Eur. J. Entomol. 107 (4): 589-595, 2010 | 10.14411/eje.2010.068

Germ cell cluster formation and ovariole structure in Puto albicans and Crypticerya morrilli (Hemiptera: Coccinea). Phylogenetic implications

Teresa SZKLARZEWICZ, Anna MICHALIK, Anna CZAJA, Sylwia SZYDLOWSKA
Department of Systematic Zoology and Zoogeography, Institute of Zoology, Jagiellonian University, R. Ingardena 6,

The organization and development of ovaries in representatives of two families (Putoidae and Monophlebidae) of scale insects are described. Developing ovaries of Puto albicans McKenzie, 1967 and Crypticerya morrilli (Cockerell, 1914) consist of numerous clusters of cystocytes that are arranged in the form of rosettes. At the end of the last nymphal instar these clusters start to protrude from the interior of the ovary into the body cavity and the ovarioles begin to be formed. The ovary of a young female is composed of about 200 spherical telotrophic ovarioles devoid of terminal filaments. The ovarioles of C. morrilli contain 8 germ cells (7 trophocytes and a single oocyte). From 25 to 45 germ cells (23-43 trophocytes and 2 or 3 oocytes) occur in the ovarioles of P. albicans. An ovariole of an adult female is subdivided into a trophic chamber (tropharium), vitellarium and ovariolar stalk (pedicel). At each stage of development, the ovaries are accompanied by large cells (termed bacteriocytes) that contain endosymbiotic microorganisms. The organization of the ovary in P. albicans is more similar to that in archaeococcoid scale insects than in neococcoid taxa. In contrast, the number of germ cells per ovariole in C. morrilli is not typical of other archaeococcoids, but resembles the derived condition seen in other iceryine taxa. The classification and phylogeny of scale insects are discussed in the light of these results.

Keywords: Coccinea, Putoidae, Monophlebidae, Puto albicans, Crypticerya morrilli, scale insects, ovaries, clusters of germ cells, telotrophic ovariole, oogenesis, endosymbiotic microorganisms, phylogeny

Received: March 19, 2010; Accepted: June 17, 2010; Published: October 20, 2010

Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)


    • Open full article

    References

    1. BAUMANN P. 2005: Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu. Rev. Microbiol. 59: 155-189 Go to original source...
    2. BEARDSLEY J.W. 1969: A new fossil scale insect (Homoptera: Coccoidea) from Canadian amber. Psyche 76: 270-279 Go to original source...
    3. BIELENIN I. 1962: Anatomical and histochemical investigations on the genus Lecanium Burm. Part. I. Female reproductive organs of Lecanium pomeranicum Kaw. (Homoptera, Coccoidea). Acta Biol. Crac. (Zool.) 5: 9-25
    4. BILINSKI S.M., BUNING J. & SIMICZYJEW B. 1998: The ovaries of Mecoptera: basic similarities and one exception to the rule. Folia Histochem. Cytobiol. 36: 189-196
    5. BLACKMAN R.L. 1985: Aphid cytology and genetics. In Szelegiewicz H. (ed.): Evolution and Biosystematics of Aphids. Proceedings of the International Symposium at Jablonna. Ossolineum, Wroc³aw, pp. 171-237
    6. BORCHSENIUS N. 1956: The question of the course of evolution of Coccoidea (Insecta, Homoptera) . Zool. Zh. 35: 546-553 [in Russian]
    7. BROWN S.W. & CLEVELAND C. 1968: Meiosis in the male of Puto albicans (Coccoidea, Homoptera). Chromosoma 24: 210-232 Go to original source...
    8. BUCHNER P. 1965: Endosymbiosis of Animals with Plant Microorganisms. Interscience, New York, 909 pp
    9. BUNING J. 1985: Morphology, ultrastructure and germ cell cluster formation in ovarioles of aphids. J. Morphol. 86: 209-221 Go to original source...
    10. BUNING J. 1994: The ovary of the Ectognatha, the Insecta s. str. In Buening J. (ed.): The Insect Ovary: Ultrastructure, Previtellogenic Growth and Evolution. Chapman and Hall, London, pp. 32-400 Go to original source...
    11. COOK L.G., GULLAN P.J. & TRUEMAN H.E. 2002: A preliminary phylogeny of the scale insects (Hemiptera: Sternorrhyncha: Coccoidea) based on nuclear small-subunit ribosomal DNA. Mol. Phyl. Evol. 25: 43-52 Go to original source...
    12. DOUGLAS A.E. 1989: Mycetocyte symbiosis in insects. Biol. Rev. 64: 409-434 Go to original source...
    13. FOLDI I. 2005: Ground pearls: a generic revision of the Margarodidae sensu stricto (Hemiptera: Sternorrhyncha: Coccoidea). Ann. Soc. Entomol. Fr. (N.S.) 41: 81-125 Go to original source...
    14. GULLAN P.J. & COOK L.G. 2007: Phylogeny and higher classification of the scale insects (Hemiptera: Sternorrhyncha: Coccoidea). Zootaxa 1668: 413-425
    15. GULLAN P.J. & SJAARDA W. 2001: Trans-Tasman Platycoelostoma Morrison (Hemiptera: Coccoidea: Margarodidae) on endemic Cupressaceae, and the phylogenetic history of margarodids. Syst. Entomol. 26: 257-278 Go to original source...
    16. HODGSON C. & FOLDI I. 2006: A review of the Margarodidae sensu Morrison (Hemiptera: Coccoidea) and some related taxa based on the morphology of adult males. Zootaxa 1263: 1-250
    17. HUGHES-SCHRADER S. 1927: Origin and differentiation of the male and female germ cells in the hermaphrodite of Icerya purchasi (Coccidae). Z. Zellforsch. 6: 509-540 Go to original source...
    18. HUGHES-SCHRADER S. 1944: A primitive coccid chromosome cycle in Puto sp. Biol. Bull. 87: 167-176 Go to original source...
    19. HUGHES-SCHRADER S. 1948: Cytology of coccids (Coccoidea, Homoptera). Adv. Genet. 2: 127-203 Go to original source...
    20. JAGLARZ M.K. 1998: The number that counts. Phylogenetic implications of the number of nurse cells in ovarian follicles of Coleoptera, Adephaga. Folia Histochem. Cytobiol 36: 167-178
    21. JURA C. 1958: The early developmental stages of ovoviviparous scale insect Quadraspidiotus ostreaeformis (Curt.) (Homoptera, Coccidae, Aspidiotini). Zool. Polon. 9: 17-34
    22. KONDO T., GULLAN P.J. & WILLIAMS D.J. 2008: Coccidology. The study of scale insects (Hemiptera: Sternorrhyncha: Coccoidea). Rev. Corpoica - Cienc. Tec. Agr. 9: 55-61
    23. KOTEJA J. 1974: On the phylogeny and classification of the scale insects (Homoptera, Coccinea) (discussion based on the morphology of the mouthparts). Acta Zool. Crac. 14: 267-325
    24. KOTEJA J. 1996: Scale insects (Homoptera: Coccinea) a day after. In Schaefer C.W. (ed.): Studies of Hemipteran Phylogeny. Proceedings of Thomas Say Publications in Entomology. Entomological Society of America, Lanham, Maryland, pp. 65-88
    25. KOTEJA J., PYKA-FOSCIAK G., VOGELGESANG M. & SZKLARZEWICZ T. 2003: Structure of the ovary in Steingelia (Sternorrhyncha: Coccinea), and its phylogenetic implications. Arthr. Struct. Dev. 32: 247-256 Go to original source...
    26. KSIAzKIEWICZ M. 1980: Ultrastructure of the trophic chamber and nutritive cord of Aspidiotus hederae (Homoptera, Coccoidea). Cell Tiss. Res. 213: 149-157 Go to original source...
    27. KUBRAKIEWICZ J., BILINSKI S.M. & MAZURKIEWICZ M. 1998a: Diptera - ovary structure and oogenesis in midges and flies. Folia Histochem. Cytobiol. 36: 197-203
    28. KUBRAKIEWICZ J., JcDRZEJOWSKA I. & BILINSKI S.M. 1998b: Neuropteroidea - different ovary structure in related groups. Folia Histochem. Cytobiol. 36: 179-187
    29. MAGAKYAN Y.A., MAKARYAN S.R., PETROSSYAN A.V., MKTCHYAN L.P., ABROYAN L.O. & HAKOPYAN L.A. 1975: The oogenesis of the ararat cochineal (Porphyrophora hamelli Brandt). I. Histomorphological characteristics of the formation of follicular apparatus and the development of oocytes. Cytologia 18: 932-936 [in Russian]
    30. MCKENZIE H.L. 1967: Mealybugs of California with Taxonomy, Biology, and Control of North American Species (Homoptera: Coccoidea: Pseudococcidae). University of California, Berkeley, 526 pp
    31. MICHALIK A., JANKOWSKA W. & SZKLARZEWICZ T. 2009: Ultrastructure nad transovarial transmission of endosymbiotic microorganisms in Conomelus anceps and Metcalfa pruinosa (Insecta, Hemiptera, Fulgoromorpha). Folia Biol. (Krakow) 57: 131-137 Go to original source...
    32. MILLER D.R. & KOSZTARAB M. 1979: Recent advances in the study of scale insects. Annu. Rev. Entomol. 24: 147-152 Go to original source...
    33. MILLER D.R. & MILLER G.L. 1993: A new species of Puto and preliminary analysis of the phylogenetic position of the Puto group within the Coccoidea (Homoptera: Pseudococcidae). Jeffersoniana 4: 1-35
    34. MORRISON H. 1928: A classification of the higher groups and genera of the coccid family Margarodidae. US Dep. Agr. Wash. Tech. Bull. 52: 1-237
    35. NIzNIK S. & SZKLARZEWICZ T. 2007: Structure and development of hermaphroditic gonad in Icerya purchasi (Insecta, Hemiptera, Coccinea: Monophlebidae). Zool. Polon. 52: 71-90
    36. SIMICZYJEW B., OGORZALEK A. & STYS P. 1998: Heteropteran ovaries: variations on the theme. Folia Histochem. Cytobiol. 36: 147-156
    37. SZKLARZEWICZ T. 1997: Structure and development of the telotrophic ovariole in ensign scale insects (Hemiptera, Coccomorpha: Ortheziidae). Tiss. Cell 29: 31-38 Go to original source...
    38. SZKLARZEWICZ T. 1998a: The ovaries of scale insects (Hemiptera, Coccinea). Morphology and phylogenetic conclusions. Folia Histochem. Cytobiol. 36: 157-165
    39. SZKLARZEWICZ T. 1998b: Structure of ovaries of scale insects. I. Pseudococcidae, Kermesidae, Eriococcidae, and Cryptococcidae (Insecta, Hemiptera, Coccinea). Int. J. Insect Morphol. Embryol. 27: 162-172
    40. SZKLARZEWICZ T. 1998c: Structure of ovaries of scale insects. II. Margarodidae (Insecta, Hemiptera, Coccinea). Int. J. Insect Morphol. Embryol. 27: 319-324 Go to original source...
    41. SZKLARZEWICZ T. & BILINSKI S.M. 1995: Structure of ovaries in ensign scale insects, the most primitive representatives of Coccomorpha (Insecta, Hemiptera). J. Morphol. 224: 23-29 Go to original source...
    42. SZKLARZEWICZ T. & MOSKAL A. 2001: Ultrastructure, distribution, and transmission of endosymbionts in the whitefly Aleurochiton aceris Modeer (Insecta, Hemiptera, Aleyrodinea). Protoplasma 218: 45-53 Go to original source...
    43. SZKLARZEWICZ T., WNcK A. & BILINSKI S.M. 2000: Structure of ovarioles in Adelges laricis, a representative of the primitive aphid family Adelgidae. Acta Zool. Stockholm 81: 307-313 Go to original source...
    44. SZKLARZEWICZ T., KcDRA K. & NIzNIK S. 2005: Ultrastructural studies of the ovary of Palaeococcus fuscipennis (Burmaister) (Insecta, Hemiptera, Coccinea: Monophlebidae). Folia Biol. (Krakow) 53: 45-50 Go to original source...
    45. SZKLARZEWICZ T., KcDRA K. & NIzNIK S. 2006: Ultrastructure and transovarial transmission of endosymbiotic microorganisms in Palaeococcus fuscipennis (Burmeister) (Insecta, Hemiptera, Coccinea: Monophlebidae). Folia Biol. (Krakow) 54: 70-74 Go to original source...
    46. UNRUH C.M. 2008: A taxonomic review of the Crypticerya species (Hemiptera: Coccoidea: Monophlebidae) of the southwestern United States and Mexico, including description of a species from Baja California. Zootaxa 159: 1-42
    47. WcGLARSKA B. 1961: Oogenesis in the ovoviviparous scale insect Quadraspidiotus ostreaeformis Curt. (Homoptera, Coccidae, Aspidiotini). Part I. Morphological and cytological investigations. Zool. Polon. 11: 267-294
    48. WITEK A. 2002: Ovariole Structure in Eulecanium tiliae and Ceroplastes sp. (Insecta, Hemiptera, Coccinea: Coccidae). MSc Thesis. Department of Systematic Zoology and Zoogeography, Jagiellonian University [in Polish]