Current Biology
Dispatches
13. Birnbaum, K., Shasha, D.E., Wang, J.Y., Jung,
J.W., Lambert, G.M., Galbraith, D.W., and
Benfey, P.N. (2003). A gene expression map
of the Arabidopsis root. Science 302, 1956
1960.
14. Kanno, S., Arrighi, J.F., Chiarenza, S., Bayle,
V., Berthome, R., Peret, B., Javot, H.,
Delannoy, E., Marin, E., Nakanishi, T.M., et al.
(2016). A novel role for the root cap in
phosphate uptake and homeostasis. eLife 5,
e14577.
15. Vogiatzaki, E., Baroux, C., Jung, J.-Y., and
Poirier, Y. (2017). PHO1 exports phosphate
from the chalazal seed coat to the embryo in
Evolution: A Parthenogenetic Nematode Shows How
Animals Become Sexless
Erich M. Schwarz
Department of Molecular Biology and Genetics, Cornell University, Ithaca, NY 14853, USA
Correspondence: ems394@cornell.edu
http://dx.doi.org/10.1016/j.cub.2017.08.040
Most animals have male and female sexes, implying that sex is ancient and beneficial; yet some have survived
for millions of years without sex. The genome of the parthenogenetic nematode Diploscapter pachys gives
clues as to how ancient asexual animals can exist.
Most animals have female and male sexes
that make haploid eggs and sperm
(gametes) through meiosis, then fuse
them to create diploid fertilized eggs
(zygotes). These processes are ancient:
genes required for meiosis are found in all
animal phyla and most eukaryotes [1,2]. It
is not yet clear why meiosis and sexual
reproduction are so widely conserved
throughout animal evolution, given that
sex is costly. Meiotic recombination
disrupts favorable combinations of
alleles, male offspring add a two-fold
burden to reproduction, and the effort of
finding a mate makes reproduction less
reliable. On the other hand, self-fertilizing
animals may be driven to extinction by
ever-accumulating harmful mutations,
since they cannot use meiosis to replace
bad alleles with good ones [3]. Also, self-
fertilizing animals are expected to be less
genetically diverse than outcrossing
animals, making them more vulnerable to
unpredictable threats such as parasites.
For these reasons, and because sex is
indeed pervasive among animals, it is
easy to assume that sex is universal.
R1064 Current Biology 27, R1060R1080, October 9, 2017 2017 Elsevier Ltd.
developing Arabidopsis seeds. Curr. Biol. 27,
28932900.
16. Kanno, S., Cuyas, L., Javot, H., Bligny, R.,
Gout, E., Dartevelle, T., Hanchi, M., Nakanishi,
T.M., Thibaud, M.C., and Nussaume, L. (2016).
Performance and limitations of phosphate
quantification: guidelines for plant biologists.
Plant Cell Physiol. 57, 690706.
17. Kim, S.A., Punshon, T., Lanzirotti, A., Li, L.T.,
Alonso, J.M., Ecker, J.R., Kaplan, J., and
Guerinot, M.L. (2006). Localization of iron in
Arabidopsis seed requires the vacuolar
membrane transporter VIT1. Science 314,
12951298.
However, a confounding minority of
animals defy this trend, either by being
only optionally sexual or by abandoning
sexual reproduction entirely. Up to 30%
of animal species have hermaphrodites
rather than females, with roughly 50%
self-fertilization on average [4]. For some
hermaphrodites, self-fertilization can be
much more frequent: the nematode
Caenorhabditis elegans has 99.9% self-
fertilizing hermaphrodites mixed with
only 0.1% males [5]. Such animals are
partly asexual, with serious evolutionary
consequences; C. elegans is completely
inbred [6], and C. elegans males show
atrophied skill at mating [5,7].
Nevertheless, self-fertilizing
hermaphrodites remain partially sexual,
and keep some of sexs advantages.
A rarer and more extreme set of animals
have abandoned sex entirely; these
animals produce eggs that develop into
new animals without fertilization (i.e., they
are parthenogenetic) [3]. Many of these
asexual animals are closely related to
other species with normal sex, implying
that their asexuality evolved only recently.
18. Kanno, S., Yamawaki, M., Ishibashi, H.,
Kobayashi, N.I., Hirose, A., Tanoi, K.,
Nussaume, L., and Nakanishi, T.M. (2012).
Development of real-time radioisotope
imaging systems for plant nutrient uptake
studies. Phil. Trans. R. Soc. Lon. 367, 1501
1508.
19. Ayadi, A., David, P., Arrighi, J.F., Chiarenza, S.,
Thibaud, M.C., Nussaume, L., and Marin, E.
(2015). Reducing the genetic redundancy
of Arabidopsis PHOSPHATE
TRANSPORTER1 transporters to study
phosphate uptake and signaling. Plant Physiol.
167, 15111526.
But others are older, having lived without
sex for 40 to 200 million years: bdelloid
rotifers, darwinulid ostracods, oribatid
mites, and root-knot nematodes [3].
These ancient asexuals pose a sharp
challenge to the idea that sex is necessary
for animal survival: how can they exist
at all?
In this issue of Current Biology, Fradin
et al. [8] have sequenced and analyzed
the genome of Diploscapter pachys,
a parthenogenetic nematode closely
related to C. elegans (Figure 1). They give
a detailed view of genetic changes that
may have rendered D. pachys asexual,
and what consequences this asexuality
had for its genome. With a parallel
genome analysis of the parthenogenetic
Diploscapter coronatus by Hiraki et al. [9],
this provides the basis for genetic and
molecular analyses of asexuality in a
nematode that should be as
experimentally tractable as C. elegans.
To provide an evolutionary context,
Fradin et al. determined the phylogenetic
relationships, chromosome counts, and
sexual life cycles for D. pachys and other
Current Biology
Dispatches
related nematode species. D. pachys and
four close relatives (D. sp. 2, D. sp. 4,
D. lycostoma, and Protorhabditis sp. 4)
formed a related group of sexless
parthenogens, with P. sp. 4 being the
most divergent member, and with a
common ancestor that lived about
18 million years ago. Unlike the others,
P. sp. 4 had sperm as well as eggs in its
female gonads; but all four of these
parthenogenetic species exhibited only
one pronucleus during zygote formation,
rather than the two pronuclei expected
for normal meiosis of a sexual species.
Thus, the eggs of D. pachys and its
parthenogenetic relatives all appear to
have a partial meiotic cell cycle in which
the first division (Meiosis I, during which
a genome normally undergoes
recombination and duplicates to four
copies) does not occur. The sperm of
P. sp. 4 may be pseudogamous; i.e.,
they may have a vestigial function of
activating eggs despite not contributing
genetic material, which could represent
an intermediate stage between normal
sex (or hermaphroditism) and complete
parthenogenesis. Another shared
peculiarity of D. pachys and its
parthenogenetic relatives is that their
nuclei have only one pair of
chromosomes, a trait seen in very few
other animals. In contrast, other
nematodes more distantly related to
D. pachys, such as C. elegans, have six
or seven pairs of chromosomes. Thus,
D. pachys ancestor may have fused
several chromosomes into one at
roughly the same time that it became
parthenogenetic.
To uncover the genomic basis of
D. pachys asexuality, Fradin et al.
sequenced its genome and compared its
gene content to C. elegans. In a typical
genome of a self-fertilizing nematode
species, one would expect an essentially
haploid sequence, with unresolved alleles
being rare. In contrast, the D. pachys
sequence was highly diploid: 60% of its
protein-coding genes could be detected
as two alleles in the genome assembly,
with an average of 4% sequence
divergence between the alleles. This is only
possible if the genome has been entirely
frozen into heterozygosity, with no genetic
recombination allowed, which fits
D. pachys loss of Meiosis I. Similarly frozen
heterozygosity has been observed in the
asexual bdelloid rotifer Adineta vaga [10].
Diploscapter
pachys
Caenorhabditis
elegans
Figure 1. Adult nematodes with eggs, reproducing without sex.
A Diploscapter pachys parthenogen is shown, with a larger Caenorhabditis elegans hermaphrodite for
comparison. Scale bar: 100 mm. (Image kindly provided by D. Fitch.)
Fradin et al. then searched D. pachys
for losses of genes and DNA sequences
involved in chromosome structure (to
explain its fused single chromosome), in
meiosis (to explain its truncated meiotic
cell cycle), and in genetic recombination
(to explain how D. pachys kept its genome
heterozygous for millions of years).
D. pachys genome had no trace of a
repetitive DNA sequence normally
associated with nematode telomeres,
and it lacked four genes for shelterin
POT1 subunit homologs (mrt-1, pot-1,
pot-2, and pot-3) that C. elegans requires
for telomere maintenance. Since mrt-1
mutants in C. elegans undergo
chromosome fusion [11], loss of mrt-1
may have induced similar fusion in
D. pachys ancestor. Moreover, D. pachys
lacked four paralogous C2H2 zinc-finger
genes, zim-1, zim-2, zim-3, and him-8.
In C. elegans, these genes are required
for meiotic recombination and share an
operon [12]; thus, D. pachys ancestor
could easily have lost them all (and lost
meiotic recombination) in a single
deletion. Other lost genes included the
meiosis-specific cohesin rec-8: its
mutants in C. elegans fail to undergo
normal Meiosis I, yet are partially viable
and fertile [13]. Again, this phenotype
resembles wild-type D. pachys.
Equivalent gene losses were also
observed in D. coronatus [9], making it
likelier that they represent conserved
events driving asexuality.
Fradin et al. found regions of the
D. pachys genome (ancestral
chromosome domains, or ACDs) whose
ancestor primarily came from a single
chromosomal region, before the fusion of
six ancestral chromosomes. Nematodes
Current Biology 27, R1060R1080, October 9, 2017 R1065
Current Biology
usually conserve the gene content of their
chromosomes over tens of millions of
years [14]. In contrast, Fradin et al.
observed that, in D. pachys, significant
numbers of genes had migrated between
ACDs. The authors further speculated
that D. pachys might have overcome the
requirement for telomeres by fusing its
chromosomes into circles. This idea is
not as wild as it might seem. Linear
chromosomes first became necessary
for eukaryotes because of meiotic
recombination [1]; if recombination is lost,
circular chromosomes become possible
again. Moreover, when telomere
formation is genetically blocked in fission
yeast, its chromosomes can in fact
become circular while continuing to
replicate and function [15]. That being
said, D. pachys and D. coronatus
chromosomes look linear in the
microscope, suggesting that Diploscapter
might instead have telomeres that
happen not to require known DNA
repeats or mrt-1 homologs.
The genome of D. pachys will enable
many new studies of asexuality. Third-
generation genome sequencing will make
it possible to settle the issue of its
chromosomal structure [16].
Technologies for gene silencing, targeted
mutagenesis, and expression analysis
should be straightforward to import from
C. elegans to D. pachys [17], which in
turn should make D. pachys the most
experimentally tractable ancient asexual.
As D. pachys is developed into an
emerging model, it will also be important
to compare it with bdelloid rotifers.
These long-studied parthenogens appear
to use pervasive horizontal gene transfer
(HGT) from other organisms to overcome

asexualitys genetic stagnation [10,18],
and perhaps even use HGT to donate
genes to one another [19]. Since HGT
into nematodes is not uncommon [20], it
could provide D. pachys with covert
gene transfer without overt sex, and
could certainly provide it with genes from
other organisms. There is much work to
be done before the question of how
animals thrive without sex is answered,
and D. pachys will be crucial to it.
REFERENCES
1. Goodenough, U., and Heitman, J. (2014).
Origins of eukaryotic sexual reproduction.
Cold Spring Harb. Perspect. Biol. 6, a016154.
2. Speijer, D., Lukes, J., and Elias, M. (2015). Sex
is a ubiquitous, ancient, and inherent attribute
of eukaryotic life. Proc. Natl. Acad. Sci. USA
112, 88278834.
3. Neiman, M., Meirmans, S., and Meirmans,
P.G. (2009). What can asexual lineage age tell
us about the maintenance of sex? Ann. N. Y.
Acad. Sci. 1168, 185200.
4. Jarne, P., and Auld, J.R. (2006). Animals mix
it up too: the distribution of self-fertilization
among hermaphroditic animals. Evolution 60,
18161824.
5. Chasnov, J.R., and Chow, K.L. (2002). Why are
there males in the hermaphroditic species
Caenorhabditis elegans? Genetics 160,
983994.
6. Andersen, E.C., Gerke, J.P., Shapiro, J.A.,
Crissman, J.R., Ghosh, R., Bloom, J.S., Felix,
M.A., and Kruglyak, L. (2012). Chromosome-
Retrotransposons: Stowaways in the Primordial
Germline
Erin S. Kelleher
Department of Biology and Biochemistry, University of Houston, 3455 Cullen Blvd., Suite 342, Houston, TX 77204, USA
Correspondence: eskelleh@central.uh.edu
http://dx.doi.org/10.1016/j.cub.2017.08.059
In order to succeed, retrotransposon transcripts must identify the subset of nuclei that will be transmitted to
offspring. A new study reveals that the primordial germline is a hideout for retrotransposon transcripts,
providing early access to future gametes.
Transposable elements are obligate
genetic parasites, whose persistence and
spread through their host genome relies on
the production of new genomic copies
(reviewed in [1]). DNA transposons move
R1066 Current Biology 27, R1060R1080, October 9, 2017 2017 Elsevier Ltd.
scale selective sweeps shape Caenorhabditis
elegans genomic diversity. Nat. Genet. 44,
285290.
7. Garcia, L.R., LeBoeuf, B., and Koo, P. (2007).
Diversity in mating behavior of hermaphroditic
and male-female Caenorhabditis nematodes.
Genetics 175, 17611771.
8. Fradin, H., Kiontke, K., Zegar, C., Gutwein, M.,
Lucas, J., Kovtun, M., Corcoran, D.L., Baugh,
L.R., Fitch, D.H.A., Piano, F., and Gunsalus,
K.C. (2017). Genome architecture and
evolution of a unichromosomal asexual
nematode. Curr. Biol. 27, 29282939.
9. Hiraki, H., Kagoshima, H., Kraus, C., Schiffer,
P.H., Ueta, Y., Kroiher, M., Schierenberg, E.,
and Kohara, Y. (2017). Genome analysis of
Diploscapter coronatus: insights into
molecular peculiarities of a nematode with
parthenogenetic reproduction. BMC
Genomics 18, 478.
10. Flot, J.F., Hespeels, B., Li, X., Noel, B.,
Arkhipova, I., Danchin, E.G., Hejnol, A.,
Henrissat, B., Koszul, R., Aury, J.M., et al.
(2013). Genomic evidence for ameiotic
evolution in the bdelloid rotifer Adineta vaga.
Nature 500, 453457.
11. Meier, B., Barber, L.J., Liu, Y., Shtessel, L.,
Boulton, S.J., Gartner, A., and Ahmed, S.
(2009). The MRT-1 nuclease is required for
DNA crosslink repair and telomerase activity
in vivo in Caenorhabditis elegans. EMBO J. 28,
35493563.
12. Phillips, C.M., and Dernburg, A.F. (2006). A
family of zinc-finger proteins is required for
chromosome-specific pairing and synapsis
during meiosis in C. elegans. Dev. Cell 11,
817829.
13. Severson, A.F., Ling, L., van Zuylen, V., and
Meyer, B.J. (2009). The axial element protein
through excision and insertion of the same
DNA fragment, relying on host DNA
replication machinery to increase their
copy numbers. By contrast,
retrotransposons self-replicate through a
Current Biology
Dispatches
HTP-3 promotes cohesin loading and meiotic
axis assembly in C. elegans to implement the
meiotic program of chromosome segregation.
Genes Dev. 23, 17631778.
14. Hillier, L.W., Miller, R.D., Baird, S.E.,
Chinwalla, A., Fulton, L.A., Koboldt, D.C., and
Waterston, R.H. (2007). Comparison of
C. elegans and C. briggsae genome
sequences reveals extensive conservation
of chromosome organization and synteny.
PLoS Biol. 5, e167.
15. Naito, T., Matsuura, A., and Ishikawa, F.
(1998). Circular chromosome formation in a
fission yeast mutant defective in two ATM
homologues. Nat. Genet. 20, 203206.
16. Dudchenko, O., Batra, S.S., Omer, A.D.,
Nyquist, S.K., Hoeger, M., Durand, N.C.,
Shamim, M.S., Machol, I., Lander, E.S., Aiden,
A.P., et al. (2017). De novo assembly of the
Aedes aegypti genome using Hi-C yields
chromosome-length scaffolds. Science 356,
9295.
17. Ward, J.D. (2015). Rendering the intractable
more tractable: tools from Caenorhabditis
elegans ripe for import into parasitic
nematodes. Genetics 201, 12791294.
18. Gladyshev, E.A., Meselson, M., and
Arkhipova, I.R. (2008). Massive horizontal
gene transfer in bdelloid rotifers. Science 320,
12101213.
19. Debortoli, N., Li, X., Eyres, I., Fontaneto, D.,
Hespeels, B., Tang, C.Q., Flot, J.F., and Van
Doninck, K. (2016). Genetic exchange among
bdelloid rotifers is more likely due to horizontal
gene transfer than to meiotic sex. Curr. Biol.
26, 723732.
20. Boto, L. (2014). Horizontal gene transfer in the
acquisition of novel traits by metazoans. Proc.
Biol. Sci. 281, 20132450.
copy-and-paste mechanism, in which a
transposon-encoded RNA is reverse
transcribed and integrated into a new
chromosomal location, thereby producing
a new copy. In this issue of Current Biology,