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Fine Structure of the Midgut Epithelium of <I>Nicoletia

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Fine Structure of the Midgut Epithelium of <I>Nicoletia Folia biologica (Kraków), vol. 58 (2010), No 3-4 doi:10.3409/fb58_3-4.217-227 FineStructureoftheMidgutEpitheliumof Nicoletiaphytophila Gervais,1844(Zygentoma:Nicoletiidae:Nicoletiinae) withSpecialEmphasisonitsDegeneration* MagdalenaM.ROST-ROSZKOWSKA,JitkaVILIMOVA and £ukasz CHAJEC Accepted May 25, 2010 ROST-ROSZKOWSKA M. M., VILIMOVA J., CHAJEC £. 2010. Fine structure of the midgut epithelium of Nicoletia phytophila Gervais, 1844 (Zygentoma: Nicoletiidae: Nicoletiinae) with special emphasis on its degeneration. Folia biol. (Kraków) 58: 217-227. The midgut epithelium of Nicoletia phytophila is composed of columnar digestive cells and regenerative cells that form regenerative nests. The cytoplasm of midgut epithelial cells shows typical regionalization in organelle distribution. Two types of regenerative cells have been distinguished: cells which are able to divide intensively and cells which differentiate. Spot desmosomes have been observed between neighboring regenerative cells. The occurrence of intercellular junctions is discussed. The midgut epithelium degenerates both in an apoptotic and necrotic way. Necrosis proceeds during each molting period (cyclic manner), while apoptosis occurs between each molting, when the midgut epithelium is responsible for e.g. digestion. These processes of epithelium degeneration are described at the ultrastructural level. Our studies not only add new information about fine structure of the midgut epithelium of N. phytophila, but contribute to resolving the relationships within the Zygentoma. There are no doubts about the very close sister position of Nicoletiidae and Ateluridae. The midgut epithelium characters confirm their close relationship. However we do not recommend classifying the atelurid genera only within Nicoletiidae: Nicoletiinae. Key words: Midgut epithelium, cell death, apoptosis, degeneration, ultrastructure. Magdalena M. ROST-ROSZKOWSKA, £ukasz CHAJEC, University of Silesia, Department of Animal Histology and Embryology, Bankowa 9, 40-007 Katowice, Poland. E-mail: [email protected] Jitka VILIMOVA, Charles University, Faculty of Science, Department of Zoology, Vinicna 7, 128 44 Praha 2, Czech Republic. E-mail: [email protected] The primitively wingless insect taxon Zygen- dae, containing one species from northern toma was originally classified in Thysanura La- California, is a putative relict and its phylogenetic treille, 1831 together with several other groups. position has been variably asigned (e.g. GIRIBET et al. TheZygentomahasbeenmostlyacceptedasanin- 2004). The classification of the two following taxa dependent taxon within the Ectognatha (Insecta s. is not still clarified. MENDES (1988) accepted two str.). The history of its classification was summa- independent families, Ateluridae and Nicoletiidae. rized by MENDES (2002a). The Archaeognatha, He mentioned the history of their classification, the second primitively wingless insect taxon, is a concerning the rank of Nicoletiidae from a sub- group closely related to Zygentoma. Their interre- family in Lepismatidae as a separate family. The lationships and relationship to Entognatha and family Ateluridae is the most diverse taxon of Zy- Pterygota are mostly resolved and accepted (e.g. gentoma, with 56 genera and about 113 species GRIMALDI &ENGEL 2005; MACHIDA 2006; GAO (MENDES 1988, 2002a). The family Nicoletiidae et al. 2008). However, the interrelationships of the was subdivided by MENDES (1988) into five sub- zygentoman subgroups are still unclear. families. The most common and widespread zygentoman The phylogenetic relationships among these family, Lepismatidae, is generally accepted, as subfamilies were described as follows (MENDES wellasthefamilyMaindroniidaewithonlyonege- 1994). The Protrinemurinae is a relict and the most nus from South America. The family Lepidotrichi- plesiomorphic group, the closest taxon, Coletinii- _______________________________________ *Supported by a grant of the Ministry of Education of the Czech Republic, MSM 0021620828, to J. VILIMOVA. 218 M.M.ROST-ROSZKOWSKA etal. nae, are clearly isolated from the remaining taxa. ronmental constraints and therefore bear impor- The Nicoletiinae, characterized only by plesio- tant phylogenetic information. Recently, KOCH & morphies,seemstobewellindividualized.Thead- DOLGENER (2008) proposed an absence of midgut vanced Cubacubaninae and Subnicoletiinae are caeca as a new synapomorphy of nicoletiids and certainly closely related. atelurids. SMITH (1998) did not accept MENDES’s (1994) The zygentoman taxa were studied by the senior proposal of the Zygentoma classification. He con- author, with co-authors respectively, concerning sidered only four families, the Lepismatidae and the comparative morphology of midgut epithelium closely related relict Maindroniidae, and relict ultrastructure (e.g. ROST 2006a; ROST et al. 2005; Lepidotrichidae closely related to Nicoletiidae, ROST-ROSZKOWSKA et al. 2007b). Since Atelura occurring in all zoogeographical regions and in- formicaria Heyden, 1855, the nominotypical spe- cluding also former Ateluridae. As the Nicoletiidae cies of the taxon Ateluridae/Atelurinae, was also are subdivided only into two subfamilies, Nico- studied (ROST-ROSZKOWSKA et al. 2010), a com- letiinae and Atelurinae, the subfamilies of MEN- parative description of the midgut epithelium of DES (1988, 1994) are treated as genera. Nicoletia phytophila, the nominotypical species of MENDES (2002b) as well other authors (e.g. the taxon Nicoletiidae, is warranted, and may con- KOCH 2003) accepted the lower rank of the Atelu- tribute to resolving the interrelationships of the ridae as a subfamily in Nicoletiidae, and proposed taxa Ateluridae and Nicoletiidae within the Zy- a dendrogram of the five nicoletiid subfamilies in gentoma. Both recognized manners of midgut which Protrinemuridae was treated as an inde- epithelial cell degeneration, apoptosis and necro- pendent family. The Atelurinae are strictly related sis, in these basal taxa of the Ectognatha are com- to Coletiniinae and both of them to the Nicoleti- pared. inae. The most recent study on the comparative analy- sis of sperm structure in the Zygentoma (DALLAI Material and Methods et al. 2004) again treated Ateluridae and Nicoleti- idae as separate families. The reconstruction of Material examined phylogenetic hypothesis suggests a close relation- ship between these two families, which seem to be Adult specimens of Nicoletia phytophila Ger- the most advanced zygentomans. The basal family vais, 1844 (Zygentoma: Nicoletiidae: Nicoletii- istheLepismatidae,nottheLepidotrichidae,asthe nae) were collected from artificial termite nests of former authors accepted, if the Zygentoma is di- Neotermes castaneus (Burmeister, 1839) and Neo- vided into two groups, Lepidotrichidae + Euzy- termes cubanus (Snyder, 1922) (Isoptera: Kaloter- gentoma with the other families. mitidae) in Prague, Czech Republic, by Dr. Ivan The subfamily Nicoletiinae, or Nicoletia group, Hrdý and Prof. Ivan Hrdý (October 2008). The ter- is monotypic, with the species Nicoletia phyto- mites originated from Cuba, Topes de Collantes. phila Gervais, 1844. This parthenogenetic species The determination of the material was confirmed has recently become widely distributed almost by Prof. Luis Espinasa. worldwide,probablybecauseofanthropogenicac- tivities (SMITH 1998). Nicoletia phytophila was mentioned from Europe only from Italy Methods (MOLERO-BALTANÁS et al. 2000), however, this old record was most probably a misidentification Light and transmission electron microscopy with Coletinia species. Besides the morphology, the ultrastructure of vitellogenesis in Nicoletia About 20 adult specimens of Nicoletia phyto- phytophila was studied (SZKLARZEWICZ 1989), phila were fixed in 2.5% glutaraldehyde (24 h, with results confirming its relation to Lepismati- o o temp. 4 C), postfixed in 2% OsO4 (2h, temp. 4 C), dae. dehydrated in a graded series of ethanol (30, 50, The Zygentoma are mostly diurnal and omnivo- 70, 90, 96 and 100%, each for 10 min) and acetone rouswiththenotableexceptionofthefamilyNico- (15 min). After immersion in acetone – epon resin letiidae which is principally subterranean and (1:1) overnight (room temperature), the material vegetarian after GRIMALDI &ENGEL (2005). was embedded in Epon 812 and polymerized in Since the Nicoletiidae are vegetarian and the Ate- 80oC. Semi- and ultra-thin sections were cut on a luridae omnivorous, different structure of their Leica Ultracut UCT25 ultramicrotome. Semi-thin midgut can be hypothesized, reflecting different sections were stained with 1% methylene blue in kinds of food (e.g. TERRA et al. 1996). Otherwise 0.5% borax and observed with an Olympus BX60 the midgut characters are not influenced by envi- light microscope. Ultra-thin sections were stained StructureoftheMidgutEpitheliumof Nicoletiaphytophila 219 with uranyl acetate and lead citrate and examined No differences in the ultrastructure of epithelial with a Hitachi H500 transmission electron micro- and regenerative cells were observed along the scope at 75 kV. sack-shaped midgut. Apoptosisandnecrosisinthemidgutepithelium Results of N. phytophila FinestructureofmidgutepitheliuminN.phytophila The midgut epithelium of N. phytophila degen- erates both in an apoptotic and necrotic way. Ne- The midgut of N. phytophila has a sack-like crosis occurs during each molting period (N. shape, which is devoid of midgut caeca, character- phytophila is a species which molts throughout istic for insects. Its epithelium is composed
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