I. Gene-frequency dynamics
II. Muller's and Rice's Ratchets
III. Population Dynamics
IV. The ecology and evolution of virulence
The question of 'why have sex' is amazingly one of the last unsolved problems of evolutionary biology (Maynard Smith 1982). Sex is so basic to life that it seems curious to question its existence. Most species of animals are dioeceous which literally translates into 'live in two houses' -- namely male and female. Many male and female behaviors revolve around the act of sex so it seems appropriate to get down to the root of the issue: why have sex? It is easier to think of the paradox of sex if we rephrase the question slightly and ask 'why have two sexes?' or let's get down to brass tacks and ask the question 'why bother producing males?'
Let's get outside of the realm of the esoteric theoretical issues of sex and think of a concrete example. Cnemidorphorus or whiptail lizards are common throughout western North America. Nearly all species of Cnemidophorus are sexual with males and females that produce male and female progeny. However, one "species" called Cnemidophorus uniparens, as its Linnean binomial implies, is uniparental; it has one-sexed parents. No males are required (Crews et al. 1983). The species manages to propagate itself quite well without any males whatsoever.
Let's think of the advantages of an asexual existence which highlights the disadvantage of males. Consider two females, one sexual the other asexual. Asexuals and sexuals produce an equal number of offspring. The sexual species must search out a mate, then copulate, then produce sons and daughters that go through the whole routine in the next generation. Asexuals produce only daughters. The sexual produces half the number of daughters because it must 'squander' half of its resources on the production of sons. Only daughters produce offspring -- males fertilize. The cost of sex is reflected in a decreased rate of population growth rate in a sexual population compared to the two-fold faster growth rate of an asexual population. In the next generation, sexual daughters are likewise disadvantaged in the reproduction game and contribute only half the number of females to the ecosystem compared to an asexual species. Get the picture? asexual whiptail lizards could potential have two times the reproductive rate of its closely related sexual species. Such facts have lead us to question the very existence of sex because the planet earth should be populated with only asexual species given they reproduce with much greater efficiency.
To make matters worse for the male cause, asexual female whiptail lizards routinely pseudocopulate one another in laboratory colonies and in nature (Crews and Young 1991). During pseudocopulation one female engages the partner in the role of male (she's on top) while the other female plays the female (bottom). Of course, it is not possible for sperm to be transferred (no testicles are present), yet the female that is copulated in such a fashion produces a larger clutch than a comparable asexual female that does not receive this kind of 'isosexual' mounting. Males are not even required for the act of sex in this species and yet it seems that pseudocopulation stimulates and enhances reproductive output of asexual species.
The pseudocopulatory behaviors of asexual whiptail lizards has a proximate basis in the cycle of reproductive hormones. When any female vertebrate produces eggs, the eggs on the ovary produce the hormone estrogen, which is responsible for triggering the female behaviors that make her receptive to copulation (usually by males). When a female ovulates eggs, the copora lutea or scars from the developing eggs are left behind on the ovary. The copora lutea begin producing the hormone progesterone. In unisexual whiptail lizards, progesterone has been clearly linked to the expression of male-like behaviors like mounting. In fact, progesterone is often metabolized into the hormone testosterone in many vertebrates. The first asexual female has developing eggs and is 'receptive' to copulation because she has high levels of estrogen. The second male-like female that pseudocopulates the first female is exactly one-half cycle out of phase with her partner. The second female possesses corpora lutea and she has high levels of progesterone. The pseudocopulation by the second apparently stimulates the first female causing her to retain more eggs on the developing ovary, thereby increasing clutch size.
Certainly not all asexual species retain sexual behavior. If there is no benefit to sexual behavior among the female asexuals then it should slowly decay as mutations that control such behavior build up in the genes. This process has been verified in Drosophila that have been engineered to be asexual (Takenaka-Decanay and Carson 1991). In most asexuals, sexual behaviors no longer serve a function and mutations are not selected against. Slowly, over the course of several generations, sexual behavior will gradually fade as deleterious mutations build. In contrast, asexual pseudocopulation in lizards increases clutch size so an asexual that retains sexual behaviors might have higher fitness than one that does not.
Given the two-fold advantage of sex, and the lack of a need for males during the act anyway, why bother producing males lizards? The same reasoning that applies to sexual and asexual Cnemidophorus lizards applies to all animals. With impeccable logic, I have justified male utility out of existence. My wife, reading this over my shoulder, snickers in the background, goading me on to erase all advantage of males. If males are useless then why am I here? If males are useless then why do most animals produce by sexual reproduction?
If Cnemidophorus uniparens has such a tremendous advantage over the co-occurring sexual species, then why hasn't the asexual species outcompeted the sexual species? It is thought that C. uniparens has been derived relatively recently. This may be true for many asexual species. They are continually spawned from sexual species, but in the long run most species remain sexual. Thus, somehow the short-term two-fold evolutionary advantage enjoyed by asexuals is surmounted by some advantage to sexual reproduction.
The main advantage of sexual reproduction is that it creates tremendous variation within a species. The union of two distinctly different genomes can produce nearly unlimited variability. Recent work comparing sexual and asexual species suggest that asexual lineages have far higher rates of parasitism than closely related sexual lineages (Lively 1996). Parasites are continually evolving new resistance genes that allow them to break down the defenses of their hosts. The hosts are likewise evolving new defensive systems that allow them to attack their rapidly evolving parasites. Without new genetic variation and lots of it, an asexual organism really has no where to run and nowhere to hide from the attack of parasites. Asexuals are genetically uniform, and a parasite can eventually evolve a resistance gene that allows it specifically target one asexual lineage of clones. Given that the asexuals become quite common owing to the two-fold advantage, the parasite does quite well by zeroing in on the now quite common clone. The asexual gradually fades to low frequency. Sexual organisms win in the long run by having the ability to evolve parasite resistance. Meanwhile, yet another asexual arises to take the place of the first, having been spawned off as a new asexual mutation from its sexual parental species.
Another advantage to sexual reproduction is that it allows deleterious mutations to be purged from the genome. A substantial fraction of sexual offspring die every generation. Many of those deaths are directly related to genetic lesions or mutations that have recently and spontaneously shown up in a species. While sexuals lineages have deleterious mutations purged each generation, an asexual lineage is not so fortunate. If a mutation arises in a clone, all daughters will inherit the genetic lesion from that point on. In any given population of asexuals, some possess many mutations while others possess few. Mutations cut into the reproductive rate of an asexual, particularly if progeny die because of mutations that disrupt early development. In any population of asexuals there will be the lucky "least-loaded clone", a clone that carries the fewest deleterious mutations. The mutational load of an asexual lineage cannot decrease below that in the least-loaded clones, but the load of mutations can increase in all clones as they acquire new mutations.
Muller, a nobel prize winning geneticist, came up the following argument regarding clones (Muller 1932). The first premise of his argument is that all clones will eventually accumulate mutations. The second premise is that most mutations are deleterious and only a few, perhaps only one in a few thousand, are beneficial. Muller's ratchet clicks with each new mutation, and with each click of the ratchet the overall fitness of the asexual lineage declines ever so slightly. To be sure, this leads to an advantage in the least-loaded clone, but eventually that lineage will accumulate mutations or be wiped out by some unforeseen disaster. A full click of Muller's ratchet occurs when the least loaded clone is removed by chance death of some natural disaster, or when the least-loaded clone accumulates yet another mutation.
Figure 9.3 Given enough time, Muller's ratchet will eliminate the least loaded clone. When this happens, the ratchet clicks once, and the asexual species becomes slightly more disadvantaged by the total load of deleterious mutations that it harbors (in preparation).
Sex has evolved as a way to create diversity. Through the process of recombination, existing variation is scrambled between alleles that come in from male and female parents. In addition, sex generates the raw material that natural selection can act upon, leading to steady "improvements" in the species. Male's thus play an important and equal role with females in generating genetic variation, the raw material for evolutionary change. As we will see in chapter 10, a female's choice of mate may depend on more fine-scale perceptions of his genetic quality and perhaps ability to resist parasites.
If two "sexes" are required for production of offspring, why does one sex produce macrogametes or large eggs, while the other produces microgametes or small sperm? Why don't the two sexes share equally by creating gametes of the same size that fuse to produce a big embryo? It seems as if males are cheating in that they produce a small wad of millions of tiny sperm relative to the enormous investment that females make in a few large eggs.
We can think of this problem in terms of yet another cost of sex, that of ensuring that each gamete successfully fuses with one other gamete. The whole point of sex is mating with someone else to create variation, so you definitely do not want your gametes to fertilize with your own gametes. The challenge then is bringing together one large gamete from a partner with your own large gametes. If gametes were equal in size, many gametes would not necessarily find a partner in fusion simply because of the limitations of search area (the gametes must search over a wide area), and the limitations of time (the gametes might exhaust or run out of reserves before fusion).
Figure 9.4. Drawing of illustrating how a microgamete can invade a population of individuals that only produce large medium-sized eggs.
Even in a pretty darn good mixture of gamete from the first parent and gamete from the second, it is tough to get each and every gamete to find a gamete from the other parental mating type. Some gametes go to waste unable to find a union. If all gametes are the same large size there would be considerable fitness loss for both parents. However, if one sex produced a few large macrogametes (what we call eggs), while the other sex produced a large number of small microgametes (what we call sperm), nearly all of the macrogametes would find a fusion partner (Parker 1982). Many of the microgametes would go to waste, but since they are so small and cheap to build it is inconsequential. While this waste of gametes is a 'cost of sex', the waste is minimized because one sex specializes in delivering a nucleus (valuable genetic variation) while the other sex specializes in delivery of nutrition to the newly fused the zygote.
In nearly all of the examples described below, it is invariably the case that more than one male participates in the fertilizing of a single female's brood, or clutch. In these cases, the males engage in sperm competition where depositing sperm is only the first step in successfully siring progeny. The sperm a male delivers to a female can be thought of as an independent stage in the life cycle of the male. Whereas sperm do not feed, they are mobile, particularly in animals with external fertilization (e.g., salmon). Even if fertilization is internal (e.g., lizards), the sperm must swim to fertilize the ova of the female. Males are strongly selected at two phases of the life cycle. The body of the male (soma) is selected for alternative behaviors that enhance the delivery of sperm to the female's eggs. Once there, the sperm (germ line) ejaculated by males is strongly selected for competing against the sperm delivered by a rival to the same female. It is a race of sorts, may the best sperm win. This is the essence of sperm competition. If two males fertilize the same females eggs, there is sperm competition.
1. Parasites and Genetic Diversity
Question: Why are there males, or why have sex?
3 Ecological hypotheses arise from the abiotic and biotic env.
Physical Environment
-> Temporal variation: Env. change hypothesis sex to anticipate unpred. changes to physical environment (no supporting evidence)
-> Spatial Variation: Competition Hypothesis (interacts with biotic)
sex to produce RARE offspring that can utilize rare resouces (no supporting
evidence)
Biotic Environment
-> Intraspecific Competition: Competition Hypothesis (ditto)
-> Parasites: Parasite Hypothesis Sex to produce the rare offspring
which can better escape infection.
The Parasite Hypothesis in more detail
Lock and Key model:
A susceptible to a (resistant to b)
B susceptible to b (resistant to c)
Assume a parasite gene a infects host genotype A
note the time-lagged advantage to being rare for A
This time lag is expected to lead to oscillations in the frequency of host and parasite alleles.
A dynamic cycle arises in which the Red Queen Rules
Support for the Parasite Hypothesis
Asexuals rule without parasites, but sexuals rule in env. with parasites.
But do parasites disproportionately infect the most common types
in mixed populations, yes parasites are more common in common clones
compared to outcrossed fish!
Cool control: inbred (sexual) fish vs clones, inbred fish get hammered
2. Conservation and Parasites
Endangered top minnow in Arizona
inbred lines re-introduced to desert streams did not survive, Why? Parasites?
Rice crops:
Biological Control:
Parasites have been effective in eliminating 75% of asexual weeds but on 33% or sexual weeds.
Muller's Ratchet
All clones accumulate mutations
"The mutational load in an asexual lineage cannot decrease below that in the least-loaded clones, but the load can increase in all clones." -- Price the ratchet clicks with each new mutation
Sex can readily purge mutations through recombination.
Rice's Ratchet
sex produces the rare progeny not at all like the parents and thus parasites can't infect
asexuals produce identical progeny which are highly susceptible to infection.
1. The spread of disease/parasite usually depends on host density -- or more precisely, the density of susceptible genotypes!
For example the rate of advance of fungal pathogen in plants is inversely proportional to plant spacing (Fig)
Consider the agricultural situation -- A seas of plants, all close together, genetically uniform
Disaster seems predictable.
2. Populations may cycle on theoretical grounds due to density-dependent transmission.
When the host is at high density transmission rates are high, thus a population is highly infected just after it starts crashing!
Evidence from Soay Sheep in the Hebrides
Curt Lively's snails
Cycles are obvious in many systems.
Consider indirectly transmitted parasites (e.g., Myxoma virus through mosquito)
Australia (no bunnies pre 1859):
What happened? Two possibilities:
The coevolution of parasites and hosts
- tight step-for-step coevolution has been well documented between parasites and their hosts.
- one of the features of parasites that can be monitored is their virulence.
- a highly virulent parasite is one that kills its host quickly.
- a reduced virulence means that the parasite doesn't reduce its host's fitness to the same extent.
- a classic example of the evolution of parasitic virulence involves the myxoma virus in populations of Australian rabbits.
- the myxoma virus causes the disease known as myxomatosis.
- the rabbits were introduced to Australia from Europe and have thrived to say the least.
- they are considered a major pest.
- in the 1950's the myxoma virus was deliberately introduced to Australia in an attempt to control the rabbit populations.
- initially it was a huge success.
- the virus was transmitted from rabbit to rabbit by means of mosquitoes.
- because of the large population of biting insects down unde, the disease spread quickly.
- myxomatosis intially decimated the standing populations - reducing them by 99% in some regions.
- the virus was extremely virulent when introduced into Australia.
- in fact, it killed 100% of its hosts.
- it wasn't too long, however, before its level of virulence began declining.
- there were two factors involved in this response.
- first, the virulence of the virus itself declined - this was demonstrated by infecting lab strains of rabbits with the virus sampled from natural populations over a number of years.
- interestingly, the same virus was introduced into France in 1952 and surreptitiously into Britain in 1953.
- in both of these countries, the virus also declined quickly in virulence
Virulence grade
high low
I II IIIa IIIb IV V
Australia
1950 100 0 0 0 0 0
1964 0 0.3 26 34 31.3 8.3
France
1952 100 0 0 0 0 0
1968 2 4.1 14.4 20.7 58.8 4.3
Britain
1953 100 0 0 0 0 0
1980 0 30.4 56.5 8.7 4.3 0
- in Australia, the rabbits themselves also began evolving resistance to the disease.
- this process was demonstrated by challenging wild rabbits captured over successive years with standard strains of the virus in the lab.
Percent mortality
Mallee pop. Gippsland pop.
1961-1966 68 94
1967-1971 67 90
1972-1975 66 85
- this example shows that both parasitic virulence and host resistance can evolve.
- natural selection will always favor increased resistance in hosts - this is the only possible outcome.
- how will selection operate on virulence in parasites?
Don't get the wrong idea: Parasites won't always evolve to be less virulent.
In fact parasites should evolve to maximize their own transmission, independent
of their effect on hosts
Consider the sheep liver fluke
sheep with worm, worm -> lays eggs
larvae attacks snail which make a mucus ball of cercariae
mucus ball eaten by ant
one larva attacks ant brain, causing it to climb up on grass stalk and stay there
Infected ant EATEN by SHEEP