Brian Charlesworth

Why bother? The evolutionary
genetics of sex

It is an astonishing ½nding–derived

from more than a century of painstaking
research into the cellular basis of repro-
duction in a huge variety of organisms–
that sex is the most prevalent mode of
reproduction among the great division
生命的 (the eukaryotes), which includes
动物, green plants, algae, fungi, 和
protozoa.1

To geneticists, sexual reproduction is
the formation of a new individual from
a cell (zygote) produced by the union of
two different cells (gametes). 在情况下
of animals, the gametes are an egg and
a sperm. When the resulting individual
reproduces, its gametes contain a patch-
work of genetic information derived
from each of the two gametes that gen-
erated it (a process called recombination).

Brian Charlesworth, a Foreign Honorary Mem-
ber of the American Academy since 1996, is Roy-
al Society Research Professor at the University of
爱丁堡. He is the author of “Evolution in Age-
Structured Populations” (1980) and coauthor of
“Evolution: A Very Short Introduction” (2003)
in addition to numerous journal articles. His re-
cent research focuses on molecular evolution and
variation, the evolution of genetic and sexual sys-
特姆斯, and the quantitative genetics of life-history
特质.

Recombination happens regardless of
whether the zygote divides to form
many separate single-celled individuals
(as in simple organisms, like yeast), 或者
whether the daughter cells remain asso-
ciated to produce a complex multicellu-
lar organism, like an oak tree or a per-
儿子. 相比之下, with asexual reproduc-
的, a single parent produces offspring
that are usually exact genetic replicates
of itself.

We have good grounds for believing
that regular sexual reproduction evolved
very early in the history of the eukary-
otes, and that most instances of asexual
reproduction among them are the result
of subsequent evolution. All mammals
and all birds reproduce sexually, 但仅

1 I thank Deborah Charlesworth for her com-
ments on the manuscript. J. Maynard Smith,
The Evolution of Sex (剑桥: 剑桥
大学出版社, 1978); G. 钟, The Master-
piece of Nature (伦敦: Croom-Helm, 1982).
A regular cycle of sexual reproduction is ab-
sent from the other division of life (prokary-
otes), which encompasses bacteria and viruses.
有, 然而, often detectable exchanges
of pieces of genetic information between indi-
viduals within prokaryote populations, involv-
ing a variety of processes that act as a substitute
for sex. See J. Maynard Smith, 氮. H. 史密斯, 中号.
O’Rourke, 和乙. G. Spratt, “How Clonal are
Bacteria?” Proceedings of the National Academy
科学系 90 (1993): 4384–4388.

代达罗斯之泉 2007

我

D
哦
w
n
哦
A
d
e
d

F
r
哦
米
H

t
t

:
/
/

d
我
r
e
C
t
.

米

我
t
.

e
d
你
d
A
e
d
A
r
t
我
C
e
–
p
d

我

F
/

1
3
6
2
3
7
1
8
2
9
2
8
6
d
A
e
d
2
0
0
7
1
3
6
2
3
7
p
d

乙
y
G
你
e
s
t

哦
n
0
8
S
e
p
e
米
乙
e
r
2
0
2
3

Brian
查尔斯-
值得
在
性别

a few dozen species of reptiles, amphib-
ia, and ½sh reproduce asexually.2 Simi-
larly, 只关于 0.1 percent of the over
three hundred thousand species of flow-
ering plants are thought to reproduce
asexually.3

Most asexual species seem to be of
recent evolutionary origin, since they
have close sexual relatives and evident-
ly have not had time to proliferate into
diverse forms.4 There are only one or
two cases where an asexual group of
multicellular organisms seems to have
been around long enough to diversify,
most notably the Bdelloid rotifers. 这些
minute animals, which live in transient
freshwater habitats (such as drops of
water on mosses), have been classi½ed
into several hundred species on the ba-
sis of anatomical and molecular differ-
ences among them. No males have ever
been found–and study of their genomic
makeup supports the view that they rep-
resent an ancient asexual group, 许多
millions of years old.5 Nonetheless, 这
Bdelloid rotifers represent the exception,
and not the rule.

Asexuality seems to be more common

among single-celled eukaryotes, 喜欢
protozoa, but the dif½culty of studying
their life cycles in nature makes it hard
to exclude the cryptic occurrence of sex.
And even so, regular sexual reproduc-
tion is widely distributed among single-

2 Maynard Smith, The Evolution of Sex; 钟,
The Masterpiece of Nature.

3 A. 中号. Koltunow, “Apomixis–Molecular
Strategies for the Generation of Genetically
Identical Seeds Without Fertilization,” Plant
Physiology 108 (1995): 1345–1352.

4 Maynard Smith, The Evolution of Sex; 钟,
The Masterpiece of Nature.

celled eukaryotes. The common features
of the cellular and molecular mecha-
nisms involved in sexual reproduction in
these and multicellular eukaryotes show
that the cellular machinery involved in
sexual reproduction probably had a sin-
gle origin around the time of the evolu-
tion of the ½rst eukaryotes, about two
billion years or so ago.

The big question about sex is: 为什么

bother? It seems much simpler for or-
ganisms to produce offspring without
going to the trouble of making gametes,
which in the case of animals like our-
selves can only meet each other as a re-
sult of elaborate behavioral and anatom-
ical adaptations. Why should there be
males? Why don’t women simply pro-
duce babies in the same way as Bdelloid
rotifers: an egg is generated by the same
process of cell division that makes the
cells of the rest of the body; it then de-
velops into an offspring. 的确, 为什么
not just split in half and regenerate the
missing half, as some flatworms do?

These questions are not new: as Ed-
ward Gibbon maliciously pointed out,
the early fathers of the Christian church
were sorely troubled by the question of
why God had not provided human be-
ings with “some harmless mode of veg-
etation” with which to propagate them-
自己. Their objections to sex were, 的
课程, purely moral. But even the amor-
al intellectual framework of neo-Dar-
winian evolutionary biology has raised
a searching question concerning the
prevalence of sex–or, more speci½cally,
about its so-called twofold cost, 哪个
John Maynard Smith brought to the at-
tention of biologists in 1971.6 一个可以

5 我. Arkhipova and M. Meselson, “Deleterious
Transposable Elements and the Extinction of
Asexuals,” Bioessays 27 (2005): 76–85.

6 J. Maynard Smith, “The Origin and Main-
tenance of Sex,” in G. C. 威廉姆斯, 编辑。, 团体
Selection (芝加哥: Aldine-Atherton, 1971),
163–175.

代达罗斯之泉 2007

我

D
哦
w
n
哦
A
d
e
d

F
r
哦
米
H

t
t

:
/
/

d
我
r
e
C
t
.

米

我
t
.

e
d
你
d
A
e
d
A
r
t
我
C
e
–
p
d

我

F
/

1
3
6
2
3
7
1
8
2
9
2
8
6
d
A
e
d
2
0
0
7
1
3
6
2
3
7
p
d

乙
y
G
你
e
s
t

哦
n
0
8
S
e
p
e
米
乙
e
r
2
0
2
3

为什么
bother?

understand this cost by considering a
sexual population with an equal number
of males and females in each generation.
Now imagine that within this population
a mutation arises that causes females to
reproduce asexually by means of all-fe-
male offspring. If the mutation has no
other effect, the average number of off-
spring per mother will be unchanged.
The mutant females will thus produce
twice as many daughters as their sexual
competitors. A simple calculation shows
that the frequency of the mutants within
the female population will double each
generation while they are still rare, 和
that they will spread rapidly through the
人口, replacing the sexual females
and causing the extinction of males.
We can make a similar but slightly
more complicated argument for her-
maphrodite organisms, which include
most flowering plants and many ma-
rine invertebrates. Here the bene½t of
a mutation that produces asexual eggs
is closer to one-and-a-half-fold than
twofold–still a substantial advantage.7
A mutation that causes fertilization of
the egg cells by the male gametes of the
same individual, without signi½cantly
reducing the individual’s ability to fer-
tilize others’ eggs, also has a consider-
able advantage.8 But though many her-
maphrodites can fertilize themselves,
the majority of hermaphrodite species
reproduce primarily by matings between
separate individuals (outcrossing).

The results of these exercises in pop-
ulation-genetic calculations show how

7 D. G. Lloyd, “Bene½ts and Handicaps of
Sexual Reproduction,” 进化生物学 13
(1980): 69–111; 乙. Charlesworth, “The Cost
of Sex in Relation to Mating System,“ 杂志
of Theoretical Biology 84 (1980): 655–671.

8 右. A. Fisher, “Average Excess and Average Ef-
fect of a Gene Substitution,” Annals of Eugenics
11 (1941): 31–38.

surprising it is that sexual species are so
common and have not rapidly evolved
either asexual reproduction or (在里面
case of hermaphrodites) complete self-
fertilization. The question of why her-
maphrodites avoid self-fertilization
has turned out to be the easier one to
回答, as was shown by Charles Dar-
win himself. The answer lies in the phe-
nomenon of inbreeding depression: 这
viability and fertility of the progeny of
matings between close relatives are usu-
ally much lower than those of the proge-
ny of matings between unrelated indi-
个人. Darwin compared experimen-
tally produced individuals, which had
been created either by self-fertilization
or outcrossing in many different species
of plants. He found an almost universal
tendency for the performance (survival,
尺寸, seed production) of the self-fertil-
ized progeny to be much worse than that
of the outcrossed progeny.9 He conclud-
编辑, 正确地, that natural selection disfa-
vors self-fertilization. Subsequent calcu-
lations have shown that a reduction of
关于 50 percent in ½tness to self-fertil-
ized progeny will prevent the spread of
a mutation that causes self-fertiliza-
tion.10 Much larger reductions are often
observed in outcrossing species.11 Odd-
莱, until the 1970s, botanists working on

9 C. 右. Darwin, The Effects of Cross and Self
Fertilisation in the Vegetable Kingdom (伦敦:
John Murray, 1876).

10 Lloyd, “Bene½ts and Handicaps of Sexual
Reproduction”; Charlesworth, “The Cost of
Sex in Relation to Mating System.”

11 C. Goodwillie, S. Kalisz, 和C. G. Eckert,
“The Evolutionary Enigma of Mixed Mating
Systems in Plants: Occurrence, Theoretical
Explanations and Empirical Evidence,“ 年度的
Reviews of Ecology, Evolution and Systematics 36
(2005): 47–79; S. C. H. 巴雷特, “The Evolu-
tion of Plant Sexual Diversity,” Nature Reviews
遗传学 3 (2002): 274–284.

代达罗斯之泉 2007

我

D
哦
w
n
哦
A
d
e
d

F
r
哦
米
H

t
t

:
/
/

d
我
r
e
C
t
.

米

我
t
.

e
d
你
d
A
e
d
A
r
t
我
C
e
–
p
d

我

F
/

1
3
6
2
3
7
1
8
2
9
2
8
6
d
A
e
d
2
0
0
7
1
3
6
2
3
7
p
d

乙
y
G
你
e
s
t

哦
n
0
8
S
e
p
e
米
乙
e
r
2
0
2
3

Brian
查尔斯-
值得
在
性别

the mating systems of plants largely ig-
nored Darwin’s explanation, 也许
because they failed to grasp the implica-
tions of population genetics for under-
standing evolution.

This explanation of the prevalence of
outcrossing raises two further questions.
第一的: why are all hermaphrodite species
not highly outcrossing? 第二: 什么
causes inbreeding depression? 那里
是, 的确, many examples of hermaph-
rodite species that reproduce nearly ex-
clusively by self-fertilization, 包括
the nematode worm Caenorhabditis ele-
gans and the plant Arabidopsis thaliana,
two of the most important ‘model orga-
nisms’ used in the study of cellular and
developmental processes. Just as with
asexuality, highly inbred species seem
often to have originated fairly recently
in evolutionary time from outcrossing
relatives.12 This is true of the two I just
提及.

As was also clear to Darwin, 问题-
able cause of a transition from outcross-
ing to inbreeding is dif½culty in obtain-
ing mates: if you cannot ½nd someone
else to fertilize your eggs, it is better to
fertilize them yourself, even if the off-
spring are of inferior quality. This situa-
tion can arise when a species invades a
new habitat where population density
低. As expected on this idea, oceanic
island populations are rich in inbreeders
compared with animals and plant pop-
ulations on the mainland from which
the colonizing species came. Many oth-
er geographical patterns associated with
breeding systems support this interpre-
tation.13 Thus, it seems likely that in-
breeding depression will generally main-
tain outcrossing, unless fertilization suc-
cess in outcrossing falls below a thresh-
old value, underneath which there is a

12 同上.

13 同上.

代达罗斯之泉 2007

net reproductive advantage to inbreed-
英.

Darwin, 然而, did not have a
convincing explanation for inbreed-
ing depression. But modern genetics
has led to the realization that inbreed-
ing makes individuals homozygous. 在
也就是说, the copy of a given gene
received through the egg is identical
to that received through the sperm. 如果
this gene carries a harmful mutation,
which happens at a low but not entirely
negligible frequency, the offspring will
receive only the mutant type. In an out-
crossing population, 另一方面,
a rare harmful mutation will nearly al-
ways be carried in a single dose, 自从
the copy of the gene in the other gamete
that forms an individual will usually be
普通的.

The exposure of harmful mutations
in a gene in double dose, with no nor-
mal copy present, is thought to be a ma-
jor source of inbreeding depression.14
Although such mutations are individu-
ally very rare within a population, 那里
are so many genes in the genome (关于
twenty-½ve thousand in the case of hu-
芒斯) 那, 集体地, we all carry sev-
eral hundred harmful mutations (差异-
ferent ones are present in different peo-
普莱).15 Most of these have very small ef-
fects on ½tness, but one or two among
the mutations an individual carries can
be lethal when made homozygous, 作为
experiments on the effects of inbreed-
ing in fruit flies and ½sh have demon-
strated.16

14 乙. Charlesworth and D. Charlesworth, “这
Genetic Basis of Inbreeding Depression,” Ge-
netical Research 74 (1999): 329–340.

15 S. Sunyaev et al., “Prediction of Deleterious
Human Alleles,” Human Molecular Genetics 10
(2001): 591–597.

16 中号. J. Simmons and J. F. Crow, “Mutations
Affecting Fitness in Drosophila Populations,”

我

D
哦
w
n
哦
A
d
e
d

F
r
哦
米
H

t
t

:
/
/

d
我
r
e
C
t
.

米

我
t
.

e
d
你
d
A
e
d
A
r
t
我
C
e
–
p
d

我

F
/

1
3
6
2
3
7
1
8
2
9
2
8
6
d
A
e
d
2
0
0
7
1
3
6
2
3
7
p
d

乙
y
G
你
e
s
t

哦
n
0
8
S
e
p
e
米
乙
e
r
2
0
2
3

为什么
bother?

We therefore have a well-supported
theory of what controls evolutionary
transitions from outbreeding to inbreed-
ing in hermaphrodites. Similar consider-
ations probably apply to the less intense
forms of inbreeding found in some spe-
cies with separate sexes. We now need
to ask if there are factors that can over-
come the twofold cost of sex, and main-
tain sexual reproduction against mu-
tations causing asexual reproduction,
analogous to the effect of inbreeding
depression in preventing the spread of
mutations causing inbreeding. There has
been a long and hard search for these,
and it is fair to say that there is still no
consensus about which of them is the
最重要的.

It is worth making a couple of points

before discussing this question in de-
tail. 第一的, we know that mammals can-
not reproduce asexually, because a mam-
mal needs both a paternal and a mater-
nal complement of genes in order to
develop successfully from an egg. 这
is because of a phenomenon known as
imprinting: some genes are temporarily
altered chemically during gamete for-
mation in such a way that they only
produce functional products if they en-
ter the zygote through the sperm, oth-
ers only if they enter through the egg.17
While only a small minority of the to-
tal set of genes is imprinted, failure to
express both copies of some of the im-
printed genes results in death. 它就在那儿-
fore impossible for a mammalian female

遗传学年度回顾 11 (1977): 49–78;
A. McCune et al., “A Low Genomic Number
of Recessive Lethals in Natural Populations
of Blue½n Killi½sh and Zebra½sh,“ 科学 296
(2002): 2398–2401.

to reproduce like a Bdelloid rotifer. 我们
need look no further for an explanation
of mammalian sexuality than this devel-
opmental requirement. But while the
reasons for imprinting are of great in-
terest, and a matter of ongoing debate,
they do not concern us here. Imprinting
does not provide a universal explana-
tion of the maintenance of sex, 自从
other groups of animals and plants do
not have imprinting and contain many
examples of asexual reproduction
他们之中.

A second point is that the problem of
a large cost of sex does not apply to the
origin of sex. The comparative evidence
already discussed suggests that sexual
reproduction ½rst evolved among single-
celled eukaryotes, which lacked any dif-
ferentiation of gametes into male and
女性, IE。, all gametes were of approxi-
mately equal size, as is the case today in
many single-celled organisms.18 With
no asymmetry of gamete size, 有
only a slight automatic advantage to
asexual reproduction.19 This means that
a small advantage to a genetic variant
conferring the ability to reproduce sex-
ually would allow it to spread. In princi-
普莱, 所以, we can explain the origin
of sex by identifying the sources of such
an advantage.

18 The distinction between male and female
gametes is an ancient one, but it is not a re-
quirement for the sexual fusion of gametes.
Once sex evolved, there was probably selec-
tion pressure in many (but not all) groups for
some individuals to produce numerous, 小的,
mobile gametes (the male gametes), 还有其他-
ers to produce a few, 大的, immobile ones (fe-
male gametes). See Maynard Smith, The Evo-
lution of Sex; 中号. G. Bulmer and G. A. 派克,
“The Evolution of Anisogamy: A Game-Theo-
retic Approach,” Proceedings of the Royal Society
乙 269 (2002): 2381–2388.

17 我. 中号. Morison, J. 磷. Ramsay, 和H. G.
Spencer, “A Census of Mammalian Imprint-
英,” Trends in Genetics 21 (2005): 457–465.

19 Maynard Smith, The Evolution of Sex;
Charlesworth, “The Cost of Sex in Relation
to Mating System.”

代达罗斯之泉 2007

我

D
哦
w
n
哦
A
d
e
d

F
r
哦
米
H

t
t

:
/
/

d
我
r
e
C
t
.

米

我
t
.

e
d
你
d
A
e
d
A
r
t
我
C
e
–
p
d

我

F
/

1
3
6
2
3
7
1
8
2
9
2
8
6
d
A
e
d
2
0
0
7
1
3
6
2
3
7
p
d

乙
y
G
你
e
s
t

哦
n
0
8
S
e
p
e
米
乙
e
r
2
0
2
3

Brian
查尔斯-
值得
在
性别

We still have to solve the problem of
how sex is maintained in the face of its
cost in species with male and female
gametes. One solution is to appeal to the
differential extinction of asexual popula-
tions.20 Imagine the following situation:
we have a set of sexually reproducing
物种, among which from time to time
a member is successfully invaded by an
asexual mutant. 然而, the asexual
species do not do as well as their sexual
rivals, in terms of their long-term ability
to survive extinction, and so they even-
tually disappear. With the right balance
between this species-level disadvantage
and the rate of conversion from sex to
asex, the majority of species will remain
性的.

This explanation ½ts many of the
broad patterns of the distribution of
asexuality. Similar patterns apply to
highly inbreeding species; once a spe-
cies has become highly inbreeding, 它
behaves in many ways as though it is
asexual. This is because individuals that
are homozygous for most of their genes
produce offspring that are genetically
nearly identical to themselves. It seems
that the long-term evolutionary fate of
both inbreeders and asexuals may be
such that extinction is much more like-
ly for them than for their outcrossing,
sexual relatives.21

Evolutionary biologists are, for good

原因, rather hostile to the idea that
selection among species plays a major
role in evolution, compared with selec-
tion among individuals. As R. A. Fisher
once wrote, “Unless individual advan-
tage can be shown, natural selection
affords no explanation of structures or
instincts which appear to be bene½cial

20 Maynard Smith, The Evolution of Sex.

21 同上。; 巴雷特, “The Evolution of Plant
Sexual Diversity.”

代达罗斯之泉 2007

to the species.”22 However, even Fisher
was prepared to make an exception for
“sexuality itself” and proposed an ex-
planation for the maintenance of sex
based on the inability of asexual species
to evolve as rapidly as sexual rivals.23

It may, 所以, be suf½cient to look
for factors that confer a quite modest ad-
vantage to sexual reproduction, not nec-
essarily large enough to prevent invasion
by an asexual mutant, but which cumu-
latively increase chances of survival in
the long run. There is no shortage of
candidates; 的确, as the Grand Inquis-
itor said in The Gondoliers, “[时间]here is
no probable, possible shadow of doubt–
no possible doubt whatever . . . ” that we
have identi½ed the major candidates. 作为
in his case, 然而, we do not know
which is the right one, and of course the
different possibilities are not mutually
exclusive. I will only briefly survey some
of the major theories under discussion,
as well as some of the relevant empirical
evidence.24
The major advantage of sexual repro-

duction is the fact that genetic recom-
bination can only occur with sex. 简短的-
ly mentioned at the beginning of this
散文, this process now needs to be de-
½ned more precisely. Gametes are hap-

22 Fisher, “Average Excess.”

23 右. A. Fisher, The Genetical Theory of Natural
Selection. A Complete Variorum Edition (牛津:
牛津大学出版社, 1999).

24 Maynard Smith, The Evolution of Sex; 钟,
The Masterpiece of Nature; 右. 乙. Michod and
乙. 右. 莱文, 编辑。, The Evolution of Sex (Sunder-
土地, 大量的。: Sinauer, 1988); 氮. H. Barton and
乙. Charlesworth, “Why Sex and Recombina-
的?“ 科学 281 (1998): 1986–1990; S. 磷.
Otto and T. Lenormand, “Resolving the Par-
adox of Sex and Recombination,” Nature Re-
views Genetics 3 (2002): 256–261.

我

D
哦
w
n
哦
A
d
e
d

F
r
哦
米
H

t
t

:
/
/

d
我
r
e
C
t
.

米

我
t
.

e
d
你
d
A
e
d
A
r
t
我
C
e
–
p
d

我

F
/

1
3
6
2
3
7
1
8
2
9
2
8
6
d
A
e
d
2
0
0
7
1
3
6
2
3
7
p
d

乙
y
G
你
e
s
t

哦
n
0
8
S
e
p
e
米
乙
e
r
2
0
2
3

为什么
bother?

loid cells–they contain only one copy
of each gene in the genome. The genes
are parts of dna molecules called chro-
mosomes, and each chromosome carries
a set of hundreds or thousands of genes
concerned with different cellular func-
系统蒸发散. (In the human genome, 有
twenty-three different chromosomes
in an egg or a sperm cell.) In a primitive
unicellular organism, such as the green
alga Chlamydomonas, the two gametes
fuse to form a zygote. The zygote is thus
diploid, IE。, it contains two sets of chro-
mosomes, one from each parental gam-
ete. After a resting phase, the zygote
then undergoes two cell divisions called
meiosis, but each chromosome only un-
dergoes one round of division. 编号-
ber of chromosomes is thereby reduced
to the haploid number. If this did not
发生, chromosome numbers would
double at each cycle of sexual reproduc-
的.

An extraordinary thing happens at
the ½rst division of meiosis: each pair
of maternal and paternal chromosomes
comes together, and the partners line up
beside each other. A number of breaks
occur at the same place on each partner,
and these are repaired in such a way that
the material on each partner is now part-
ly maternal and partly paternal, in a re-
ciprocal pattern. The resulting products
then part from each other at the ½rst di-
vision of the cell. This is followed by the
second division, resulting in four hap-
loid cells, in which each chromosome
is made up of segments of paternal and
maternal material. These cells go on di-
viding by the normal cell division pro-
过程, in which chromosomes split into
two daughter chromosomes. 最终,
these differentiate into gametes, 哪个
fuse with other gametes to restart the
循环.

This basic pattern is found through-
out the single-celled eukaryotes, 形式-

ing a major part of the evidence for the
ancient origin of sex. Much the same
holds true for animals like ourselves,
except that with us the diploid zygote
divides by normal cell divisions to pro-
duce the diploid cells that make up most
of our body. Meiosis is postponed until
the production of eggs or sperm in the
reproductive organs.

Accompanying the process of sexual

fusion of cells is, 所以, 一个过程
of mingling of material from maternal
and paternal chromosomes. This is why
no two people in the world are exactly
alike genetically, except for identical
twins. To see this, consider the case of
a mating between two Chlamydomonas
gametes, which differ at two different
locations on a chromosome. One gam-
ete is aband the other is ab, 哪里的
alternatives at each site are Aversus a
and Bversus b, 分别. The zygote
will contain both aband ab. In the ab-
sence of recombination, the gametes
derived from this zygote will be either
abor ab, with equal probability. 但
with recombination, we will also see
the combinations Ab and aB. The fre-
quency with which these are found is
the recombination frequency for the two
locations–and it is higher, the larger
the distance between them on the chro-
mosome.

Geneticists discovered recombination

by carrying out crosses in which they
could detect the presence of the variants
at the two locations because they affect-
ed visible properties of the individuals
carrying them. We can measure recom-
bination frequencies by counting the
numbers of offspring of the four differ-
ent types. Exactly the same holds for hu-
mans as for Chlamydomonas, except that
our diploidy and small family sizes make
it much harder to measure recombina-
的. Genes at distant locations on the
same chromosome, and genes on differ-

代达罗斯之泉 2007

我

D
哦
w
n
哦
A
d
e
d

F
r
哦
米
H

t
t

:
/
/

d
我
r
e
C
t
.

米

我
t
.

e
d
你
d
A
e
d
A
r
t
我
C
e
–
p
d

我

F
/

1
3
6
2
3
7
1
8
2
9
2
8
6
d
A
e
d
2
0
0
7
1
3
6
2
3
7
p
d

乙
y
G
你
e
s
t

哦
n
0
8
S
e
p
e
米
乙
e
r
2
0
2
3

Brian
查尔斯-
值得
在
性别

ent chromosomes (which behave inde-
pendently of each other during meiosis),
have recombination frequencies of 50
百分. Locations very close to each
other on a human chromosome typical-
ly have a recombination frequency of
around one in one hundred million.

Recombination through sexual repro-
duction allows the production of all pos-
sible combinations of variants at differ-
ent locations in the genome. This has
some staggering implications. 认为
we have one thousand locations in the
genome, each with two different vari-
ants in the population. 的数量
possible types of gametes that can exist
is then 2 raised to the power of 1000,
IE。, 大约 10 其次是 300
noughts. It is currently estimated that
there are about six million variants at
chromosomal sites in human popula-
系统蒸发散, so the true number of combina-
tions is something like 10 其次是
1.8 million noughts.

But if there were no sex and no recom-

bination, new mutations would remain
associated with whatever genetic vari-
ant they happened to be combined with
起初. If in our example the popula-
tion were initially ab, a mutation to A
would create ab and Ab. The population
is likely to be mostly ab for a long time,
so that a mutation from b to Bwould
probably arise in an ab gamete, giving
just three types in the population (ab,
Ab, and aB). The combination abcan
be generated only by a (very unlikely)
further mutation event, or by recombi-
nation in zygotes that carry both aBand
Ab. This is not possible if there is no sex-
ual reproduction, or if the population is
highly inbred (in the latter case, 几乎
all zygotes carry identical pairs of gam-
etes, so that recombination has no ef-
影响). 的确, populations that repro-
duce asexually, or by very close inbreed-
英, characteristically show far fewer

combinations of variants at different lo-
cations than do sexual populations, 只是
as this argument predicts.

现在, if Aand Brepresent variants that

confer higher ½tness on their carriers,
the combination abis likely to be the
½ttest of the four, yet it is unlikely to be
produced in the absence of sex and re-
combination. This suggests that these
facilitate the action of natural selection,
by speeding up the production of selec-
tively favorable combinations of genet-
ic variants. This idea was ½rst clearly
stated around 1930 by R. A. Fisher25 and
H. J. 穆勒,26 and still forms the core of
much thinking about the evolutionary
advantage of sex.

This effect can be realized in numer-
ous different situations. One is when a
population faces selection pressure to
adapt to a new environment. Under a
wide range of circumstances, sex and
recombination then help to accelerate
适应. 而且, mathematical
models demonstrate that genetic fac-
tors that influence the frequency of re-
combination also increase in frequen-
cy in the population under these condi-
系统蒸发散, because they become associated
with the favorable gene combinations
they create.27 Environments that con-
tinually change–such as those created
by interactions between hosts and their
parasites, which are constantly adapting
to each other–are especially likely to
create selection pressures of this kind.
Some have suggested that selection pres-

25 Fisher, The Genetical Theory of Natural Selec-
的.

26 H. J. 穆勒, “Some Genetic Aspects of
性别,” American Naturalist 66 (1932): 118–138.

27 Barton and Charlesworth, “Why Sex and
Recombination?”; Otto and Lenormand, “Re-
solving the Paradox of Sex and Recombina-
”。

代达罗斯之泉 2007

我

D
哦
w
n
哦
A
d
e
d

F
r
哦
米
H

t
t

:
/
/

d
我
r
e
C
t
.

米

我
t
.

e
d
你
d
A
e
d
A
r
t
我
C
e
–
p
d

我

F
/

1
3
6
2
3
7
1
8
2
9
2
8
6
d
A
e
d
2
0
0
7
1
3
6
2
3
7
p
d

乙
y
G
你
e
s
t

哦
n
0
8
S
e
p
e
米
乙
e
r
2
0
2
3

为什么
bother?

sures from parasites may be the major
factor favoring sex.28

The possibility that adaptation to a
new environment promotes increased
recombination has been demonstrated
by experiments involving selection for
traits such as ddt resistance in flies:
these have shown increases in recom-
bination frequencies in addition to the
trait under selection.29 A recent experi-
ment on flour beetles revealed a similar
effect of selection for resistance to a
parasite.30 Furthermore, 实验
where a novel environment challenges
Chlamydomonas populations show that
populations that are allowed to repro-
duce sexually evolve faster than popula-
tions that can only reproduce asexual-
ly.31 Therefore, a body of experimental
data supports the plausibility of this type
of mechanism, although it falls short of
proving that it is indeed the main cause
of the origin and maintenance of sex.
Recombination also allows more ef-
½cient removal of harmful mutations
from the genome. While natural selec-
tion usually keeps these mutations at
very low frequencies, again the sheer
number of genes in the genome ensures
that the total number of such mutations
in the population is very large. 马特-

28 Barton and Charlesworth, “Why Sex and
Recombination?”; Otto and Lenormand, “Re-
solving the Paradox of Sex and Recombina-
化”; 瓦. D. 汉密尔顿, “Sex Versus Non-sex
Versus Parasite,” Oikos 35 (1980): 282–290.

29 S. 磷. Otto and N. H. 巴顿, “Selection for
Recombination in Small Populations,” Evolution
55 (2001): 1921–1931.

30 氧. Fischer and P. Schmid-Hempel, “Selec-
tion by Parasites May Increase Host Recombi-
nation Frequency,” Biology Letters 1 (2005):
193–195.

matical models demonstrate that it is
harder for the population to remove del-
eterious mutations from the genome in
the absence of recombination, 创建一个
selection pressure to maintain recombi-
nation frequencies at a nonzero level.32
These models predict that if recombi-
nation stops, harmful mutations would
eventually become more prevalent, 甚至
spreading throughout the species.33

The Y chromosomes of many species
with separate sexes, including humans,
provide a test case. 这里, males have a
Y chromosome and an X chromosome,
which pair up at meiosis but only recom-
bine over a very small portion of their
length. Females have two X chromo-
somes, which recombine normally with
each other at meiosis. In mammals, 这
Y carries a gene that causes individuals
to develop as males; in the absence of
an intact Y chromosome, an embryo
will develop as a female. 因此, the Y
chromosome determines gender. 但,
paradoxically, its lack of recombination
means that most of the Y behaves like
an asexual genome. This makes it very
vulnerable to the accumulation of harm-
ful mutations. Despite clear evidence
from some remaining genetic similari-
ties that the human X and Y chromo-
somes were once almost identical in ge-
netic makeup (about two hundred mil-
lion years ago), only a handful of genes
out of the thousand or so that were orig-
inally present on the Y now remains–
因此, it is degenerate.34

32 Barton and Charlesworth, “Why Sex and
Recombination?”; Otto and Lenormand, “Re-
solving the Paradox of Sex and Recombina-
”。

33 瓦. 右. 米, “Experimental Tests of the
Adaptive Signi½cance of Sexual Reproduction,”
自然评论遗传学 3 (2002): 241–251.

31 氮. Colegrave, “Sex Releases the Speed Limit
on Evolution,“ 自然 420 (2002): 664–666.

34 乙. 时间. Lahn and D. C. 页, “Four Evolution-
ary Strata on the Human X Chromosome,” Sci-

代达罗斯之泉 2007

我

D
哦
w
n
哦
A
d
e
d

F
r
哦
米
H

t
t

:
/
/

d
我
r
e
C
t
.

米

我
t
.

e
d
你
d
A
e
d
A
r
t
我
C
e
–
p
d

我

F
/

1
3
6
2
3
7
1
8
2
9
2
8
6
d
A
e
d
2
0
0
7
1
3
6
2
3
7
p
d

乙
y
G
你
e
s
t

哦
n
0
8
S
e
p
e
米
乙
e
r
2
0
2
3

Brian
查尔斯-
值得
在
性别

This pattern has been observed repeat-

edly in other groups where Y chromo-
somes have evolved, quite independent-
ly of each other.35 In a species of fruit fly
called Drosophila miranda, a whole chro-
mosome has become attached to the Y
chromosome, and is inherited in exact-
ly the same way as the original Y. 这是,
然而, only about one million years
老的, giving us an opportunity to study
the early stages of its degeneration.36
Harmful genetic changes on the new Y
chromosome have clearly accumulat-
编辑:37 about one-third of the genes that
have been examined contain mutations
that destroy their function, and all of
the genes seem to have some minor but
harmful mutations.38 The evolution of
Y chromosomes thus provides particu-
larly striking evidence that the removal
of recombination from a large part of
the genome leads to its gradual evolu-
tionary decline.

在这种情况下, the survival of the popula-

tion is not endangered, since selection
has acted to compensate for the degen-
eration of the Y by raising the rate at

恩斯 286 (1999): 964–967; D. Charlesworth,
乙. Charlesworth, and G. Marais, “Steps in
the Evolution of Heteromorphic Sex Chro-
mosomes,” Heredity 95 (2005): 118–128.

35 同上.

36 同上。; 中号. Steinemann and S. Steinemann,
“Enigma of Y Chromosome Degeneration:
Neo-Y and Neo-X Chromosomes of Drosoph-
ila miranda a Model for Sex Chromosome
进化,” Genetica 102/103 (1998): 409–
420; D. Bachtrog, “Sex Chromosome Evolu-
的: Molecular Aspects of Y Chromosome
Degeneration in Drosophila,” Genome Research
15 (2005): 1393–1401.

37 Steinemann and Steinemann, “Enigma of Y
Chromosome Degeneration.”

38 Bachtrog, “Sex Chromosome Evolution.”

代达罗斯之泉 2007

which gene products arise from the un-
impaired X chromosome in males.39
然而, in an asexually reproducing
物种, it seems likely that the accumu-
lation of harmful mutations would con-
tinue until the species suffers a serious
loss of ½tness. Coupled with the reduced
ability to adapt to changes in the envi-
罗门特, the apparent inability of most
asexual or highly inbreeding species to
maintain themselves does not seem
surprising. 的确, it is actually the per-
sistence of apparently ancient asexual
团体, like the Bdelloid rotifers, 那
raises the most challenging questions
about the evolutionary signi½cance of
sex.40

我

D
哦
w
n
哦
A
d
e
d

F
r
哦
米
H

t
t

:
/
/

d
我
r
e
C
t
.

米

我
t
.

e
d
你
d
A
e
d
A
r
t
我
C
e
–
p
d

我

F
/

1
3
6
2
3
7
1
8
2
9
2
8
6
d
A
e
d
2
0
0
7
1
3
6
2
3
7
p
d

乙
y
G
你
e
s
t

哦
n
0
8
S
e
p
e
米
乙
e
r
2
0
2
3

39 我. Marín, 中号. L. 西格尔, 和乙. S. 贝克, “这
Evolution of Dosage Compensation Mecha-
nisms,” Bioessays 22 (2000): 1106–1114.

40 Maynard Smith, The Evolution of Sex; Arkhi-
pova and Meselson, “Deleterious Transposable
Elements.”
下载pdf