proctophyllodidae: Proctophyllodes Histiostomatidae (Heinemann and Hughes, 1969). 106 42 fuchsi Mironov, Pyroglyphidae: Dermatophagoides farinae Hughes) In most cases, the type of reproduction is only suspected and is 107 43 (Fig. 1) was identified under a Nikon SMZ1000 stereomicroscope based mainly on population structure since detailed studies are 108 44 (Nikon Instruments Europe, Amsterdam, Netherlands). After im- usually missing. Moreover, some phenomena concerning repro- 109 45 mersion into a droplet of Karnovsky’s fixative (Karnovsky, 1965) duction can be misinterpreted. For instance, a well-known 110 46 (mixture containing 2% formaldehyde and 2.5% glutaraldehyde in cosmopolitan species, H. feroniarum (Histiostomatidae), has been 111 47 0.1 M cacodylate buffer, pH 7.2) on a Parafilm-coated microscopic for years believed to be comprised of arrhenotokous and thelyto- 112 48 slide, the anterior part of the body was cut off with a fine razor kous populations (Hughes and Jackson, 1958). Recent unpublished 113 49 blade and the remaining rear part was transferred into fresh fixa- molecular studies (in co-operation with Dr. Miros1awa Dabert, 114 50 tive for 24 h at 4 C.
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