resolved — the sperm head is closer
to the site of fertilisation [15,17] — this
is unclear for Onthophagus. What
are the characteristics of short sperm
that contribute to fertilization success?
Or approaching the problem from
another angle, what drives the
evolution of (large) spermatheca size?
Larger spermathecae could promote
increased sperm competition and
relate to a greater propensity for
polyandry. Genetic correlations
mating rates could be addressed
experimentally. Artificial selection
incorporating monandrous (no sexual
selection) and polyandrous lines
(sexual selection) could be applied to
verify whether fertilisation efficiency
increases with intensity of
postcopulatory sexual selection. This
approach could also aid in the
investigation of whether inclusive
fitness is higher in polyandrous than in
monandrous females as predicted .
To specifically investigate the good
sperm aspect in this system, it would
be necessary to investigate offspring
viability in relation to father’s
fertilization success. Finally, sperm
number could also play a role (for
example ), so do males with short
sperm also transfer more or less sperm
(depending on how costly short sperm
are to produce)? Future work in this
vein could helpverify key predictionsof
sexually selected sperm processes
[7,8] and further the understanding of
reproductive traits central in speciation
1. Andersson, M. (1994). Sexual Selection
(Princeton: Princeton University Press).
2. Simmons, L.W. (2001). Sperm Competition and
Its Evolutionary Consequences in the Insects
(Princeton: Princeton University Press).
3. Arnqvist, G., and Rowe, L. (2005). Sexual
Conflict (Princeton: Princeton University Press).
4. Fisher, R.A. (1958). The Genetical Theory of
Natural Selection, Second Revised Edition
(New York: Dover Publications Inc).
5. Yasui, Y. (1997). A ‘good sperm’ model can
explain the evolution of costly multiple mating
by females. Am. Nat. 149, 573–584.
6. Curtsinger, J.W. (1991). Sperm competition and
the evolution of multiple mating. Am. Nat. 138,
7. Keller, L., and Reeve, H.K. (1995). Why do
females mate with multiple males? The sexually
selected sperm hypothesis. Adv. Stud. Behav.
8. Pizzari, T., and Birkhead, T.R. (2002). The
sexually-selected sperm hypothesis:
sex-biased inheritance and sexual
antagonism. Biol. Rev. 77, 183–209.
9. Simmons, L.W., and Kotiaho, J.S. (2007).
Quantitative genetic correlation between trait
and preference supports a sexually selected
sperm process. Proc. Natl. Acad. Sci. USA 104,
10. Swanson, W.J., and Vacquier, V.D. (2002). The
rapid evolution of reproductive proteins. Nature
Rev. Genet. 3, 137–144.
11. Hosken, D.J., Garner, T.W.J., and Ward, P.I.
reproductive characters. Curr. Biol. 11, 489–493.
12. Martin, O.Y., and Hosken, D.J. (2003). The
evolution of reproductive isolation through
sexual conflict. Nature 423, 979–982.
13. Morrow, E.H., and Gage, M.J.G. (2000). The
evolution of sperm length in moths. Proc. Roy.
Soc. Lond. B 267, 307–313.
14. Minder, A.M., Hosken, D.J., and Ward, P.I.
(2005). Co-evolution of male and female
reproductive characters across the
Scathophagidae (Diptera). J. Evol. Biol. 18,
15. Miller, G.T., and Pitnick, S. (2002).
Sperm-female coevolution in Drosophila.
Science 298, 1230–1233.
16. Morrow, E.H., and Gage, M.J.G. (2001).
Artificial selection and heritability of sperm
length in Gryllus bimaculatus. Heredity 87,
17. Pattarini, J.M., Starmer, W.T., Bjork, A., and
Pitnick, S. (2006). Mechanisms underlying the
sperm quality advantage in Drosophila
melanogaster. Evolution 60, 2064–2080.
18. Garcia-Gonzalez, F., and Simmons, L.W. (2007).
Shorter sperm confer higher competitive
fertilization success. Evolution 61,
19. Simmons, L.W., and Kotiaho, J.S. (2002).
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and genotypic variation and condition
dependence in sperm competition traits.
Evolution 56, 1622–1631.
20. Gage, M.J.G., and Morrow, E.H. (2003).
Experimental evidence for the evolution of
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1Centre for Ecology, Evolution and
Conservation, School of Biological Sciences,
University of East Anglia, Norwich Research
Park, Norwich NR4 7TJ, UK.2Zoological
Museum, University of Zurich,
Winterthurerstrasse 190, CH-8057 Zurich,
E-mail: email@example.com, demont@
Establishment of proper attachments between chromosomes and
microtubules is essential for the accurate division of the genome. Two recent
studies indicate that these attachments are facilitated by the geometry of
chromosomes and the bipolar arrangement of spindle microtubules.
Jason Stumpff and Charles L. Asbury
Cell division in eukaryotes involves
interactions between microtubules of
the mitotic spindle and protein
complexes called kinetochores, which
assemble at centromeric regions of
chromosomes. Paired sister
chromosomes in mitosis, or paired
homologous chromosomes in meiosis
I, can only be segregated properly if
their kinetochores bind to microtubules
that emanate from opposite spindle
poles, an arrangement known as
bi-orientation (Figure 1). Errors in
segregation lead to aneuploidy, the
cause of human trisomy disorders
and a hallmark of cancer. Thus, the
mechanisms promoting bi-orientation
have been a subject of intense
investigation for many years. Two
recent studies, one of which appeared
in Current Biology, suggest that
spindle and chromosome geometry
are sufficient to achieve
Historically, two general
mechanisms for bi-orientation have
been considered (reviewed in ). The
first relies on geometric constraints
that compel paired kinetochores to
face towards opposite directions. This
directional bias, in conjunction with the
bipolar arrangement of microtubules in
the spindle, is thought to promote
attachments between spindle poles
and kinetochores that face each other
and provide a means to avoid making
attachment errors. The second
mechanism relies on a widely
conserved phospho-regulatory system
that corrects erroneous attachments
by promoting detachment when paired
chromosomes are connected to the
same spindle pole, an arrangement
called syntelic attachment (Figure 1A).
Syntelic attachments generate less
tension than bi-oriented attachments,
and this reduced tension is thought to
activate the Aurora family of kinases,
which in turn causes detachment of
kinetochore–microtubules. The relative
importance of these two mechanisms
in ensuring bi-orientation, however,
Recently, powerful assays for
analyzing chromosome bi-orientation
and segregation have been developed
in budding yeast (Saccharomyces
cerevisiae). With advances in imaging
and molecular techniques, researchers
can now monitor the attachment status
and subsequent segregation of
individual chromosomes in live cells
(reviewed in ). Fluorescent markers
that bind near the centromeres of a
specific chromosome pair appear as a
single focus when the pair is attached
to just one spindle pole. Once
bi-orientation is achieved, the
centromeres undergo transient
separations and two fluorescent foci
can be discerned. The marked chro-
mosomes canthen be followed through
the division process for unambiguous
determination of segregation errors.
A few years ago, Dewar and
co-workers  used this bi-orientation
assay to test the relative importance of
chromosome geometry and error
correction mechanisms during mitosis.
Their study assayed bi-orientation of
containing two yeast centromeres,
which presumably lack any geometric
bias. When introduced into cells, these
dicentric minichromosomes usually
achieved bi-orientation, provided that
the budding yeast aurora kinase,
Ipl1, was active. In contrast, the
minichromosomes rarely bi-oriented in
strains with inactive Ipl1. The results of
Dewar et al.  suggest that any
connection that is capable of
transmitting tension across sister
chromosomes is sufficient for
bi-orientation and that geometric
constraints between sister
kinetochores may be dispensable.
However, a geometric contribution to
bi-orientation of native chromosomes
was not strictly ruled out.
Shugoshin-1 (Sgo1) is another
protein implicated in the correction of
sgo1 mutants do not respond to a lack
of tension on kinetochores. However,
chromosome segregation in sgo-1
mutants is largely normal, suggesting
that tension-dependent error
correction is dispensable for mitotic
division. Interestingly, the ability of
sgo1 mutants to segregate
chromosomes can be compromised by
treatment with microtubule-
depolymerizing drugs . Normally,
cells delay mitosis when microtubules
No geometric bias
Figure 1. Two ways to promote proper attachment of sister kinetochores to spindle microtubules.
(A) If no geometric bias exists, the orientation of the sister kinetochores will be uncorrelated. After one sister has attached a microtubule tip, the
other will bind microtubules emanating from either direction with equal probability. Without bias, sisters will make attachments to microtubules
emanating from the same spindle pole, thus becoming mono-oriented, 50% of the time. Correction of these erroneous attachments occurs
by Ipl1/Sgo1-mediated detachment of one or both kinetochores (presumably triggered by a lack of tension), allowing another attempt at
bi-orientation. Given the high error rate and the fact that multiple sisters must achieve bi-orientation, numerous rounds of detachment and
reattachment would have to occur for all chromosomes to achieve bi-orientation. (B) Alternatively, sister kinetochores may tend to face in
opposite directions as a result of some intrinsic geometric constraint. Binding of one kinetochore to a microtubule emanating from the left
would then predispose its sister to bind a filament emanating from the right. In the context of a bipolar spindle, a strong geometric bias would
favor bi-orientation, without the need for corrective detachment.
Current Biology Vol 18 No 2
are depolymerized but will form Download full-text
spindles and segregate chromosomes
when the drugs are removed. Similar
treatment of sgo1 mutant cells results
removal, chromosome segregation is
defective and the cells die.
In a recent study, Indjeian and
Murray  examined why sgo1
mutants exhibit this mysterious
sensitivity to microtubule poisons.
They assayed bi-orientation in sgo1
mutants following incubation with
microtubule-depolymerizing drugs and
discovered that proper chromosome
attachment and segregation were
strongly correlated with the extent of
spindle-pole separation at the time of
drug removal. Under conditions in
which spindle poles were not
separated, when the drug was
washed-out, bi-orientation and
chromosome segregation were
abnormal as previously observed,
but, under experimental conditions in
which spindle poles were separated
at the time of drug release, proper
attachments were made and cells
underwent successful division. Thus,
bi-orientation in sgo1 mutants
seems to depend on whether
spindle poles are separated when
are established. Since spindle poles
must be separated for the geometry
of paired kinetochores to promote
bi-orientation, this work suggests that
proper spindle geometry and, by
extension, chromosome geometry
are sufficient for successful mitotic
Another recent study reached
a similar conclusion after investigating
the importance of chromosome
geometry for successful meiotic
division . During meiosis I, paired
homologs are held together by sites of
recombination, which can occur far
from the centromere and thus may
not constrain the orientation of
kinetochores. Lacefield and Murray 
studied the correlation between
successful meiotic chromosome
segregation and the position of
recombination events. In ipl1 mutant
cells, chromosome segregation failed
more frequently when recombination
sites were positioned far from the
centromere. Normal segregation was
restored when an artificial tether was
used to hold chromosomes together
near the centromere, indicating that
geometric constraints imposed on
meiotic centromeres are sufficient for
successful division. Taken together,
these two studies [1,2] suggest that
tension-dependent error correction is
dispensable during both mitosis and
meiosis inbudding yeast, providedthat
chromosome and spindle geometry are
If yeast cells with normal
chromosome and spindle geometry do
not rely heavily on error correction,
then why do ipl1 mutants fail to
properly segregate their chromosomes
the majority of the time ? One
possible explanation is that Ipl1
function is needed both for error
correction and for establishing proper
spindle and chromosome geometry.
Consistent with this idea, recent
bipolar spindle assembly . If the
relative timing of pole separation is
disrupted in ipl1 mutants, then the
intrinsic geometry needed to avoid
syntelic attachments may be
compromised at the time when
are being made. If Ipl1 has this
additional role, but Sgo1 is involved
only in error correction, this could
explain why the severity of
chromosome segregation defects is
these two genes [6,7,9,10]. Further
investigation of Ipl1’s role in spindle
assembly may provide key information
about the regulation of spindle
geometry and bi-orientation.
in creating the proper chromosome
geometry. Exactly how this geometry
is established remains unclear. An
intriguing idea is that formation of a
centromere-specific chromatin loop
regulates kinetochore orientation,
this structure might be formed [11,12].
In conclusion, both intrinsic
geometry and error correction appear
to promote chromosome bi-orientation
in budding yeast. Why would it be
beneficial for cells to employ two
mechanisms to ensure bi-orientation
when either seems to be sufficient?
Perhaps the combination is optimal for
segregating chromosomes with both
ensures accuracy, but the required
detachment and reattachment cycle
may take a considerable amount of
time. By reducing the error rate,
a geometry-based mechanism that
promotes bi-orientation during the
initial stages of microtubule
attachment could make the process far
more time-efficient (Figure 1). These
concepts are likely to be applicable to
bi-orientation in other eukaryotes as
well. In vertebrate cells, for example,
paired mitotic kinetochores are
presumed to be geometrically
constrained, spindle poles separate
before chromosomes attach to the
spindle and the Aurora B kinase is
required to achieve normal
the molecular basis of chromosome
and spindle geometry and how it
promotes bi-orientation should prove
to be a fascinating line of investigation
for years to come.
1. Indjeian, V.B., and Murray, A.W. (2007).
Budding yeast mitotic chromosomes have an
intrinsic bias to biorient on the spindle. Curr.
Biol. 17, 1837–1846.
2. Lacefield, S., and Murray, A.W. (2007). The
spindle checkpoint rescues the meiotic
segregation of chromosomes whose
crossovers are far from the centromere. Nat.
Genet. 39, 1273–1277.
3. Tanaka, T.U., Stark, M.J., and Tanaka, K.
(2005). Kinetochore capture and bi-orientation
on the mitotic spindle. Nat. Rev. Mol. Cell Biol.
4. Tanaka, T.U. (2002). Bi-orienting chromosomes
on the mitotic spindle. Curr. Opin. Cell Biol. 14,
5. Dewar, H., Tanaka, K., Nasmyth, K., and
Tanaka, T.U. (2004). Tension between two
kinetochores suffices for their bi-orientation on
the mitotic spindle. Nature 428, 93–97.
6. Indjeian, V.B., Stern, B.M., and Murray, A.W.
(2005). The centromeric protein Sgo1 is
required to sense lack of tension on mitotic
chromosomes. Science 307, 130–133.
7. Biggins, S., Severin, F.F., Bhalla, N.,
Sassoon, I., Hyman, A.A., and Murray, A.W.
(1999). The conserved protein kinase Ipl1
regulates microtubule binding to kinetochores
in budding yeast. Genes Dev. 13, 532–544.
8. Kotwaliwale, C.V., Frei, S.B., Stern, B.M., and
Biggins, S. (2007). A pathway containing the
Ipl1/aurora protein kinase and the spindle
midzone protein Ase1 regulates yeast spindle
assembly. Dev. Cell 13, 433–445.
9. Biggins, S., and Murray, A.W. (2001). The
budding yeast protein kinase Ipl1/Aurora
allows the absence of tension to activate the
spindle checkpoint. Genes Dev. 15, 3118–3129.
10. Tanaka, T.U., Rachidi, N., Janke, C., Pereira, G.,
Galova, M., Schiebel, E., Stark, M.J., and
Nasmyth, K. (2002). Evidence that the Ipl1-Sli15
(Aurora kinase-INCENP) complex promotes
chromosome bi-orientation by altering
kinetochore-spindle pole connections. Cell 108,
heterochromatin in centromere function. Philos.
Trans. R. Soc. Lond. B. Biol. Sci. 360, 569–579.
12. Bloom, K., Sharma, S., and Dokholyan, N.V.
(2006). The path of DNA in the kinetochore.
Curr. Biol. 16, R276–R278.
13. Cimini, D. (2007). Detection and correction of
merotelic kinetochore orientation by Aurora B
and its partners. Cell Cycle 6, 1558–1564.
Department of Physiology and Biophysics,
University of Washington, Seattle,
Washington 98195, USA.