Download Sperm competition: a form of sexual selection

You always know who your mother is
• in some parts of Italy it is widely believed that a man must shoot a honey
buzzard every year if his wife is to remain faithful
• to fulfill this ritual many men usually leave their wife behind
• some times the wife encourages him to go
• for a male to leave his partner behind is risky business
• most times we implicitly assume all sperm come from the same man
• more frequently than we would like to think, this is probably wrong
• sperm from different males compete to fertilize the egg
• this idea forms the basis of sperm competition
• what are the consequences for the female within whom this competition
occurs?
• what are the consequences for the male that inseminates the female?
• sperm competition is widespread across the animal kingdom
• this concept has changed the way biologists view the world
Sperm competition: a form of sexual selection
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Sperm competition in ancient history - the Greeks
• before Christ was born, Aristotle and his predecessors knew about sperm
competition
• they saw that if a bitch copulated with two males during a single heat she could
produce pups in the litter fathered by each male
• the Greeks understood male anatomy very well because war provided lots of
male bodies for dissection, but dissection of women was forbidden
• Aristotle correctly illustrated the male uro-genital tract, but his knowledge of
female anatomy was abysmal.
• Aristotle was confused about menstruation - egg comes from mix of blood and
female semen, but 400 years later Galen (130-201 A.D.) proposed that
male and female semen coagulated to form an embryo (right!)
• Aristotle also saw that if a hen copulated with two cockerels of different types
the chicks usually resembled the second male that mated - combining
two modern ideas of genetic markers and last male sperm precedence
Aristotle was right about things he could see
Darwinian origins of sperm competition
• little else happened with sperm competition theory for about 2,000 years after
Aristotle died
• eggs and sperm were discovered as well as fusion to form embryos
• sperm competition resurfaces with Charles Darwin
• the problem:
problem: if natural selection favors those who leave lots of offspring, then
how could structures or behaviors that were obviously detrimental to
their bearers evolve by natural selection?
• the example:
example: gaudy plumage or songs of male birds that made them
conspicuous to predators
• Darwin’
Darwin’s grandfather (Erasmus) wrote about some attributes of males that
helped in fighting to obtain females
• Charles thought that maybe females were attracted to beauty and preferred
attractive males, but wasn’
wasn’t sure exactly why
• Darwin identified two forces at work: competition between males and selection
by females that he termed sexual selection
• although initially neglected, by 1930’
1930’s this concept was acknowledged on par with
natural selection as a great theory
Darwin advanced sperm competition with sexual selection
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Next: sperm competition meets parental investment
• Darwin assumed sperm competition only operated until an individual had
acquired a mate
• in late 1960s Bob Trivers asked what drives sexual selection and poses the
idea that the effort put into raising the offspring determines the intensity
of sexual selection
• Put another way: sexual selection operates most intensely upon the sex that
invests the least in rearing offspring
• most of the time this is the male - contributes sperm, doesn’
doesn’t carry fetus or
care for young after birth
The sex that invests the most (females) become
limiting for the one investing less (males), therefore
increasing sexual selection pressure on the males
Example of Trivers idea: the peacock
• male provides few million sperm
• female does everything else
• once inseminated, female is out of game
• male can inseminate again in minutes
• sexually active males ALWAYS
outnumber receptive females
• this leads to intense competition and
females can afford to be choosy
• upshot: all females get inseminates, but
reproductive success of males is
highly variable
The most aggressive or attractive peacock always
wins out, hence the peacock’
peacock’s strong sexual
dimorphism
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Trivers idea still works in role reversal: magpies and phalaropes
• magpie males have huge investment
• feed incubating female and young
• parental duties limit his ability to
inseminate other females
• net result: similar reproductive success
among all males and very little
sexual dimorphism - female and
male magpies look almost
identical (to us anyway)
• phalarope males incubate and care for
young
• females compete for males and males
choose
• female phalaropes are larger, more
aggressive, and more colorful
The level of investment by each sex determines the intensity of sexual selection
Trivers big idea was rooted in a little fruit fly (D.
(D. melanogaster)
melanogaster)
• Angus Bateman used genetic marker of
eye color to track reproductive
success of male and female flies
• he determined the mothers and fathers of
9,500 flies
• for a male, the more he copulated, the
better his reproductive success
• for a female, one copulation was enough,
so additional copulation did
nothing to increase her
reproductive success
• therefore males like to copulate as often
as possible, but from a
reproductive standpoint females
have nothing to gain
• forms the basis for big ideas about how
sexual selection works
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Trivers big idea lays the foundation for behavioral ecology
• Trivers championed Bateman’
Bateman’s studies and opened a new field
• also introduced the concept of ‘mixed reproductive strategy’
strategy’: males of
socially monogamous species (like birds) form a pair bond with one
female but never pass on the opportunity to copulate with another
female in order to further enhance reproductive success
• males reproductive success not limited by ability to produce sperm
• sperm are small and cheap to produce compared to eggs
• males seem to have an almost limitless supply
• therefore, sexual selection operates more intensely on males, right?
• problem:
problem: if numbers of males and females are about equal, then mow can
most males copulate with many females and each female copulate
only once?
• presumed answer (wrong):
(wrong): females simply acquiesced and put up with
repeated matings from other males (but their heart really wasn’
wasn’t in it)
In fact, females of many species are pretty interested in
copulating repeatedly in search of the perfect mate
The Father of Sperm Competition and the yellow dungfly
• Geoff Parker spent his graduate career looking
at cow pies in England
• he noticed intense competition for females by
the male flies
• as soon as a female lands she is grabbed by a
male who copulates, who is then ripped
off her by a larger male, who mates
again with her until another larger male
throws him off
• so females regularly copulate w/ several males
• maybe the sperm of the two males competes
after copulation in the female
• similar mating occurs in guppies
Sperm of different ejaculates
compete between males for
fertilization of female eggs
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Understanding the different meanings of sperm competition
• Darwin had thought about acquisition of partners
• Parker had thought about acquisition of fertilization by sperm
• Parker pointed out that acquiring a partner does no good if your sperm lose
out to someone else
• So sexual selection can continue right up to the point of fertilization
• if females copulate with multiple males, then sexual selection favors the
male who can fertilize the most eggs
• males could win by having faster swimming sperm or maybe sperm that
disabled competing sperm from another male
Studying how sperm win this
contest for fertilization is the
basis for the study of sperm
competition
Sexual Conflict: the true battle of the sexes
• Parker’
Parker’s idea was that selection picks out individuals rather than the
population or species as a whole
• same concept popularized by The Selfish Gene (Dawkins)
• far from being cooperative between the sexes, reproduction is a selfishly
motivated exercise
• each male and female out to maximize benefits and minimize costs
• sometimes interests coincide, but usually it’
it’s everyone out for themselves
• this conflict has been the driving force for many behavioral, physiological,
and anatomical aspects of reproduction
Males and females are out to
“screw” each other (literally) to
get the best genetic deal
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Intersexual and Intrasexual Conflict: male versus male versus female
• Parker was initially less concerned about the battle between the sexes
relative to the battle within one sex: males
• sperm competition generates opposing selection pressure on males:
• males who successfully fertilize females inseminated by other males win
• males who prevent females they have inseminated from being fertilized
by sperm from another male win
• fertilizing more females is great, but costs of being cuckolded are also great
• reproductive success of cuckolded male is depressed, and reduced even
further if the male spends time rearing offspring that are not his own
Pre and post-copulatory
sperm competion have
shaped the evolution of all
species including our own
Sperm competition: the evolutionary arms race
• selection pressure of sperm competition drives the evolution of traits that
promote male reproductive success
• a war of attack and counter-measures to nullify the advantage
• as soon as males evolve a characteristic, other males evolve to compensate
• example: a larger ejaculate by some males prompts counter-selection on
males to better protect their paternity (i.e. decrease female infidelity)
• next example: better paternity protection by some males prompts counter
selection on males to evolve ways to outsmart paternalistic males
and fertilize their mates
•
Sound familiar?
“Running as fast as you can to
stay in the same place”
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Love on the rocks: the complicated sex life of barnacles
• Darwin dissected barnacles for eight
tedious years
• found not all barnacles were
hemaphrodites,
hemaphrodites, some had
separate sexes
• in many species the males were minute
with several living parasitically
inside the female
• Darwin found 14 in one female!
• Darwin described them as mere bags of spermatozoa
• it seemed just one male could easily fertilize all the female’
female’s eggs
Intense sperm competition occurring
inside the female barnacle
Why didn’
didn’t Darwin pursue the idea of sperm competition?
• maybe he never made the connection - unlikely
• illegitimate fertilization in plants was pretty clear
• his poems on plant reproduction were considered thinly veiled erotica
• Victorian prudery was well establish - taboo subjects and sexual repression
• He wrote enthusiastically about the penis of one species being “wonderfully
developed”
developed”, lying “coiled up, like a great worm”
worm” and “when fully
extended, it must equal between eight to nine times the length of the
animal.”
animal.”
• his wife Emma and daughter Henrietta acted as censors. Henrietta was
described as both closeted Victorian matriarch and fussy moralist
• Darwin’
Darwin’s grandfather was very enthusiastic about sex
and prescribed it to his patients as a cure for
hypochondria. Since Henrietta was also a
hypochondriac, maybe she should have taken
her grandfather’
grandfather’s suggested treatment
Bad timing for sperm competition
in the Victorian era
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Changing the androcentric view of reproduction
• battle between the sexes had been seen as very asymmetric
• active males versus passive females
• females were thought to only chose from different partners
• until recently, a mixture of unconscious sexism and biological ignorance
perpetuated the idea that sexual selection was male-dominated
• a male who copulates with multiple females increases offspring
• a female is unlikely to increase number, but maybe increase quality
• if evolution is a game of numbers, then quantity is more important than quality
• therefore, the belief persists that sexual selection operates more on males
• the argument for multiple female mating was acquiescence, maybe because
initial sperm competition studies were on insects (hard to know their
motivation)
• research in 1980s on birds showed that far from passive, females often
actively sought multiple male partners
• sperm choice by the female was a new idea of post-copulatory selection
Females mate often and exercise mechanisms
of sperm choice in reproduction
Changing the androcentric view of reproduction (part 2)
• if females could choose between different sperm, there is sexual conflict
• when one sex evolves a method to constrain the reproductive success of the
other, selection immediately favors counter adaptation to negate the
advantage
• example: males evolve a longer penis, females evolve longer uterus
• escalating race of adaptation and counter-adaptation
• sperm competition was viewed with anger by the feminists in 1980s
“A woman without a man is like a fish without
a bicycle”
bicycle”
Gloria Steinem
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Turning the focus upon humans: sperm competition
• Robin Baker and Mark Bellis combined infidelity and evolutionary theory
• research on extra-marital sex, used undergraduate students to gather data
• reported that their nationwide survey revealed high levels of polyandry
• also suggested the idea of “killer sperm”
sperm” battling in female reproductive tract
• also suggested females use orgasm as a selection method to control sperm
uptake and paternity of offspring
• claimed a correlation between testis size and success in sperm competition
• measured testes of 14 colleagues
• took photos and asked women to rate the men on the likelihood they
would engage in extra-pair copulation if given the chance
• Baker reported his prediction was absolutely correct - significant correlation
• sloppy science with poor experimental design: relationship of height, race and
other could easily account for the positive correlation
• then the ideas of “killer”
killer” and “kamikaze”
kamikaze” sperm, with blockers, egg getters,
and all the rest began to unravel
Almost impossible to perform controlled
studies on humans
So what can we learn about and from sperm competition?
1.
2.
Why should an individual copulate with more than one partner?
If a female copulates with more than one male, then how’
how’s the father
chosen? What determines which male fertilizes her eggs?
3. How do sexual conflicts arising from sperm choice and sperm competition
get resolved (antagonistic co-evolution)?
•
Why questions: Why do males inseminate with a particular number of sperm? Why do some males
remain particularly close to females before and after copulating? Why do females of some species initiate
copulations with so many males? Why do females seek extra-pair copulations?
•
How questions: How do physiological processes including sperm choice transform copulations into
offspring? How do the sperm of different males interact in the reproductive tract? How important are sperm
choice and sperm competition in determing which male fertilizes the egg?
Sexual conflict challenges longcherished assumptions about male
and female roles in sex
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