Download Sexual selection

October 28, 2009
Bioe 109
Fall 2009
Lecture 15
Sexual selection
- what is sexual selection?
- Darwin defined sexual selection as:
the fitness advantage that some individuals have over others of the same sex solely with
respect to reproduction.
- Darwin viewed sexual selection as being quite distinct from natural selection.
- to him, natural selection favored variations among individuals based mainly on survivorship.
- characters such as the peacock’s tail posed a problem for Darwin’s theory because they
appeared to incur a cost to survival - surely a mutant peacock with a tail 1/10 the length would be
more efficient at escaping predators.
- Darwin came up with a solution to this problem by proposing that characters may evolve that
conferred a disadvantage to survivorship if they conferred an advantage in reproductive success.
- although Darwin made an important distinction between natural and sexual selection, there is
really little need for this.
- sexual selection simply addresses one fitness component: reproductive success.
- a character that increases reproductive success acts to increase overall fitness - even if it has a
detrimental effect on another fitness component such as survivorship.
Total Fitness = Viability + Fecundity + Longevity + Mating success
- Darwin recognized that “trade-offs” may occur between fitness components.
- thus, a trait increasing mating success may evolve even if it causes a reduction in viability as
long as there is an overall increase in fitness.
Why does sexual selection occur?
- because of an “asymmetry” of sex - i.e., sexual reproduction creates different selection
pressures for males and females.
- the basic argument is rather simple; in a large number of species, females invest more in their
offspring than do males.
- eggs are more costly to produce than sperm and the total reproductive output of females is
potentially much lower than males.
- since eggs (and pregnancies) are more expensive to produce than sperm, an important
difference emerges in what limits the lifetime reproductive success of a female versus a male.
females:
males:
limited by # of eggs and/or pregnancies
limited by # females mated
- in other words, we predict that access to females will be a limiting resource for males (usually)
but access to males will not be a limiting resource for females (usually).
- this sets up a conflict that is manifest as sexual selection.
- the difference between males and females leads, in very general terms, to two main
consequences:
1. males should be competitive - they should compete among themselves for access to females.
2. females should be choosy - since her investment is larger than males, she has more to lose by
making a bad decision.
- these are the two forms of sexual selection identified by Darwin: “male-male competition” and
“female choice”.
- male-male competition is also called “intrasexual selection” because selection occurs among
males.
- female choice is also called “intersexual selection” because selection involves an interaction
between males and females.
- this was first shown in a classic experiment by Bateman in 1948.
- Bateman carried out a very simple experiment to examine the reproductive success of male and
female Drosophila melanogaster.
- he placed 3 male and 3 female fruitflies in bottles and allowed them to mate.
- all flies used in these experiments carried unique sets of genetic markers.
- by examining the resulting progeny from these cultures, Bateman was able to see who mated
with whom and how many offspring each individual produced.
- a clear difference emerged between males and females.
- for males, reproductive success increased in direct proportion to the number of mates.
- for females, reproductive success did not increase with more than one mate.
- furthermore, variation in the number of mates among males was higher than seen among
females.
- some males had no mates (the biggest losers), the biggest winners were those that had 3.
- for females, the vast majority had one or two mates - none had 0 and virtually none had 3.
- sexual selection, variation in fitness due to variation in success at getting mates, was much
stronger in males than in females.
- similar results have been obtained in other species – like the rough-skinned newt example
described in the textbook.
- in situations where males are limiting resources to females (such as in pipefish), things are
reversed (as theory predicts).
- here, females are larger and more brightly colored than males (who have specialized brood
pouches they use to incubate eggs laid by females).
- females are aggressive and fight amongst themselves for access to males.
- in pipefish, females experience a wider variance in reproductive success than males and gain a
linear increase in fitness with an increasing number of mates.
Intrasexual selection
- intrasexual selection typically occurs in species where individual males can monopolize access
to females.
- this monopolization can take the form of some direct control of the females themselves or
through the control of some resource important to females.
- male-male competition can take on a number of distinct forms.
1. Combat
- outright combat is the most obvious form of male-male conflict.
- combat among males can lead to sexual dimorphism in size in which males are larger than
females
- it can also lead to the evolution of weaponry, such as horns in ungulates and beetles.
2. Sperm competition
- male-male competition does not stop when copulation is over.
- the true determinant of a male’s mating success is not whether he copulates, but whether his
sperm actually fertilize eggs.
- if a female mates with multiple males within a short period of time, there will be a race among
the males to successfully fertilize her eggs.
- females from a wide variety of many species are known to produce offspring that are sired by
more than one male.
- multiple paternity clearly sets the stage for sperm competition.
- what traits would be selected in sperm competition?
- one obvious one would be to simply increase the amount of ejaculate, thus increasing one
male’s chances of displacing sperm of other males.
- other less direct forms of sperm competition involve the transfer of compounds into the females
reproductive tract that modify her behavior.
- notable here are seminal fluid proteins.
- in species like Drosophila and other insects these proteins have been found to have a strong
influence on many important traits of females including longevity, egg-laying rate and re-mating
rate.
3. Infanticide
- in some species of mammals competition among males continues even beyond conception.
- one of the most striking examples of infanticide involves the African lion.
- the basic social unit of lions is called the pride.
- prides consist of a group of closely related females (mothers, daughters, sisters, nieces, etc.)
- the pride also consists of a small group of resident males - two or three is the usual number.
- the males are usually related to each other - we know this from DNA fingerprinting work - and
not related to the females.
- this situation arises because females reaching sexual maturity remain in the pride where they
were born whereas males disperse to other prides.
- males must fight and defeat the group of resident males in order to gain control of the pride.
- the average time that male lions maintain control of a pride is only about 2 years.
- because residence in the pride is the key to reproductive success of male lions, they quickly
begin trying to father cubs.
- one impediment to quick fatherhood is the presence of still-nursing cubs, because females do
not return to breeding condition until their cubs are weaned.
- how do male lions overcome this problem?
- they resort to the grisly task of killing any cubs in the pride that are not weaned.
- this is a highly successful strategy.
- it results in females returning to breeding condition an average of 8 months earlier than they
otherwise would.
- however, it has a heavy cost on the species.
- about 25% of all cub mortality in the first year is caused by infanticide and about 10% of
overall lion mortality.
4. Alternative male reproductive strategies.
- alternative male reproductive strategies are also very common.
- an excellent example is provided by the phenomenon of “jacking” in Pacific salmon.
- in some species (coho and sockeye), a proportion of males spend a small time at sea (6 months)
and mature at a very small size.
- they then attempt to “sneak” fertilizations from pairs of large, sea-run fish by rushing in and
releasing sperm at the appropriate time.
- these sneaky males may enjoy a substantial reproductive success.
- this strategy exhibits some degree of genetic control but also is influenced by environmental
factors (notably the hatchery environment which can generate a much higher proportion of jacks
than seen in nature).
Intersexual selection
- in species where males advertise for mates and females choose among them, inter-sexual
selection can lead to the evolution of elaborate coloration, exaggerated male secondary
characteristics and courtship behavior.
- male-male competition was traditionally believed to be the prevalent type of sexual selection.
- now, female choice is recognized as being equally important and there is much recent
experimental evidence to support it.
- however, a critical question needs to be answered:
Why should females have preferences for certain male characters?
- some types of female choice are easy to explain - for example, in many species of birds and
spiders the male will court the female by bringing her food items.
- in the common tern, females show a strong preference for males that bring a lot of food.
- the amount of food a male brings during courtship turns out to be strongly correlated with the
amount of food he brings to feed chicks.
- the female clearly has her reasons for selecting males with this character.
- this is an example of direct benefits.
- how about lekking species?
- leks are aggregations of males that gather in sites, defend small territories, and display for
females - e.g., grouse, ruffs, Jackson’s widowbird.
- in lekking species, a male’s only contribution is his sperm - how does female choice evolve
here?
- let us consider four models.
1. Runaway selection
- the first theoretical answer to the evolution of why females prefer certain types of males was
first developed by R.A. Fisher in a process he called “runaway selection”.
- in this process a genetic correlation develops between a male trait and female preference for
that trait.
- the simplest model assumes two genetic loci - one determining female preference (P locus) for
the exaggerated male trait and one controlling the male trait itself (T locus).
- let’s use the example of stalkeye flies in which females appear to mate with males having long
eyestalks.
- females having an allele (P1) that causes them to prefer males with long eyestalks will produce
sons possessing that trait (T1).
- these males will have an advantage over other males in the population because some females
prefer them.
- the sisters of these males with longer eyestalks will have a preference for this trait because their
mother did.
- the correlation will be strengthened by linkage disequilibrium between the two loci.
- now, consider a mutation that causes a slightly longer eyestalk (T2).
- because the female preference allele (P1) is tightly linked to this locus, preference for the
exaggerated character is automatic.
- each generation, males may develop slightly longer eyestalks (by the action of female choice)
but each generation females prefer longer eyestalks than their mothers did.
- this results in a positive feedback loop that can result in “runaway selection”.
- eventually the selection for even greater male traits will be opposed by natural selection when
the trait reduces male survivorship.
2. Good genes models
- the good genes hypothesis predicts that females choose males with certain traits because the
trait is an honest “indicator” of overall genetic quality.
- any male trait that is correlated with overall genetic quality is thus an indicator of “good genes”.
- the trait thus serves as a “guide” by which females choose mates.
- is there support for the good genes model?
- many studies have obtained support for the good genes model.
- one of the best examples is that described in the textbook involving gray tree frogs by Allison
Welch.
- in this species, males differ in the length of their mating calls and females appear to prefer
males with longer calls.
- the good genes hypothesis predicts that the progeny of longer-calling males should be
genetically superior to shorter-calling males.
- females are thus using the call length as an indicator trait and it behaves as an honest signal.
- Welch et al. (1998) did a nice experiment in which they fertilized the eggs of females with two
males - a “short caller” and a “long-caller”.
- having the same mother but different fathers, the progeny are half-sibs.
- the tadpoles were reared under two feeding regimens - low and high food.
- they then examined a number of fitness related traits including larval growth rates, time to
metamorphosis, mass at metamorphosis, larval survival, and juvenile growth.
- out of 18 individual comparisons, the progeny of short calling males never did better than long
callers.
- long callers did significantly better in 8 comparisons.
- the difference between males is statistically significant.
- thus, we can conclude that females are benefiting by choosing longer-calling males.
3. Sensory bias
- sensory bias models predict that female preference for certain male traits may evolve prior to
the appearance of the male trait itself.
- in other words, females have a pre-existing sensory bias for the trait.
- females will thus prefer males that happen by chance to produce that trait.
- under this model, the attraction that the female has for the male trait is an incidental by-product
of her sensory system.
- there is no direct selection on the female to be attracted to that male trait.
- evidence supporting the sensory bias model comes from phylogenetic studies.
- for example, in wolf spiders female preference for tufted forelimbs appears in a phylogeny of
the group prior to the appearance of the male trait itself.
- this suggests that the tufts evolved to take advantage of a pre-existing bias in female to prefer
males with these tufts.
- a number of additional studies have demonstrated pre-existing female preferences for male
traits that don’t yet exist.
- examples include, swordtails (the male sword), two species of grassfinches (crests of feathers
on the head), and tungara frogs (addition of chucks to mating calls).
- sensory bias models differ dramatically from “good genes” models because females are not
assumed to obtain any benefits whatsoever from the male trait.
- the male is modifying female behavior and stimulating her to mate but she gains no direct or
indirect benefit in choosing that male over any other.
4 Chase-away selection
- this model is based on the prediction that the optimal mating rate of males is not the same as
females.
- therefore, males are always attempting to stimulate females to mate at a level that benefits
themselves but not the female.
- this leads to an intraspecific Red Queen process.
- males evolve adaptations (i.e., ornaments, courtship displays) that enable them to mate females
at an elevated rate.
- females, in turn, evolve counter-adaptations that enable them to resist the male adaptation and
mate at more optimal levels.
- this leads to a perpetual cycle of adaptations and counter-adaptations involving a class of
“sexually-antagonistic genes”.
- evidence favoring the chase-away model has been obtained in Drosophila in which females
were prevented from “counter-adapting” to male-benefit genes.
- in about 32 generations, adaptations appeared in the males that allowed them to increase their
fitness at the expense of females.