Sex is the norm…or is it?
Sexual reproduction has an ancient evolutionary history, perhaps arising concomitantly with the evolution of eukaryotic cells (1). As a result, most eukaryotic organisms existing today reproduce sexually at some stage in their life history (2). During sexual reproduction, a diploid organism produces haploid gametes via meiosis. Fertilization and fusion of the two gamete nuclei restores the diploid chromosome number. As a result, somatic cells of sexually produced progeny have the same number of chromosomes as the somatic cells of the parent. However, the progeny are not identical to the parents because recombination, independent assortment, and fertilization result in organisms with new combinations of alleles. (Mutation can, of course, produce new alleles as well.)
Metazoa are typically bisexual, with males producing small, motile, and numerous sperm, and females producing large, non-motile, less numerous eggs. Fertilization delivers the haploid sperm nucleus into the egg and fusion of the sperm and egg nuclei restores the diploid state. Importantly, fertilization also activates the egg to undergo mitosis, triggering the cell divisions and developmental processes that ultimately produce a viable, multicellular progeny organism with all the appropriate fingers and toes.
In the background of this ancient, “mainstream” sexuality, some species in all major eukaryotic taxa of the tree of life have completely lost the ability to reproduce sexually or gained the ability to reproduce asexually at least some of the time (1-3). The cellular and genetic processes that underlie metazoan asexual reproduction are fascinating, as are considerations of the evolution, costs, and benefits associated with sexual reproduction. The discussions are allegorically rich, with terms like “Mueller’s Ratchet” and “The Tangled Bank” and “Red Queen.” The interested reader will get a good vertebrate-focused overview in Avise’s book, Clonality (1).
A variety of “vegetative” reproduction modes are present in metazoa, typically involving growth of an individual from somatic cells of the parent. Examples include growth of colonial corals and multiplication of sea anemones by pedal laceration. Metazoa can also reproduce asexually via parthenogenesis, in which viable, fertile offspring arise from unfertilized eggs. The resulting progeny can be male or female, depending on the mechanisms of sex determination in that species, as well as on the specific mechanisms by which the egg is produced. (See the Parthenogenesis PowerPoint file for illustrations of the mechanisms of parthenogenetic egg production.)
In contrast to the more or less uniform processes that underlie meiosis, the processes involved in parthenogenesis are diverse, reflecting the evolution of parthenogenesis in multiple independent lines, sometimes even within an individual species. It is an area of rich, confusing literature sprinkled liberally with competing, hard to pronounce terminology. In this teaching review, I focus on the major features that are likely to arise in an undergraduate biology class. The featured reviews in the bibliography would be useful for the teacher who wishes to develop expert knowledge in this area.
Reproduction by Obligate Parthenogenesis: Sometimes, there is no baby daddy!
Obligate parthenogenetic species must reproduce via parthenogenesis at some point in their life history. Dozens of obligate parthenogenetic species are known, including species of rotifers, mites, daphnia, stick insects, hymenoptera, planaria, frogs, reptiles, and fish.
Some obligate parthenogenetic species are unisexual and reproduce exclusively by parthenogenesis. These species are comprised of only females whose eggs can develop in the absence of the developmental trigger of fertilization to produce the next generation of all female offspring. In an interesting variation called gynogenesis or “sexual parasitism”, the egg is fertilized by sperm from a related species, but all of the chromosomes donated by the male are discarded, resulting in only female progeny that contain only genes of maternal origin. In another interesting variation, hybridogenesis, the egg is fertilized by sperm and the resulting female offspring contains both maternal and paternal chromosomes. However, at oogenesis in the offspring, the paternal chromosomes are discarded. As a result, the male can be a genetic father, but never a genetic grandfather. (You can see what I mean when I say the mechanisms at play in parthenogenesis are remarkably diverse! See the Parthenogenesis PowerPoint file for an illustration of parthenogenesis, gynogenesis, and hybridogenesis.)
Some obligate parthenogenetic species are bisexual, producing one sex via parthenogenesis (often haploid males) and the other sex via sexual reproduction (often diploid females). However, parthenogenesis can produce males (arrhenotoky) or females (thelytoky), depending on whether the unfertilized egg develops into a male or female. In some species, obligate parthenogenesis alternates with sexual reproduction, producing cycles of parthenogenetic generation(s) of females and bisexual generations of both sexes, often in response to environmental conditions. Good examples of this cyclical parthenogenesis are known in aphids, rotifers, and water fleas.
Reproduction by Facultative Parthenogenesis: A different way to swing both ways…
In addition to the ~80 species in which the species’ normal life history includes reproduction by parthenogenesis, parthenogenesis can also be facultative: the species contains both males and females and can reproduce by sexual means. However, at varying frequencies, eggs can also unilaterally undergo development to produce viable progeny. Facultative parthenogenesis has been described in birds (turkeys, chickens, quail), reptiles (lizards and snakes), and fish. Although usually considered to be a relatively uncommon process associated with captivity or other stresses, facultative parthenogenesis was recently demonstrated to be surprisingly common in natural populations of snakes (4).
Induced Parthenogenesis: Infections & Experimentation
In a variety of insects, parthenogenesis can also occur as a result of bacterial infections (5). For example, Wolbachia bacteria that are present in the egg are passed into the embryo. This infection results in in an abnormal division in the first mitosis following the completion of meiosis. As a result, haploid embryos that would normally develop into haploid males become diploid and develop into females, which can transmit the bacteria to the next generation within her eggs. If the bacterial infection is “cured,” bisexuality can be restored (6) or the species may be permanently locked into a unisexual state, creating an obligate parthenogenetic species (7).
No parthenogenetic mammals have been observed, presumably because of the genetic imprinting processes that modify genes during gametogenesis. A viable mammalian embryo requires genes that have passed through both female and male gametogenesis, i.e. they need to inherit one chromosome from a mother and one from a father. The hurdle created by imprinting apparently prevents natural parthenogenesis in mammals. However, in the laboratory, viable and fertile mice offspring can be produced by injecting a mature egg with a nucleus from an immature egg. Variations in this approach have significant promise for “therapeutic cloning,” for example as a mechanism to generate organs that are perfect matches for transplant patients. In a recent example, embryonic stem cells could be generated by transplantation of a somatic nucleus into a mouse oocyte (8). In contrast to approaches that require use of oocytes, induced pluripotent stem cell are likely to offer similar returns with less controversy (9).
Why doesn’t parthenogenesis always produce clones?
Parthenogenesis in vertebrates can be thought of simply as production of diploid rather than haploid eggs. In some cases, diploid eggs can be produced by mitosis, resulting in progeny that are exact clones of the mother. More frequently, the eggs are produced by meiosis, with restoration of the diploid state occurring via cell or nuclear fusion at either meiosis I or meiosis II, or by premeiotic or postmeiotic doubling of chromosomes. (See the PowerPoint file, Parthenogenesis, for illustrations of some of these mechanisms.) The genetic consequences of meiotic parthenogenesis vary considerably. For example, if chromosomes are duplicated prior to meiosis, a tetraploid cell will enter meiosis. Meiosis will restore the diploid state, producing diploid eggs that are genetically identical to the parent, as if the eggs had been produced by mitosis! In other cases, meiotic parthenogenesis produces offspring that are not identical to the mother. In the snake case described in the “Why Meiosis Matters” lesson, the offspring are, in fact, male.
For the Fatherless Snake Lesson: Parthenogenesis & Sex Determination
Testes formation in mammals is initiated by genes located on the Y chromosome. Thus, males are typically XY and females XX. An embryo that inherited two Y chromosomes would lack essential genes and be unable to develop. Sex determination in reptiles is more diverse, with sex determination being driven by temperature of embryo incubation or by genes present on autosomes or on sex chromosomes (10, 11). Sex chromosomes in reptiles and birds are called Z and W and are somewhat analogous to the X and Y chromosomes of mammals. Although there are exceptions, the heterogametic sex (i.e. ZW) is typically female. Thus, it is possible that facultative parthenogenotes in reptiles and birds are male because the Z and W chromosomes segregate at meiosis I. In other words, following meiosis I, one cell contains 2 copies of the Z chromosome and the other cell contains 2 copies of the W chromosome. If meiosis II did not occur properly (i.e. the second polar body nucleus fused with the egg nucleus), the resulting diploid eggs would be ZZ or WW. However, only the ZZ egg could develop to produce a viable offspring, since some genes on the Z chromosome are essential. Thus, only ZZ (male) offspring would be produced.
Be forewarned! We shouldn’t get too comfortable with the satisfying explanation above. A recent report of female Boa constrictors parthenogenotes (12), once again reinforces that we need to maintain an open mind to new information. The accompanying PowerPoint presentation illustrates this meiotic process. It seems that pretty much anything goes in the strange and wonderful world of parthenogenesis and sex determination.
1. Avise, JC. 2008. Clonality: the genetics, ecology, and evolution of sexual abstinence in vertebrate animals. Oxford University Press, Oxford ; New York.
2. Bell, G. 1982. The masterpiece of nature: the evolution and genetics of sexuality. University of California Press, Berkeley.
3. Suomalainen, E, A Saura, and J Lokki. 1987. Cytology and evolution in parthenogenesis. CRC Press, Boca Raton, Fla.
4. Booth, W, CF Smith, PH Eskridge, SK Hoss, JR Mendelson, 3rd, and GW Schuett. 2012. Facultative parthenogenesis discovered in wild vertebrates. Biol. Lett. 8:983-985.
5. Huigens, ME, RF Luck, RH Klaassen, MF Maas, MJ Timmermans, and R Stouthamer. 2000. Infectious parthenogenesis. Nature 405:178-179.
6. Pannebakker, BA, NS Schidlo, GJ Boskamp, L Dekker, TJ van Dooren, LW Beukeboom, BJ Zwaan, PM Brakefield, and JJ van Alphen. 2005. Sexual functionality of Leptopilina clavipes (Hymenoptera: Figitidae) after reversing Wolbachia-induced parthenogenesis. J. Evol. Biol. 18:1019-
7. Stouthamer, R, JE Russell, F Vavre, and L Nunney. 2010. Intragenomic conflict in populations infected by Parthenogenesis Inducing Wolbachia ends with irreversible loss of sexual reproduction. BMC Evol. Biol. 10:229.
8. Tachibana, M, P Amato, M Sparman, NM Gutierrez, R Tippner-Hedges, H Ma, E Kang, A Fulati, H-S Lee, and H Sritanaudomchai. 2013. Human embryonic stem cells derived by somatic cell nuclear transfer. Cell 153:1228-1238.
9. Yamanaka, S, and HM Blau. 2010. Nuclear reprogramming to a pluripotent state by three approaches. Nature 465:704-712.
10. Gross, J, and D Bhattacharya. 2010. Uniting sex and eukaryote origins in an emerging oxygenic world. Biol. Direct 5:53.
11. Warner, DA. 2011. Sex determination in reptiles. Hormones and Reproduction of Vertebrates: Reptiles:1-38.
12. Booth, W, DH Johnson, S Moore, C Schal, and EL Vargo. 2011. Evidence for viable, non-clonal but fatherless Boa constrictors. Biol. Lett. 7:253-256.