Many primitive organisms are hermaphrodites, meaning each

1
How did separate sexes evolve?
Many primitive organisms are hermaphrodites,
meaning each individual produces both sperm
and eggs In more complex animals, sexes are
usually separate - gender can be
determined by environmental factors
temperature of eggs, for many reptiles
social dominance, for some fish In the most
advanced cases, gender is genetically determined
by sex chromosomes
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Sex chromosomes in humans
Each human genome consists of - 22 pairs of
autosomes, or normal chromosomes - one pair of
sex chromosomes
male
female
X Y
X X
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Sex chromosomes in humans
male
female
X Y
X X
X chromosome contains hundreds of functional
genes Y chromosome is nearly devoid of useful
genes - contains the SRY gene, the master gene
that causes an embryo to develop as a
male - a few genes for male fertility - a few
unrelated genes, and a lot of junk DNA X and Y
chromosomes do not recombine, for most of their
length
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How did sex chromosomes evolve?
Separate sex chromosomes have evolved many times
in different lineages
hermaphrodite environmental sex determination
Sex is determined by one gene
Part of Y stops recombining with the X chromosome
This leads to the evolution of two separate
sexes, with a sex-determining chromosome
for males that no longer recombines with a
homologue -
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Sexually antagonistic genes
Many genes are expressed in both sexes, but some
alleles benefit males, while other alleles
benefit females
Female guppy
Male guppies
Alleles producing bright colors and big tails are
good for males make them attractive to females
The same alleles are bad for females, who dont
need help attracting mates just makes them more
visible to predators
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Female choice vs. sexually antagonistic (SA)
alleles
Results with guppies, flies crickets show
females that chose sexy males, or are forced
to inherit SA alleles, end up having -
sexy sons (guppies) - have high reproductive
success - may be unhealthy, though we will
explore why - lousy daughters - reduced
reproductive success (crickets) - retarded
development (flies) they inherit dads
good-for-boys, bad-for-girls alleles
Rice (1998) PNAS 95 6217 Brooks (2000) Nature
406 67 Fedorka Mousseau (2002) Nature 429 65
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Sexually antagonistic genes
When the male-benefit alleles are expressed in a
male, they confer a fitness advantage (so are
favored by natural selection) When passed to
daughters, they will have a negative effect on
female fitness - selection will now act
against male-advantage alleles - In
this generation, selection favors
female-advantage alleles-- but these will
then get passed on to sons - -
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Sexually antagonistic genes
This leads to an endless back-and-forth cycle,
striking a balance between the sexes
Selection on one sex can interfere with the
adaptive evolution of the other sex -
because they share a common gene pool, alleles
are constantly passing back and forth
between males females - selection will
act against male-advantage alleles in
females, and against female-advantage alleles in
males
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Male-advantage alleles
Alleles that are hostile to females but
beneficial to males can rapidly accumulate in
the male genome, however-- escaping the
effects of counter-selection in females
IF they are only expressed in males How is
this possible?
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As soon as you have a system where one gene
determines if an organism becomes a male, you
quickly accumulate neighboring (linked) alleles
that benefit male reproduction First
observed in guppies
Female
Males
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Hitchhiking the Y
Why do male-advantage traits accumulate on the Y?
-Y is passed father-to-son, never part of
a female genome Alleles can accumulate on the Y
chromosome that benefit males and harm females,
escaping counter-selection in females
colorful males have a mating advantage
colorful females just suffer higher predation
(females dont need help mating) ?
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Hitchhiking the Y
Entire genes can move off of autosomes (normal
chromosomes) and onto the Y chromosome, where
male-advantage alleles can then pile up at
these loci (and exploit females) Y and X
chromosomes stop recombining as an adaptation to
keep male-benefit alleles on Y, and out of
female genome Initially, the fact that Y
chromosomes dont recombine benefits males -
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Are the sexes locked in a genetic war?
Less extreme case can genes not located on Y
chromosome still be sexually antagonistic? -
rare alleles of many (or even most) genes exist
that benefit one sex and harm the
other Normally, alleles that benefit one sex are
countered by alleles that protect or benefit the
other sex (suppressor alleles) This is a Red
Queen process you have to run to stay in place
- also considered an evolutionary arms
race -
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Sexually antagonistic genes are widespread (Rice,
1992)
Experiment make an artificial sex-determining
gene, and see if alleles accumulate at
neighboring loci that benefit that sex
daughters sons
females males
A
A
a
A
a
a
a
a
orange eyes
red eyes
a
a
a
a
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Sexually antagonistic genes are widespread (Rice,
1992)
Experiment make an artificial sex-determining
gene, and see if alleles accumulate at
neighboring loci that benefit that sex
daughters sons
females males
A
A
a
A
a
a
a
a
orange eyes
red eyes
a
a
a
a
throw out red-eyed sons and orange-eyed daughters
16
Sexually antagonistic genes are widespread (Rice,
1992)
Experiment make an artificial sex-determining
gene, and see if alleles accumulate at
neighboring loci that benefit that sex
daughters sons
females males
A
a
a
A
a
a
a
a
red eyes
orange eyes
orange eyes
red eyes
(1) Offspring can only get red eye allele from
mom (2) All red-eyed sons and orange-eyed
daughters are discarded (3) Red eye allele
effectively makes offspring female
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Sexually antagonistic genes are widespread (Rice,
1992)
Prediction alleles that benefit females but harm
males should 1) accumulate in females over
time 2) be linked to the red-eye gene After
29 generations, red-eyed sons were allowed to
survive - these sons have now inherited the
red-eye gene, and with it, any
female-benefit alleles that have hitchhiked
along What would you expect the fitness of
red-eyed sons to be, compared to orange-eyed
brothers?
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Are the sexes locked in a genetic war?
Are females normally locked in an endless arms
race with males? - are they forced to
counter-adapt to male evolution to avoid
being taken advantage of by hostile male-benefit
alleles? Experiment allow male flies to adapt,
while preventing females from evolving
counter-measures to male mating tactics -
in other words, artificially arrest female
evolution, and see if males evolve ways to
exploit females when females cannot
evolve protective responses
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Are the sexes locked in a genetic war? (Rice,
1996)
Experiment allow male flies to adapt, while
preventing females from evolving
counter-measures to male mating tactics
(1) male flies were allowed to evolve freely over
30 generations (2) female flies were cloned,
and identical females were added to the
experimental population in every generation
(3) females always had the same genetic make-up,
could not evolve in response to male
adaptations (a stationary target) (4) over
time, did males get better at exploiting
females?
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Some male traits actively harm females
Results male flies adapted to the female clone
population
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Some male traits actively harm females
Results male flies adapted to the female clone
population
22
Some male traits actively harm females
Results male flies adapted to the female clone
population
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Love is a battlefield
Results male flies adapted to the female clone
population (1) after experiment, males had
24 higher fitness, compared to
un-adapted control males (2) mating became
more frequent and dangerous for females - the
new male alleles lowered female fitness ?
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Chase-away selection
Studies of fruit flies and worms have shown that
male seminal fluid proteins (1) increase
female egg-laying, temporarily (2) inhibit
females from re-mating with other males (3)
directly harm females (lowered survival after
mating) Males alleles push his own reproductive
agenda - force female to put all her
effort into his offspring, at the
expense of her future reproductive success
(and that of his competitors) Females
constantly evolve counter-measures to block
exploitation
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Chase-away selection
Drosophila seminal fluid contains 83 gene
products - thus a highly complex blend of
chemical warfare agents is used to push the
males agenda - Some proteins are for
competing with other males - may harm females as
an indirect consequence - Some directly affect
female behavior Termed chase-away selection
because Y-linked SA alleles must be countered
by X-linked or autosomal alleles in females,
which in turn favors new Y-linked SA alleles,
which in turn.
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The Red Queens Genitalia
Insects often show the signs of intense
evolutionary arms races in their mating
structures (morphological adaptations) - in
species where males have adaptations to prolong
mating (specially shaped genitalia,
claspers, flattened abdomen), females have
corresponding counter-adaptations (spines on
abdomen, tilting abdomen) that inhibit mating
- the degree of sexual armament is random
between species (there is no predictive
power of ancestry), but is always strictly
correlated within a species -
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Chase-away selection genomic imprinting
Mammals that feed their embryos by a placenta
present an opportunity for males to fight
females after mating has occurred Male strategy
force female to invest all of her energy into
his offspring (immediate payoff) Female
strategy save energy for future clutches of
offspring (save for the future) Genes involved
in growth of the fetus are imprinted differently
in males and female gametes
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Chase-away selection genomic imprinting
Imprinted genes are differentially methylated, to
turn expression on or off in the zygote (which
grows into a fetus) Insulin-like growth factor
II gene (IGF-II) is switched off on maternal
chromosome, but on the paternal chromosome this
gene is switched on - promotes general cell
growth - forces female to invest more energy in
fetal growth An unrelated receptor (CI-MPR) is
switched on on the maternal chromosome, but is
turned off on the paternal chromosome - binds
excess IGF-II before it can trigger fetal
growth - allows mother to slow fetal growth
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Chase-away selection genomic imprinting
IGF
mpr
- paternal imprinting accelerate fetal growth
paternal
maternal
- maternal imprinting slow fetal growth
igf
MPR
30
Sexual antagonism depends on mating
system (Holland Rice, 1999)
The previous experiment looked at fly populations
where mating occurred among large groups, and
promiscuity was common - male
exploitation of females quickly evolved when
there there were opportunities for multiple sex
partners New experiment What happens when
flies are forced to pair up and be
monogamous (one partner for life)? monogamy
treatment one female housed with one
male control one females housed with three
males (multiple mating
opportunities, as commonly occurs in nature)
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Effects of monogamy after 34 generations
(1) females reproduced more, but also survived
more (2) males attempted fewer matings
32
Effects of monogamy after 47 generations
reproductive rate
- Monogamy increased the overall reproductive
rate for the population - Also increased the
development rate of offspring - Monogamous
populations became better adapted
development time of offspring
generation
45 46 47
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Effects of monogamy
Monogamy constrains the reproductive success of
both mates to be identical - neither sex
can exploit the other when theres no one else to
mate with Former conflicts between
mates turn into opportunities for mutualism
(i.e., everybody-wins scenarios) - Males
evolved to be less harmful to females -
Females evolved to be less resistant to
male-induced harm Mating fidelity (cooperation)
removed the costs of antagonistic
coevolution between the sexes
34
Degeneration of the Y chromosome return of the
ratchet
To keep male-advantage alleles out of the female
genome, the X chromosome does not recombine
with the Y - the Y thus acts like a clone,
transmitted w/out change from father to
son The Y chromosome eventually begins to
degenerate due to accumulating mutations, due
to the exact same causes discussed earlier for
asexual reproduction (1) Mullers ratchet bad
mutations pile up over time (2) Background
trapping of beneficial mutations Eventually, the
Y has few functional genes (as in humans)
35
Evidence the Y loses functional genes by
background trapping
(1) in D. miranda, part of an autosome
translocated onto the Y - accumulated
many bad mutations in genes on the new
Y, compared to its autosome homologue (2)
steroid sulfate gene is functional on mouse Y,
but is not functional in humans (3) shown
experimentally w/ flies (Rice, 1994) -
make an autosome act like a Y (sex determining)
by not letting it pass through females (throw
out daughters) - after 35 generations,
males had 47 lower fitness -
36
Evidence the Y loses functional genes by
background trapping
(4) in our fancy-tailed friend the guppy, sexy
males have sexy sons -- but the sexier the
son, the more likely he is to die... when
young, before developing his colorful ornaments
also when older fitness benefits
of male-advantage alleles are balanced by -
fitness costs of ornaments... - or,
hitch-hiking deleterious mutations that can only
survive on super-sexy Y
chromosomes
Brooks (2000) Nature 406 67-70
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Full circle gain and loss of the Y
Trick females into mating more
Collects a bunch of male-advantage alleles
Y comes into existence (sex determined by one
gene)
Harm females by mating
Lack of recombination with the X chromosome
38
Full circle gain and loss of the Y
Collects a bunch of male-advantage alleles
Y comes into existence (sex determined by one
gene)
Mutations near the male-advantage
alleles hitchhike onto Y
Lack of recombination with the X chromosome
Y keeps accumulating deleterious mutations
Degeneration of the Y
X O sex determination (found in many insects)
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In summary think about sexual conflict in terms
of (1) Male-advantage alleles (i.e., bright
color) - are good when expressed in males
attract mates - are bad when expressed in
females attract predators resolution
confinement to Y chromosome (females are safe)
result eventual deterioration of the Y
(Mullers ratchet) (2) Sexually antagonistic
alleles (i.e., toxic seminal fluid) - help male
assert his reproductive agenda, to the detriment
of females he mates with
resolution females must constantly counter-adapt
(open-ended) result arms race, each sex
limiting the others adaptive evolution