- wS I - %a X > a JUL26 1978 J Med Genet: first published as 10.1136/jmg.15.3.165 on 1 June 1978. Downloaded from Review article LIEDEIIL LOIES DIV. Journa oiec,-181 Parthenogenesis URSULA MITTWOCH From The Galton Laboratory, Department of Human Genetics, University College London, Wolfson House, 4 Stephenson Way, London NWI 2HE 'Behold, a virgin shall conceive, and bear a son, and means 'the development of the egg cell into a new shall call his name Immanuel.' The most famous individual without fertilization', and this simple reference to virgin birth is actually based on a definition is adequate for many lower animals. In other mistranslation, for the Hebrew word almah, in Isaiah animals, however, embryos produced without fer- 7, 14, means a young woman, and not necessarily a tilisation suffer a high mortality, a fact that is reflected virgin. In the New English Bible the quotation begins: in the definition of parthenogenesis by Beatty (1957) 'A young woman is with child.' as 'the production of an embryo from a female gamete In non-human mammals also claims of virgin births without the concurrence of a male gamete, and with or have not so far withstood the rigours of scientific without eventual development into an adult'. Beatty examination. Nevertheless, parthenogenesis is a (1967) subsequently modified this definition by sub- phenomenon of undoubted biological interest which stituting 'without any genetic contribution from a male leads to the production of living young in many types gamete' for 'concurrence of a male gamete'. The of animals, as well as in plants. White (1977) has purpose of thus extending the definition was to include estimated that the proportion of animal 'species' which the special case of gynogenesis, in which a sper- reproduce exclusively by parthenogenesis, and are matozoon enters an egg and activates it to complete copyright. therefore all female, is of the order of one in a the second meiotic division and to develop into an thousand. Parthenogenesis may initiate early em- embryo, but does not contribute any chromosomal bryonic development in mammals, and its lack of material (see below). Whether or not this process success in this class poses some fundamental and as should be included within the province of partheno- yet unresolved problems regarding the significance of genesis is clearly a matter of choice. fertilisation in the physiology of reproduction and It will be clear, however, that parthenogenesis does embryonic development. This is one of the reasons not necessarily imply that the mother has had no http://jmg.bmj.com/ why parthenogenesis is once again an area of active access to a male. In different groups of animals both research. fertilised and unfertilised eggs of the same female may An individual resulting from the development of an proceed to form embryos. For instance, in aphids unfertilised egg is variously referred to as 'partheno- parthenogenetic generations alternate with others in genone', 'parthenogen', or 'parthenote'. The last term which fertilisation takes place. This is known as is American, while 'parthenogenone' is preferred in the 'cyclical parthenogenesis'. In bees an egg may be British literature (Graham, 1974). either fertilised or develop parthenogenetically. This on September 24, 2021 by guest. Protected process is known as 'facultative parthenogenesis'. Definitions of parthenogenesis Indeed, the possibilities for parthenogenesis in the life cycle-dof different-- types; of .animals- are many- and The fact that in certain animals, females may produce varied. This subject has been reviewed by eggs capable of development without previous Suomalainen (1950), by Narbel-Hofstetter (1964), copulation has been known for a long time and was and by White (1973, 1978). Parthenogenesis in called 'lucina sine concubitu'. The term 'partheno- plants has been discussed by Stebbins (1950) and by genesis' is due to Richard Owen (1849) who defined it Nygren (1954). as 'procreation without the immediate influence of a On any definition, however, parthenogenesis is male'; this includes various processes such as fission distinct from asexual reproduction since it involves the and budding in addition to the development of unim- production of egg cells, whereas in asexual repro- pregnated ova. Several authors have since attempted duction new individuals are formed from somatic cells to redefine the term. of the parent. As will be shown below, partheno- According to Suomalainen (1950) parthenogenesis genesis can occur in the absence of meiosis, so that the 165 166 Mittwoch J Med Genet: first published as 10.1136/jmg.15.3.165 on 1 June 1978. Downloaded from egg will have the same chromosome constitution as the If a diploid oogonium completes the two meiotic mother. For this reason, the processes are sometimes divisions and continues development in the absence of equated, particularly in the literature of theoretical nuclear fusion, the resultant embryo will be haploid, at genetics (Maynard Smith, 1971; Williams, 1975). least initially. As will be shown below, the somatic From a physiological point of view, however, the pro- cells of such embryos may subsequently become cesses are different since an egg is a specialised repro- diploid or polyploid. ductive cell which exerts an undoubted influence on Haploid parthenogenesis has been achieved experi- the development of the embryo. Parthenogenesis is, mentally, particularly in amphibia. In this class also, therefore, better regarded as an incomplete form of artificial fertilisation with sperm which had been sexual reproduction. previously inactivated with x-rays has led to the pro- Lastly, parthenogenesis must be distinguished from duction of gynogenetic embryos. Such embryos hermaphroditism, that is the production of male and resemble those produced by parthenogenesis in not female gametes by the same organism. Some her- possessing any paternal chromosomes, but they differ maphrodites are capable of self-fertilisation, but this in the mode of origin and possibly also in the process, involving as it does the union of male and possession of non-nuclear material derived from the female gametes, is clearly distinct from partheno- sperm. genesis. Haploid parthenogenesis forms part of the sex Nuclear fusion is not a bar to parthenogenesis, determining mechanism in certain insects, spiders, and provided both nuclei are of the same gametic sex, that rotifers in which males are formed from haploid, is female, as exemplified by the fusion of the egg unfertilised eggs, whereas diploid, fertilised eggs give nucleus and a polar body. This process is known as rise to females. 'automixis', whereas the term 'amphimixis' relates to Diploid or polyploid parthenogenesis can proceed the fusion of male and female gametes. Development via a number of routes, some of which are illustrated of a new individual in the absence of amphimixis is in Fig. 1. Diploid eggs may be formed by the known as 'apomixis'. This term, however, has been suppression of either the first or second polar bodies. defined in different ways by different authors. Accord- Alternatively, polar bodies may be extruded and sub- ing to Beatty (1957), apomixis in animals is synony- sequently fuse with the egg cell. The second meiotic mous with parthenogenesis, whereas White (1977) division may be completed without extrusion of thecopyright. restricts the term to parthenogenesis in the complete second polar body and the resultant diploid egg cell absence of meiosis. The term 'apomixis' is commonly then undergoes cleavage. It is also possible, however, used with reference to plants and here modes of repro- that the two products of the second meiotic division duction other than parthenogenesis may be included are separated by immediate cleavage, thus initiating (Suomalainen, 1950). The process of sexual repro- haploid parthenogenesis (Witkowska, 1973a). If duction in plants differs from that in animals, since in neither polar body is extruded, the resulting egg would plants a diploid sprophyte generation alternates with a be tetraploid, since the primary oocyte contains the http://jmg.bmj.com/ haploid gametophyte generation, and so the break- duplicated number of chromatids in preparation to down of fertilisation may have different con- undergoing two meiotic divisions. sequences. In the present review the term 'apomixis' Since homologous chromosomes normally segreg- will henceforth be avoided. ate during the first meiotic division, suppression of the second polar body will result in the egg receiving either Haploid, diploid, and polyploid parthenogenesis two paternal or two maternal partners of any pair of chromosomes, though some recombination will have Parthenogenetic development may proceed by various occurred as a result of crossing-over. This process can on September 24, 2021 by guest. Protected routes depending on whether meiosis of the egg cell is be achieved in mammals experimentally (see below). completed normally or, failing this, which of the stages Since crossing-over occurs during prophase in the has been omitted. Alternatively, meiosis may be com- primary oocyte, recombination is likely to have pletely suppressed and the egg develop as a result of occurred even in cases where the first polar body has mitotic divisions only. The number of chromosome been suppressed. However, if diploid parthenogenesis sets in the embryo can further be varied by failure of occurs via the route of premeiotic chromosome cell division as a result of DNA synthesis, either doubling, the first meiotic division occurs with the before meiosis or afterwards, in what would otherwise diploid number of bivalents. In some species it is have been a cleavage division. This process is known known that pairing is restricted to sister chromo- as endoreduplication. Different routes of partheno- somes. Therefore, in spite of the fact that meiosis is genetic devefopment are illustrated in Fig. 1. Their completed, no effective crossing-over takes place. genetic implications have been discussed by Beatty Diploid parthenogenesis can also arise from a (1957) and by Uzzell (1970). normally reduced haploid egg which develops in the Parthenogenesis 167 J Med Genet: first published as 10.1136/jmg.15.3.165 on 1 June 1978.