© 1988 Nature Publishing Group
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clustered in one of the three exons: the
proportion of nucleotide sites that are
polymorphic in this exon is three and a
half times that in the other exons and
between two and four times that in the
introns'. Thus, Dover would need to post-
ulate that conversion influenced both
flanking regions, both introns and two
exons, but not the third exon! Hudson
et al. have a more parsimonious
interpretation.
Furthermore, the theoretical founda-
tion for some of Dover's claim is lacking.
Dover offers no support at all for his claim
that unbiased conversion will decrease the
polymorphism at a locus but not affect its
rate of divergence. Because unbiased
conversion amounts to an additional
mechanism of drift, one might expect that
it would increase the rate of divergence
between species. Until we see a formal
model, we will remain unconvinced that
unbiased conversion has any effect on
intraspecific nucleotide polymorphism
beyond that attributable to drift.
Do Dover's 'turnover mechanisms'
have any potential at all to explain the
Adh data? Slippage, unequal crossing
over and transposition all generate length
mutations. Thus none of them can explain
the Adh data where aligned nucleotide
sequences were used to determine div-
ergence, and length variations were
excluded from the measure of poly-
morphism. These mechanisms have no
special significance to tests of this sort.
They act simply to increase the mutation
rate, and thus cannot increase divergence
between species without also increasing
polymorphism within species. They
cannot generate discrepancies from the
neutral model as long as we are careful to
count the result of a single mutational
event as no more than one change (this is
most easily done by excluding length
mutations, as Hudson et al. did).
Unbiased conversion is just a mech-
anism of drift, but biased conversion is
another matter. It is natural selection at
the level of the gene and, like other select-
ive forces, can increase or decrease either
polymorphism or divergence, or both. For
example, the rate of divergence would be
decreased if the currently fixed allele had
the ability to convert other alleles. This
amounts to the gene being constrained
by selection: new alleles are at a dis-
advantage, polymorphism is reduced, and
there is no departure from the neutral
model. As we noted', departures can arise
from the fixation of a new selectively
favoured allele, whether it is by biased
conversion or selection at the phenotypic
level. Here polymorphism is reduced
while overall divergence is unaffected.
More relevant to the excess poly-
morphism of the Adh locus is the pos-
sibility that a system of balanced, biased
conversion among three or more alleles
might allow an accumulation of neutral
polymorphism on each allele. This
possibility is consistent with the conclusion
of Hudson et al. that the excess variation
in one exon of the Adh locus suggests a
selectively maintained polymorphism in
the area. The only viable explanation for
the Adh data that we can construct from
Dover's turnover mechanism is essentially
the one proposed by Hudson et al . .
What can we conclude about Dover's
general point, that we need to consider
turnover mechanisms as a force in mol-
ecular evolution which is distinct from
natural selection and neutral drift? Where
they are unique events, slippage, unequal
crossing over and transposition are simply
mechanisms of mutation. Biased conver-
sion, or any given mutation that occurs
repeatedly, is a form of natural selection
at the gene level (which may or may not be
opposed by selection at higher levels).
Unbiased conversion is a mechanism of
drift. In short, the effects of turnover
mechanisms may be understood within
the contexts of natural selection and
neutral drift. To the extent that they are
special at all, it is only because they
provide a means to transfer information
between members of a repeated gene
family. All mutations may not be equally
likely, and they may differ in their forward
and backward rates, but these possibilities
are already incorporated into existing
population-genetics models'. We are
reminded of Maynard Smith's concluding
statement to the book edited by Dover
and Flavell': "people have been thinking
about evolution for a long time, and ...
some of their conclusions may be worthy
of attention."
There is no mysterious third force. The
Adh data will ultimately be explained with
reference to natural selection and neutral
drift. We need to determine the relative
roles of these two forces, and the test
developed by Hudson et al., which was the
subject of our original report, goes a
considerable way towards that goal.
JULEE A. GREENOUGH
PAUL H. HARVEY
Department of Zoology,
University of Oxford,
South Parks Road,
Oxford OXI 3PS, UK
I. Hudson, R.R .. Kreitman, M.E. & Aguade. M. Genetics
116, 153-159 (1987).
2. Greenough, J.A. & Harvey, P.H. Nature 329, 585-586
(1987).
3. Kreitman, M. Ox[ Surv. evol. Bioi. 4, 38--60 (1987).
4. Falconer, D.S. Introduction to Quantitative Genetics 2nd
edn (Longman. London, 1981).
5. Dover. G.A. & Flavell, R.B. (eds) Genome Evolution
(Academic, London. 1982).
Is there a role for herpesvirus
in AIDS?
SIR-Latchman
1
has challenged the signi-
ficance of our original observation' on
herpes simplex virus (HSV)-induced
human immunodeficiency virus (HIV)
trans-activation'. He argues: first that the
observed transcriptional activation of
HIV is nonspecific, as others have shown
that HSV infection can activate hetero-
logous genes; second that the activation is
limited to the transfected gene and does
not generally apply to endogenous genes,
as a transfected, but not an endogenous,
beta-globin gene can be trans-activated;
and third that the system used may not be
relevant to the regulation of expression of
the proviral HIV genome, because tran-
scription of other viral genes is signifi-
cantly suppressed by HSV infection.
Although valuable, Latchman's reason-
ing is incomplete and we would like to add
three comments. First, the trans-activa-
tion of HIV-LTR by HSV infection is
specific in that none of the heterologous
promoters were activated within the same
experiment. Furthermore, in our most
recent studies', we have localized a 73-
base-pair sequence from the HIV-LTR
which can confer HSV responsiveness to
a heterologous gene that was previously
unresponsive to HSV infection. Second,
the HIV genome is not an endogenous
gene, therefore the differential activation
of a transfected gene and endogenous
genes is irrelevant for this system. There is
no evidence for site-specific retroviral
integration in infected cells, and thus the
integration of provirus into the cellular
chromatin upon either infection or trans-
fection will be a random event. Third,
Latchman states that the "studies involving
cells latently infected with HIV itself will
be necessary to confirm the provocative
suggestion of Mosca et al. ". We have
addressed this statement directly by con-
structing a permanent SW480 colon
carcinoma' cell line containing HIV pro-
viral DNA. This cell line has a low con-
stitutive level of reverse-transcriptase
activity which is augmented 14-fold by
HSV-1, 12-fold by transfection with the
combination of HSV IE175 (ICP-4) and
IEllO (ICP-0) genes, and 13-fold by
transfection with the HIV-1 tatllll gene.
These data indicate that infection with
HSV is able to enhance the replication of
infectious HIV.
In addition to our results, recent data of
Quinn et al.
5
suggest that individuals with
previous herpesvirus infections are par-
ticularly susceptible to either HIV infec-
tion or disease progression. Thus, it is
becoming increasingly clear that herpes-
viruses have a role in HIV infection.
J.D. MoscA
D.P. BEDNARIK
N.B.K. RAJ
P.M. PITHA
The Johns Hopkins University
Oncology Center, Baltimore,
Maryland 21205, USA
I. Latchman, D.S. Nature 325,487 (1987).
2. Mosca, J.D. eta/. Nature325.67-70(1987).
3. Mosca J.D. eta/. Proc. natn. A cad. Sci. U.S.A. 84, 7408-7412
(1987).
4. Adachi, A. eta/. J. V!rol. 59,284-291 (1986).
5. Quinn, T.C. eta/. J. Am. med. Soc. 257,2617-2621 (1987).