lecture 10 - conflict between sexes - Cal State LA

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Transcript lecture 10 - conflict between sexes - Cal State LA

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
Sex chromosomes in humans
Each human genome consists of:
- 22 pairs of autosomes, or normal chromosomes
- one pair of sex chromosomes
male
female
XY
XX
Sex chromosomes in humans
male
female
XY
XX
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 don’t recombine for most of their length
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
- in other words, the Y chromosome is on its own
Sexually antagonistic genes
Many genes are expressed in both sexes, but some alleles benefit
males, while other alleles benefit females
Male guppies
Alleles producing bright
colors and big tails are
good for males: make them
attractive to females
Female guppy
The same alleles are bad
for females, who don’t need
help attracting mates; just
makes them more visible to
predators
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 dad’s good-for-boys, bad-for-girls alleles
Rice (1998) PNAS 95: 6217
Brooks (2000) Nature 406: 67
Fedorka + Mousseau (2002) Nature 429: 65
Sexually antagonistic genes
When male-benefit alleles are expressed in a male, they give
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
- colorful females get eaten, those with “plain” alleles survive
In this generation, selection favors female-advantage alleles -but these will then get passed on to sons…
- plain sons won’t attract mates, won’t reproduce
- rare colorful sons will reproduce, pass on colorful alleles
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
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
Hitchhiking the Y
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
Genes coding for 17 out of 18 male traits involved in mating
displays (color, tail, fins) are located on the Y-chromosome,
right next to the gene controlling male development
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 don’t need help mating)
termed sexually antagonistic alleles, since they help one
sex at the expense of the other sex
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 don’t recombine benefits
males
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
- endless cycle of adaptation and counter-adaptation
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
a
a
a
a
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
red
eyes
orange
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
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?
Sexually antagonistic genes are widespread
(Rice, 1992)
Prediction: alleles that benefit females but harm males will..
1) accumulate in females over time
2) be linked to the red-eye gene
Result: red-eye males had half the fitness of orange-eye males
The red-eye allele, by staying in females for 29 generations, had
“collected” many alleles of nearby genes that were:
- beneficial to females
- harmful when expressed in males
Proof that sexually-antagonistic alleles exist for many genes
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, but prevent females
from evolving counter-measures to male mating tactics
- in other words, artificially arrest female evolution;
see if males evolve ways to exploit females when
females cannot evolve protective responses
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?
Some male traits actively harm females
Results: male flies adapted to the female clone population
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 + dangerous for females
new male alleles lowered female fitness
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)
Male’s 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)
Chase-away selection
Drosophila seminal fluid contains 83 gene products
- thus a highly complex blend of chemical warfare agents is
used to push the male’s agenda
Some seminal fluid proteins are for competing with other males
- likely harm females as an indirect consequence
of male-male competition (intra-sexual selection)
Other proteins 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….
The Red Queen’s 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
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
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) promotes cell growth
IGF-II is switched off on maternal chromosome, but on the
paternal chromosome this gene is switched on
- daddy forces mommy 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
Chase-away selection: genomic imprinting
paternal
IGF mpr
maternal
igf MPR
- paternal imprinting:
accelerate fetal growth
- maternal imprinting:
slow fetal growth
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 female housed with three males (multiple mating
opportunities, as commonly occurs in nature)
Effects of monogamy after 34 generations
(1) females reproduced more, but also survived more
(2) males attempted fewer matings
Effects of monogamy after 47 generations
reproductive rate
- Monogamy increased the overall
reproductive rate for the
population
- Also increased the development
rate of offspring
development time of offspring
45
46
47
generation
Effects of monogamy
Monogamy constrains the reproductive success of both mates to
be identical
- neither sex can exploit the other when there’s 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
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 is thus 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) Muller’s ratchet: bad mutations pile up over time
(2) Background trapping of beneficial mutations
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
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
Brooks (2000) Nature 406: 67-70
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
Full circle: gain and loss of the Y
Y comes into
existence
(sex determined
by one gene)
Collects a bunch
of male-advantage
alleles
Trick females
into mating more
Harm females
by mating
Lack of recombination
with the X chromosome
Full circle: gain and loss of the Y
Y comes into
existence
(sex determined
by one gene)
Collects a bunch
of male-advantage
alleles
Mutations near the
male-advantage alleles
hitchhike onto Y
Y keeps accumulating
deleterious mutations
Lack of recombination
with the X chromosome