See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/280691646

Parthenogenesis: Birth of a New Lineage or Reproductive Accident?

Article  in  Current Biology · August 2015

DOI: 10.1016/j.cub.2015.06.055 · Source: PubMed

CITATIONS READS

15 2,547

2 authors:

Casper J Van der Kooi Tanja Schwander

University of Groningen University of Lausanne
37 PUBLICATIONS   377 CITATIONS    96 PUBLICATIONS   2,304 CITATIONS   

SEE PROFILE SEE PROFILE

Some of the authors of this publication are also working on these related projects:

Floral petal surface micro-structure View project

Evolution of insect sex determination View project

All content following this page was uploaded by Casper J Van der Kooi on 19 October 2017.

The user has requested enhancement of the downloaded file.

Current Biology

Dispatches
2. Mennella, V., Keszthelyi, B., McDonald, K.L., cytoplasm before incorporation into the PCM centrosome size in C. elegans embryos. Curr.
Chhun, B., Kan, F., Rogers, G.C., Huang, B., matrix. Mol. Biol. Cell 25, 2984–2992. Biol. 21, 1259–1267.
and Agard, D.A. (2012). Subdiffraction-
resolution fluorescence microscopy reveals a 8. Hamill, D.R., Severson, A.F., Carter, J.C., and 14. Laos, T., Cabral, G., and Dammermann, A.
domain of the centrosome critical for Bowerman, B. (2002). Centrosome maturation (2015). Isotropic incorporation of SPD-5
pericentriolar material organization. Nat. Cell and mitotic spindle assembly in C. elegans underlies centrosome assembly in C. elegans.
Biol. 14, 1159–1168. require SPD-5, a protein with multiple coiled- Curr. Biol. 25, R648–R649.
coil domains. Dev. Cell 3, 673–684.
3. Schnackenberg, B.J., Khodjakov, A., Rieder, 15. Conduit, P.T., and Raff, J.W. (2015). Different
C.L., and Palazzo, R.E. (1998). The 9. Pelletier, L., Ozlu, N., Hannak, E., Cowan, C., Drosophila cell types exhibit important
disassembly and reassembly of functional Habermann, B., Ruer, M., Muller-Reichert, T., differences in mitotic centrosome assembly
centrosomes in vitro. Proc. Natl. Acad. Sci. and Hyman, A.A. (2004). The Caenorhabditis dynamics. Curr. Biol. 25, R650–R651.
USA 95, 9295–9300. elegans centrosomal protein SPD-2 is required
for both pericentriolar material recruitment and 16. Conduit, P.T., Brunk, K., Dobbelaere, J., Dix,
4. Moritz, M., Zheng, Y., Alberts, B.M., and centriole duplication. Curr. Biol. 14, 863–873. C.I., Lucas, E.P., and Raff, J.W. (2010).
Oegema, K. (1998). Recruitment of the Centrioles regulate centrosome size by
gamma-tubulin ring complex to Drosophila controlling the rate of Cnn incorporation into
10. Woodruff, J.B., Wueseke, O., Viscardi, V.,
salt-stripped centrosome scaffolds. J. Cell Mahamid, J., Ochoa, S.D., Bunkenborg, J., the PCM. Curr. Biol. 20, 2178–2186.
Biol. 142, 775–786.
Widlund, P.O., Pozniakovsky, A., Zanin, E.,
Bahmanyar, S., et al. (2015). Centrosomes. 17. Megraw, T.L., Kilaru, S., Turner, F.R., and
5. Conduit, P.T., Feng, Z., Richens, J.H.,
Regulated assembly of a supramolecular Kaufman, T.C. (2002). The centrosome is a
Baumbach, J., Wainman, A., Bakshi, S.D.,
Dobbelaere, J., Johnson, S., Lea, S.M., and centrosome scaffold in vitro. Science 348, dynamic structure that ejects PCM flares.
808–812. J. Cell Sci. 115, 4707–4718.
Raff, J.W. (2014). The centrosome-specific
phosphorylation of Cnn by Polo/Plk1 drives
Cnn scaffold assembly and centrosome 11. Lane, H.A., and Nigg, E.A. (1996). Antibody 18. Lucas, E.P., and Raff, J.W. (2007). Maintaining
maturation. Dev. Cell 28, 659–669. microinjection reveals an essential role for the proper connection between the centrioles
human polo-like kinase 1 (Plk1) in the and the pericentriolar matrix requires
6. Conduit, P.T., Richens, J.H., Wainman, A., functional maturation of mitotic centrosomes. Drosophila centrosomin. J. Cell Biol. 178,
Holder, J., Vicente, C.C., Pratt, M.B., Dix, C.I., J. Cell Biol. 135, 1701–1713. 725–732.
Novak, Z.A., Dobbie, I.M., Schermelleh, L.,
et al. (2014). A molecular mechanism of mitotic 12. Haren, L., Stearns, T., and Luders, J. (2009). 19. Kim, S., and Rhee, K. (2014). Importance of the
centrosome assembly in Drosophila. eLife 3, Plk1-dependent recruitment of gamma-tubulin CEP215-pericentrin interaction for
e03399. complexes to mitotic centrosomes involves centrosome maturation during mitosis. PLoS
multiple PCM components. PLoS One 4, One 9, e87016.
7. Wueseke, O., Bunkenborg, J., Hein, M.Y., e5976.
Zinke, A., Viscardi, V., Woodruff, J.B., 20. Buchman, J.J., Tseng, H.C., Zhou, Y., Frank,
Oegema, K., Mann, M., Andersen, J.S., and 13. Decker, M., Jaensch, S., Pozniakovsky, A., C.L., Xie, Z., and Tsai, L.H. (2010). Cdk5rap2
Hyman, A.A. (2014). The Caenorhabditis Zinke, A., O’Connell, K.F., Zachariae, W., interacts with pericentrin to maintain the neural
elegans pericentriolar material components Myers, E., and Hyman, A.A. (2011). Limiting progenitor pool in the developing neocortex.
SPD-2 and SPD-5 are monomeric in the amounts of centrosome material set Neuron 66, 386–402.

Parthenogenesis: Birth of a New Lineage or

Reproductive Accident?
Casper J. van der Kooi and Tanja Schwander
University of Lausanne, Department of Ecology and Evolution, Le Biophore, CH – 1015 Lausanne, Switzerland
Correspondence: Casper.vanderKooi@unil.ch (C.J.v.d.K.), Tanja.Schwander@unil.ch (T.S.)
http://dx.doi.org/10.1016/j.cub.2015.06.055

Parthenogenesis — the ability to produce offspring from unfertilized eggs — is widespread among
invertebrates and now increasingly found in normally sexual vertebrates. Are these cases reproductive
errors or could they be a first step in the emergence of new parthenogenetic lineages?

The phenomenon of virgin birth has long first, it is the only account of ‘natural son is highly unlikely. As male sex in
fascinated scientists and laymen alike. parthenogenesis’ in a mammal. Mammals humans is determined by genes on the
The first account of parthenogenesis in are believed to be completely unable to Y chromosome, Mary, as a woman,
the literature is the prophecy of Jesus reproduce via parthenogenesis because could not have transmitted any
Christ’s birth in Isaiah 7:14: ‘‘Therefore the of a number of developmental and genetic Y chromosomes to her offspring. In
Lord himself will give you a sign: The virgin constraints [1]. Second, while the contrast to humans, parthenogenetic
will conceive and give birth to a son, and ‘‘Blessed Virgin Mary’’ might have been production of sons is expected in species
will call him Immanuel’’. This reference to able to conceive a daughter via with other types of sex determination.
parthenogenesis is unusual in two ways: parthenogenesis, the conception of a For example, in birds, some reptiles and

Current Biology 25, R654–R676, August 3, 2015 ª2015 Elsevier Ltd All rights reserved R659
 Current Biology

Dispatches

of a very small proportion of unfertilized

Female may reproduce via eggs in a normal, sexual species.
sex and/or parthenogenesis For example, in different species of
Drosophila, observed rates of accidental
parthenogenesis in natural populations
Sexual Accidental Sexual Facultative Obligate
range from one egg in 100,000 to one in a
with million successfully developing into an
reproduction parthenogenesis reproduction parthenogenesis parthenogenesis
Current Biology adult [8]. These hatching rates are orders
of magnitude lower than for facultative
Figure 1. The efficiency of parthenogenesis varies widely. parthenogenesis, where the majority of
Accidental parthenogenesis refers to the very rare hatching of unfertilized eggs in sexual populations, unfertilized eggs hatch. However, without
often due to reproductive errors, that can generate male offspring in species with female heterogamety. systematic screens for hatching success
Given the very low hatching success, accidental parthenogenesis is often not adaptive. Under
of eggs laid by virgin females, accidental
facultative parthenogenesis a female may reproduce via sex and/or parthenogenesis; hence this
reproductive mode combines the advantages of sex and parthenogenesis. Under obligate and facultative parthenogenesis can be
parthenogenesis, females cannot reproduce sexually at all, even if mated to males of sexual lineages. difficult to distinguish. Widely popularized
Populations consisting solely of obligate parthenogens are characterized by the virtual absence of examples of rare parthenogenesis in
males. However, many species feature mixed reproduction, with some females reproducing sexually
and others via obligate parthenogenesis. These species are characterized by sex ratios ranging from vertebrates are typically interpreted as
50:50 to strongly female-biased. facultative parthenogenesis [9], including
reports of parthenogenesis in sharks
[10,11], snakes [5] and Komodo dragons
butterflies, females are the heterogametic recent paper by Fields et al. [6] in Current [4], producing offspring while kept
sex: they carry two differentiated sex Biology documents a new case of solitarily in captivity. Given the current
chromosomes (Z and W) while males female-producing parthenogenesis in evidence, these examples are, however,
are homogametic (ZZ). This sex a critically endangered ray species, most likely cases of accidental rather than
determination system can result in the the sawfish Pristis pectinata. Pristis facultative parthenogenesis, mimicking
virgin birth of sons if parthenogenesis is species — like all sawfish — are the high incidence of accidental
automictic [2], whereby oocytes undergo characterized by their elongated flat nose parthenogenesis among invertebrates.
a normal meiosis that results in four lined with teeth. P. pectinata occurs in Distinguishing whether the sawfish
haploid products (one egg cell and three coastal areas of the western Atlantic sea, females are a case of facultative,
polar bodies). Under sexual reproduction, mostly in bay areas around Florida. A accidental, or obligate parthenogenesis
the polar bodies would degenerate and microsatellite-based genetic screen of would require additional studies, ideally
the egg cell would fuse with a sperm 190 individuals in a wild population involving breeding experiments. Although
to generate a diploid zygote. Under revealed seven females that were most such experiments might be difficult to
automictic parthenogenesis, diploidy is likely produced via parthenogenesis. conduct with P. pectinata because of
restored via the fusion of the egg cell Parthenogenetic ancestry was deduced its ecological requirements, they could
and one of the polar bodies [2]. As because the seven females were generate interesting insights into the
in self-fertilization or mating with homozygous at all or almost all screened evolution of parthenogenesis. For
relatives, automictic parthenogenesis loci [6]. Mating between relatives can also example, because of its great inefficiency,
can cause an increase in homozygosity, result in homozygosity, but individuals in accidental parthenogenesis [7,8] is
including homozygosity at the sex the screened population were not related generally not adaptive (Figure 1). An
chromosome. Hence ZW females can to each other. Furthermore, mating exception might be situations where
parthenogenetically produce ZZ sons between close relatives is unlikely given sexual females fail to find a mate. Stalker
and ZW daughters (WW individuals are the ecology of the species, leaving [12] predicted that in marginal populations
generally not viable). Thus, automictic parthenogenesis as the most likely or other situations where mates are
parthenogenesis is the mechanism explanation [6]. limited even inefficient accidental
underlying the occasional production Are these parthenogenetically parthenogenesis could be adaptive and
of sons and daughters well known for produced sawfish females rare thus selectively favored. This prediction
many species of bagworm moths [3] ‘accidents’, or could they be indicative is supported by evidence from natural
and recently described in some reptile of a unique case of adaptive, facultative populations of Drosophila vinegar flies
species, including Komodo dragons [4] parthenogenesis in a vertebrate? and stick insects. In these species,
and snakes [5]. Facultative parthenogenesis, where accidental parthenogenesis rates are
While male-producing parthenogenesis an individual female can produce especially high in low-density populations
is rare, female-producing parthenogenesis offspring either sexually or where large fractions of adult females
is widespread among animals and parthenogenetically (Figure 1), is remain unmated [13,14]. Thus, via the
mostly obligate (Figure 1), with many exceedingly rare among animals. A accumulation of gradual changes,
documented cases in species-rich much more widespread phenomenon accidental parthenogenesis might be a
invertebrate groups such as insects, is accidental parthenogenesis — also stepping-stone to ‘true’ parthenogenesis
nematodes and crustaceans, and with called spontaneous parthenogenesis, and give rise to new facultative or obligate
only few examples in vertebrates [2]. A or tychoparthenogenesis [7]: the hatching parthenogenetic lineages.

R660 Current Biology 25, R654–R676, August 3, 2015 ª2015 Elsevier Ltd All rights reserved
 Current Biology

Dispatches

So, could accidental parthenogenesis 2. Suomalainen, E., Saura, A., and Lokki, J. 9. Lampert, K. (2008). Facultative parthenogenesis
(1987). Cytology and Evolution in in vertebrates: reproductive error or chance?
in humans ever give rise to a new Parthenogenesis (Boca Raton: CRC Press). Sex. Dev. 2, 290–301.
parthenogenetic lineage? Probably
not, as the developmental and genetic 3. Seiler, J. (1960). Untersuchungen über die 10. Chapman, D.D., Shivji, M.S., Louis, E.,
Entstehung der Parthenogenese bei Solenobia Sommer, J., Fletcher, H., and Prodöhl, P.A.
constraints in humans and other triquetrella F.R. (Lepidoptera, Psychidae) II. (2007). Virgin birth in a hammerhead shark.
mammals would most likely prevent the Analyse der diploid parthenogenetischen Biol. Lett. 3, 425–427.
S. triquetrella. Verhalten, Aufzuchtresultate
emergence of adaptive parthenogenesis und Zytologie. Chromosoma 11, 29–102. 11. Feldheim, K.A., Chapman, D.D., Sweet, D.,
in natural populations [1]. As it turns out, Fitzpatrick, S., Prodöhl, P.A., Shivji, M.S., and
even the most famous speculation about 4. Watts, P.C., Buley, K.R., Sanderson, S., Snowden, B. (2010). Shark virgin birth
Boardman, W., Ciofi, C., and Gibson, R. produces multiple, viable offspring. J. Hered
parthenogenesis, Jesus Christ’s birth, (2006). Parthenogenesis in Komodo dragons. 101, 374–377.
owes its existence not to a miracle but to a Nature 444, 1021–1022.
12. Stalker, H.D. (1956). On the evolution of
human error during the translation of 5. Booth, W., Johnson, D.H., Moore, S., Schal, parthenogenesis in Lonchoptera (Diptera).
Isaiah 7:14 from Hebrew to Greek: The C., and Vargo, E.L. (2011). Evidence for viable, Evolution, 345–359.
Hebrew word almah can refer to a young non-clonal but fatherless Boa constrictors.
Biol. Lett. 7, 253–256. 13. Kramer, M.G., and Templeton, A.R. (2001).
woman of marriageable age, whether Life-history changes that accompany the
married or not [15]. The ‘young woman’ 6. Fields, A.T., Feldheim, K.A., Poulakis, G.R., transition from sexual to parthenogenetic
and Chapman, D.D. (2015). Facultative reproduction in Drosophila mercatorum.
became a ‘virgin’ in the gospel according parthenogenesis in a critically endangered Evolution 55, 748–761.
to Matthew, where almah was translated wild vertebrate. Curr. Biol. 25, R446–R447.
14. Schwander, T., Vuilleumier, S., Dubman, J.,
as the Greek parthenos. 7. Bell, G. (1982). The Masterpiece of Nature: The and Crespi, B.J. (2010). Positive feedback in
Evolution and Genetics of Sexuality (Berkeley, the transition from sexual reproduction to
REFERENCES CA: University of California Press). parthenogenesis. Proc. R. Soc. B. Biol. Sci.,
rspb20092113.
8. Templeton, A.R. (1979). The parthenogenetic
1. Engelstaedter, J. (2008). Constraints on the capacities and genetic structures of sympatric 15. Argyle, A.W. (1963). The gospel according to
evolution of asexual reproduction. BioEssays populations of Drosophila mercatorum and Matthew, Volume 33 (Cambridge: Cambridge
30, 1138–1150. Drosophila hydei. Genetics 92, 1283–1293. University Press).

Binocular Vision: Joining Up the Eyes

Andrew T. Smith
Department of Psychology, Royal Holloway, University of London, Egham, Surrey TW20 0EX, UK
Correspondence: a.t.smith@rhul.ac.uk
http://dx.doi.org/10.1016/j.cub.2015.06.013

To provide a unitary view of the external world, signals from the two eyes must be combined: a new study
pinpoints the location in the human brain where the requisite combination occurs.

A fundamental feature of human vision is wider field of view (only modestly wider in however, it has long been known that this
that, despite having two eyes, we humans but much wider in horses, sheep is not the case and that the answer is
normally see only one representation of and many other mammals). The most ‘‘somewhere in the visual cortex’’. In this
the world around us. This phenomenon, studied benefit is that having two eyes issue of Current Biology, Barendregt et al.
imaginatively termed cyclopean permits stereoscopic vision: the [2] present evidence from functional
perception by the late Bela Julesz [1], construction of accurate estimates of the magnetic resonance imaging (fMRI) that
requires a seamless combination of two distances of nearby objects based on the transformation occurs between the
completely separate neural signals and subtle differences between the two retinal primary visual cortex, known as V1, and
imposes on the brain a substantial images. These benefits depend on the the second visual area, V2.
computational burden that a cyclops replacement of two representations of the Whether a given neuron is responsive to
would be spared. There are, however, world by a single, cyclopean light stimulation in either eye or is driven
a number of benefits to having two representation. Where in the brain does only by one eye has been addressed in
eyes that collectively outweigh the this happen? It might be expected that a many neurophysiological studies, starting
computational cost. Perhaps the most harmonious coalition of left and right with the pioneering work of Nobel Prize
obvious, although not necessarily the would be constructed at the very first winners Hubel and Wiesel, who found that
evolutionary driver, is insurance against processing stage at which both signals the primary visual cortex of macaques
loss of an eye. Another is that it permits a are present in proximity: the thalamus; contains a mixed bag of cells, some

Current Biology 25, R654–R676, August 3, 2015 ª2015 Elsevier Ltd All rights reserved R661
View publication stats