On Some Terms Used in the Cytogenetics and Reproductive Biology of Scale Insects (Homoptera: Coccinea)

On some terms used in the cytogenetics and reproductive biology of scale insects (Homoptera: Coccinea)

I.A. Gavrilov1, V.G. Kuznetsova2

Zoological Institute, Russian Academy of Sciences, Universitetskaya nab. 1, St.Petersburg 199034, Russia. E-mails: [email protected], [email protected]

Abstract. The significance and validity of some terms conventionally used in papers on coccid cytogenetics and reproductive biology are discussed, and some suggestions are made for the terminology to be more correct in describing of remarkable phenomena and processes associated with coccid reproduction and individual development. It is proposed to apply the terms “Lecanoid”, “Comstockiella” and “Diaspidid” referring to the genetic systems of scale insects not only to bisexually reproducing species, but also to parthenogenetic species and populations showing heterochromatinization of paternal set of chromosomes (PGH) during the development of male embryos. It is also proposed to unify the spelling of the above terms as follows: Lecanoid, Comstockioid and Diaspidoid. The classification of the known types of parthenogenesis of scale insects is revised, and the occurrence of facultative and obligatory parthenogeneses is discussed. The existence of true viviparous scale insects is questioned, and the term “ovoviviparity” (instead of “viviparity”) is treated to be the only proper one for all the hitherto studied species with embryonic development inside the mother’s body. The fusions of a cleavage nucleus with polar bodies resulting in the so-called “dizygotic soma” characteristic of the pseudococcid and diaspidid embryonic development is proposed to designate as the “Schrader fusions” in honor of Franz Schrader, the discoverer of this unique phenomenon. Key words: genetic systems, paternal genome heterochromatinization, parthenogenesis, ovoviviparity.

The cytogenetics of the scale insects has a This paper is aimed to revise, update and unify long history. During nearly 100 years a number of coccid terminology, and to compare the significance the world’s eminent cytogeneticists were studying of some terms with analogous ones in other groups the remarkable genetic systems of scale insects of insects. In this paper we shall discuss the basic and have elaborated the special terminology for terminology for (1) genetic systems, (2) partheno- different processes and phenomena associated with genesis, (3) strategy of birth and (4) “dizygotic” coccid reproduction and individual development. development of scale insects. A review of the considerable literature on the subject and our own studies of many coccid species Genetic systems led the authors to conclude that some terms are First we have to clarify what we mean by “ge- incorrect or only partially correct and, addition- netic systems”. In line with Nur (1980), White ally, not easily accessible to non-coccidologists. (1973), and Normark (2003) we treat genetic

Free access: www.zin.ru/journals/compcyt 170 I.A. Gavrilov, V.G. Kuznetsova system as a combination of sex-determining sification of coccid genetic systems has been elabo- mechanisms, chromosome behavior in meiosis and rated by Nur (1980), based on his own study and modes of reproduction (bisexual, parthenogenetic that of earlier workers. In the papers of all the or hermaphroditic). For details the reader is re- above-mentioned authors the three principal ge- ferred to the authoritative reviews by Hughes- netic systems, Lecanoid, Comstockiella, and Schrader (1948), Brown (1965), Nur (1980), and Diaspidid, have originally been considered as bi- Normark (2001) as well as to our review in Rus- sexual, because all these systems are associated sian (Kuznetsova and Gavrilov, 2005). Here we with PGH (Lecanoid) or with PGH followed by will discuss only the systems with the special pa- PGE (Comstockiella and Diaspidid) that occur ternal genome heterochromatinization (PGH) and during embryogenesis or prior to spermatogen- elimination (PGE), that is, the systems where the esis. It is necessary at this stage to briefly charac- paternal set of chromosomes is rendered inactive terize these systems. In each above system a male in most tissues by heterochromatinization during develops from a diploid zygote, containing one the development of male embryos. We shall make haploid genome of maternal origin and one hap- a brief retrospective journey into the history of loid genome of paternal origin. However the pa- names of these systems. ternal set of chromosomes becomes heterochro- Hughes-Schrader (1948) was the first to clas- matic and genetically inert in early embryogenesis, sify the coccid genetic systems. Based on 31 spe- hence only the maternal genome is in fact trans- cies of scale insects studied at that point in time, mitted by the sperm to the next generation. The mainly by her and Franz Schrader, Salli Hughes- difference is that in the Lecanoid system the hetero- Schrader described different forms of partheno- chromatic complement is maintained as such dur- genesis, different special types of meiosis and ing development, whereas in the two remaining unique examples of hermaphroditism. In her re- systems it is completely (Diaspidid) or partly view, Hughes-Schrader used the term “Lecanoid” (Comstockiella) eliminated just prior to the first meiosis for a type of spermatogenesis discovered prophase of spermatogenesis. Of the three sys- in several species of mealybugs (from the genera tems, the Comstokiella system seems to be the Pseudococcus Westwood, 1840 and Phenacoc- most wide-spread chromosome system in coccus Cockerell, 1893), soft scales (from the gen- cids (Nur, 1980). era Coccus Linnaeus, 1758, Saissetia Deplanche, We emphasize however, that it is far not always 1859 and Parthenolecanium Šulc, 1908), a spe- easy to unequivocally diagnose just what system cies of felt scales (Gossyparia spuria (Modeer, is characteristic of a species under study. Further 1778)) and an unidentified species of the genus still some species can be equally referred as having Dactilopius Costa, 1829. At the time, the above one or another system. For example, if males are listed groups were classified as a “section Leca- absent, the genetic system would hence be noidae” in contrast to the sections “Margaroidae” considered as parthenogenesis. However, it is and “Diaspidoidae”. More recently, Brown (1963, currently definitely established that many scale 1965), based on the study of numerous species of insect species combine thelytokous reproduction armored scales (Diaspididae), coined the terms with amphimixis, producing males amphimictically “Comstockiella” and “Diaspidid” to designate the or parthenogenetically, and parhtenogenetically genetic systems, discovered by him for the first produced males also have PGH/PGE. Moreover, time respectively in the genus Comstockiella some species variously manifest thelytokous and Cockerell, 1896 and in some genera of the sub- sexual lineages in different geographical regions or family Diaspidinae. The most comprehensive clas- on different host plants. In spite of these facts,

Comp. Cytogenet., 2007. 1(2) On some terms used in the cytogenetics and reproductive biology of Coccinea 171 which have already been well known in those days, advised to consult White’s (1973) review. Suo- Nur (1980) classified the systems with PGH/PGE malainen et al. (1987) described different mecha- as either purely sexual or parthenogenetic only, then nisms accounting for parthenogenetic develop- an unequivocal identification of the genetic system ment. The most common forms of parthenogen- in many species is unnecessarily complicated (if esis are arrhenotoky, deuterotoky and thelitoky. not impossible). If one follows the Nur’s classi- In arrhenotoky, insects are haplodiploid, with hap- fication, two or even more genetic systems could loid males developing from unfertilized eggs while be assigned to one and the same species. A curious diploid females developing from fertilized diploid situation occurs in the family Lecaniidae (currently eggs. Deuterotoky involves the development of Coccidae) that according to Nur (1980) does not unfertilized eggs in either males or females. have Lecanoid system. The solution of the problem Thelitoky is a form of complete parthenogenesis is to consider PGH/PGE separately from the mode where unfertilized eggs develop in diploid females, of reproduction. The PGH is known to constitute therefore, thelitokous species have females only. a fundamental characteristic of chromosomal Among insects, coccids are well known to behavior in coccid meiosis. It seems to have have a unique diversity of the types of partheno- evolved only once, in the basic phylogenetic line genesis (Nur, 1971). Parthenogenetic species and of scale insects (represented by the superfamily races have been repeatedly described in the fami- Coccoidea), and then three main genetic systems, lies Margarodidae, Pseudococcidae, Coccidae, in order of increasing complexity, sequentially Asterolecaniidae, and Diaspididae (Hughes- developed on the basis of PGH. Parthenogenesis Schrader, 1948; Brown, 1965; Nur, 1971, 1980, is in its turn a mode of reproduction, and it has 1990; Gavrilov, 2007). In the classification of the evolved independently in a number of species and types of parthenogenesis the following characters has been reported in different coccid taxa (as with are conventionally used: the mode of reproduc- or without PGH/PGE). Parthenogenetic lines are tion (obligatory = permanent, and facultative), the known to arise occasionally under certain eco- sex of progeny (arrhenotoky, thelytoky, and deu- logical and geographical factors. Thus, we propose terotoky) and some fundamental cytogenetical traits to apply the terms “Lecanoid”, “Comstockiella” (generative = haploid, and somatic, that is in turn and “Diaspidid” not only to bisexually reproducing subdivided into apomictic and automictic). How- species but also to facultatively parthenogenetic ever, in scale insects some complicated patterns species and populations having PGH/PGE. We of parthenogenesis occur that embarrass the clas- find it also necessary to unify the terminology for sification. Many authors have attempted to clas- genetic systems designating them as «Lecanoid», sify coccid parthenogeneses (Thomsen, 1927; «Comstockioid», and «Diaspidoid», and write Hughes-Schrader, 1948; Nur, 1971, 1972, 1980). these names from the capital letter. This unification In the most recent classification (Nur, 1980) sev- will thus allow do not confuse the names of genetic eral types of parthenogenesis are recognized based systems with the names of taxonomic groups. on 1) sex of progeny; 2) ploidy of males (haploid and diploid arrhenotoky); 3) number of chromosomes in oogonia and in the first metaphase of Parthenogenesis oogenesis (gonoid and agonoid thelytoky); each Parthenogenesis where virgin females produce of the two last types is additionally subdivided into offspring represents one of the common modes of subtypes based on the mechanism of diploidy res- reproduction in insects. For all the groups in which titution. Nur (1980) rejected such traditional terms parthenogenesis has been found the reader is as “obligatory” and “facultative” parthenogenesis

Comp. Cytogenet., 2007. 1(2) 172 I.A. Gavrilov, V.G. Kuznetsova since in many parthenogenetic scale insects males cally, it should also be mentioned that achiasmatic are sometimes present but do not participate in meiosis occurs in many insect orders, e.g. Meco- fertilization. He also rejected the terms “meiotic” ptera, Orthoptera, Trichoptera, Lepidoptera, and “ameiotic” parthenogenesis since, according Heteroptera, Diptera and Coleoptera, however to his studies (Nur, 1979), some parthenogenetic has never been evidenced for Coccinea and other species, even though they show no pairing of chro- homopteran insects. mosomes in meiosis, have however two divisions Thirdly, the formation of bivalents is thought to – reductional and equational. Therefore, Nur be important for regular segregation of homologues (1980) proposed to replace these terms by some in anaphase, and the lack of chromosome pairing alternative terms – “gonoid” and “agonoid” in coccid meiotic prophase (Nur, 1979) is then thelytoky, which we have mentioned above. These the phenomenon calling for further investigation. innovations, however, can not be considered ap- Finally, discarding of traditional terminology to- propriate. gether with the invention of new terms would act Firstly, without a special sophisticated investi- as a barrier to communication between cocci- gation, it is difficult to say with certainty whether a dologists and specialists on other groups having species has an obligatory or facultative partheno- similar reproductive strategies, including parthe- genesis. It seems quite clear that only few species nogenesis. It should be added that based on the with obligatory parthenogenesis occur in Coccinea. Nur’s (1980) terminology, several types of par- The evidence for this view is that in the Nur’s thenogenesis could be attributed to a species, for (1990) list all species considered as obligatory par- example to Coccus hesperidum Linnaeus, 1758, thenogenetic, have in fact a mixed reproductive which, according to Nur (1979, 1980), has apo- strategy and include both parthenogenetic and bi- mixis and amphimixis, gonoid and agonoid sexual forms associated with different host plants. thelytoky. The taxonomical status of these forms, whether or Thus, we suggest to recognize obligatory and not they represent separate species, has been re- facultative parthenogenesis; use only conventional peatedly discussed in the literature (see Nur, 1990), terminology for pathenogenesis (arrhenotoky, but still remains disputable. For example, Euro- thelytoky and deuterotoky, meiotic and ameiotic pean species Marchalina hellenica (Gennadius, parthenogenesis), and reject the terms gonoid and 1883) (Margarodidae) was reported as obliga- agonoid thelytoky. tory thelytokous because males are absent (Ho- vasse, 1930), and females have no spermatheca Strategy of birth (Marzo et al., 1990). The males are however There are three known strategies of birth such claimed to occur in some regions ( S. Drosopoulos as oviparity, ovoviparity and viviparity, and all of and Ch. Hodgson, personal communications). these occur in insects. Oviparous insects lay eggs Males were also found in Marchalina caucasica with little or no emryonic development within the Hadzibeyli, 1969, which is considered as a syn- mother’s body. In ovoviviparity, eggs remain within onym of M. hellenica (Jashenko, 1999). the mother’s body until they hatch or are about to Secondly, the very existence of chromosomal hatch. Ovoviviparity differs from viviparity in that reduction in oogenesis is sufficient to classify the the ovoviviparous embryos are nourished by the parthenogenesis as that of meiotic type. It is pres- egg yolk rather than the mother’s body. Ovovivi- ently widely known that in many insects bivalents parity is diplayed by many insects and is suggested are formed, however crossing-over is absent, and to be widely distributed among Coccinea, how- meiosis is achiasmatic (White, 1973). Parentheti- ever only few publications deal with this pheno-

Comp. Cytogenet., 2007. 1(2) On some terms used in the cytogenetics and reproductive biology of Coccinea 173 menon in scale insects (Hagan, 1951; Koteja, Dizygotic development 1990; Tremblay, 1997). As is customary when coc- Some scale insects are characterized by a very cidologists describe species, they use the terms specific pattern of individual development that “viviparity” and “ovovivivparty” without comments bears some similarity to a “double” fertilization and probably without clear understanding differ- resulting in the formation of triploid endosperm in ences between these two terms. Hagan (1951) in the angiospermous plants. In species of the coc- his famous fundamental monograph gave a clear cid families Pseudococcidae and Diaspididae an definition of the ovoviviparity to distinguish it from embryo is known to develop from two different viviparity: “The egg contains sufficient yolk to nour- cells. One of these cells is a normal diploid zygote ish the embryo until hatching and maternal depo- that gives rise to the majority of insect tissues. The sition of offspring. No special nutritional structures other cell is a polyploid secondary zygote that re- are developed”. Yet another important character of the ovoviparous development is the presence sults from the fusion of a cleavage nucleus with of a clearly visible chorion covering the egg. Ev- polar bodies. The secondary zygote gives rise to erything considered, all hitherto studied scale in- a polyploid bacteriome, or mycetome. Thus, in the sects are ovoviviparous. Tremblay (1997) hold the latter, each cell includes a haploid set of paternal same viewpoint regarding soft scales and scale chromosomes and several maternal complements insects in general. Alternatively, Koteja (1990), (Schrader, 1923; Hughes-Schrader, 1948; Brown, based on Buchner’s (1965) anatomical studies of 1965; Normark, 2001). Stictococcus and Amiomorpha species, made a It is surprising, however, that there is no spe- conclusion that “distinction between oviparity and cial term for cytogenetic processes followed by ovoviviparity is not clear” and speculated that the the formation of “dizygotic” soma. The absence above species are viviparous and receive nour- of such term renders it difficult to discuss this spe- ishment from the mother’s body. However, cial evolutionary pattern in scientific and, especially, Buchner took an interest in endosymbionts, but educational papers and books, and also the com- not in the mode of embryonic development of the munication with other biologists. Here, we pro- species under investigation, therefore, additional pose to designate fusions between a cleavage studies are required to solve the problem. Based nucleus and polar bodies in the course of on the current knowledge on the subject and our pseudococcid and diaspidid embryonic develop- own data on more than 100 species from 9 fami- ment as “Schrader fusions” in honor of the out- lies (unpublished), the eggs of scale insects always standing geneticist Franz Schrader, the discoverer have both chorion and yolk, so they are clearly of this unique phenomenon. ovoviviparous. We cannot exclude, however, that during further investigation of scale insects, espe- ACKNOWLEDGEMENTS cially from the tropics, species with true viviparity will be discovered. So long as the issue remains This study was supported (for I.G.) by the grant open, while making the preparation of scale in- of the President of the Russian Federation MK - sects, special attention should be given to stage of 353.2007.4 and by INTAS PhD Fellowship grant the egg development inside the mother’s body and No. 06-1000014-5958, and (for V.K.) by the to the presence of chorion and yolk in the eggs. Russian Foundation for Basic Research (Grant 05- This evidence may have important implications for 04-48387) and the Program of the Presidium RAS both general biology of scale insects and taxonomi- “Dynamics of gene pools in plants, animals and cal conclusions (Williams, 1985; Danzig, Gavrilov, man”. 2005).

Comp. Cytogenet., 2007. 1(2) 174 I.A. Gavrilov, V.G. Kuznetsova

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