Transcript Slide 1

Topic 17. Lecture 26. Evolution of Populations and
Ecosystems-I
Last time, we considered whatever little is understood
regarding Macroevolution at the functional level of
molecules, cells, and multicellular organisms.
Now we are moving at the upper levels of populations and
ecosystems. At these levels, organisms are treated as
individuals, ignoring their internal complexity and taking
into account only their external features that characterize
them as members of populations.
Naturally, the key problems of evolution cannot be
addressed in this way - we will not attempt to understand
complex adaptations by considering individuals. Still,
many important and fascinating issues can be studied at
the level of populations, including evolution of sex, aging ,
and interactive behavior.
Organism
Individual
Within its domain of applicability, treating organisms as
individuals, and considering only simple external
phenotypes, is a very productive approach to
Macroevolution.
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What questions can be addressed by considering Macroevolution of simple phenotypes?
Independently evolving individuals:
1. Phenotypic plasticity
2. Non-interactive behavior
3. Semelparity and iteroparity
4. Clutch size
5. Dormancy
6. Aging
Gene transmission:
1. Mutation
2. Maintenance of sex
3. Crossing-over
4. Systems of mating
5. Origin of sex
6. Outcomes of genetic conflicts
Interactions between individuals:
1. Warning coloration
2. Dispersal
3. Aggression
4. Cooperation and altruism
Complex population-level phenomena:
1. Multicellularity and coloniality
2. Anisogamy and sex allocation
3. Mate choice
4. Female preferences and male displays
5. Conflicts between gametes and sexes
6. Conflicts between relatives
7. Eusociality
For some of these questions, surprisingly definite answers have been obtained. For other
questions, there are no definite answers yet, but, at least, we know how to look for them.
Independently evolving individuals: 1) phenotypic plasticity
Obviously, an individual can increase its fitness
by developing the phenotype that suits its
particular environment. The ability to do this is
called phenotypic plasticity.
The norm of reaction of a genotype refers to the
set of phenotypes that can be produces by this
genotype under all feasible environments.
Some forms of phenotypic plasticity may be just
imposed by physical laws, and not evolved - think
of low fecundity under starvation.
When exposed to predators, a growing
Daphnia develops "horns" (left) that offer
it some protection.
The tadpoles of Pacific treefrog Pseudacris regilla develop different shapes in different
environments. In the presence of predatory insects, tadpoles develop deep tails and bodies,
while in the presence of predatory fish, tadpoles develop shallow tails and bodies.
Plants also often develop very different phenotypes under different environments, even
when they are genetically identical, as these two plants are.
Independently evolving individuals: 2) non-interactive behavior
Let us consider just one aspect of non-interactive behavior, foraging. If the environment
consists of "patches", foraging involves two decisions. The first is whether to enter a patch
in search of food, and the second is to judge how long to continue searching for food in that
location. The predator attempts to maximize
E/(H+S),
where E is the energy obtained from prey, S is the search time involved, and H is handling
time that includes capture, killing, eating and digesting. For a range of prey, the predators
average intake rate is
Eaverage/(Haverage+Saverage).
When the predator has found a new item, it has two choices. It can eat the new item, in
which case the profitability is Enew/Hnew, or it can leave it and search for an item already in its
diet, in which case the expected profitability is Eaverage/(Haverage+Saverage).
The predator should eat this new item if
Enew/Hnew ≥ Eaverage/(Haverage+Saverage).
This simple analysis leads to several predictions:
1) Predators with long Haverage and short Saverage should be specialists. Lions have a very low
Saverage but a high Haverage, which can be prohibitively large for some prey individuals.
2) Predators with short Haverage and long Saverage should be generalists and consume a wide
range of items.
3) Only predators with both Haverage and Saverage being short can afford using small prey with
low Eaverage. An extreme case of such evolution is provided by star-nosed moles.
Unusual anatomical and behavioral specializations of star-nosed moles resulted from
selection for speed, allowing the progressive addition of small prey to their diet.
Obviously, this analysis assumes that evolution can produce optimality, which may be
justified because the phase space is simple in this case. Of course, there are trade-off's
between E, H, and S - it is impossible to handle a moose in 120ms.
Independently evolving individuals: 3) semelparity and iteroparity
Many organisms are iteroparous, i. e. can reproduce repeatedly, often in the course of many
years. However, some organisms are semelparous (monocarpic), and reproduce only once
and then die. A three examples of semelparous species:
Agava
Echium
Semelparity is taxonomically and ecologically widespread.
Salmon
How can semelparity evolve? Why death after reproduction is often favored by selection?
Semelparous plants have a higher reproductive output per
episode than iteroparous species. An organism that puts all
available resources into reproduction will have a higher
reproductive output than an organism that withholds some
resources for future growth and survival.
For example, if a 10% increase in reproductive effort results in
more than a 10% increase in reproductive success, then this
increase will be favored by selection. If this differential holds
over all levels of reproduction, natural selection favors putting
all resources into reproduction, i. e. semelparity.
Again, we ignore internal functioning of the organism, and
simply consider different dependencies of R. S. on R. E.
Independently evolving individuals: 4) clutch size
Parents can be expected to produce clutches of the size that maximizes their fitness (the
number of surviving young) - and not the fitness of each individual offspring. Moreover,
parents can also trade current against future reproduction, and the optimal clutch size is the
one which maximizes lifetime reproductive success.
Highly fecund organisms sacrifice offspring size and viability for their increased numbers.
Relation between egg size and relative recapture rate (scaled to a maximum of 1) of juvenile
Atlantic salmon. Dashed lines represent the derivative of the function relating maternal
reproductive success to egg size.
Independently evolving individuals: 5) dormancy
Many species produce eggs or seeds that refrain from hatching despite developmental
preparedness and favorable environmental conditions. Instead, these propagules hatch in
intervals over long periods, although their viability declines with age. Such variable hatch
tactics represents bet-hedging, by maternal individuals, against future catastrophes and
evolve due to individual selection.
Germination and emergence are
stimulated by environmental cues, but
strongly influenced by maternal
controls.
Independently evolving individuals: 6) aging
Aging (senescence) is a decline in performance and fitness with advancing age. The rate of
aging is not prescribed by hard laws of physics, and "why individuals age at a particular
rate?" is a perfectly legitimate evolutionary question.
Should selection be opposed to aging and favor immortality? Not necessarily: there is no
selection in favor of high performance of an organism at ages that are never reached in
nature .
However, this is not the whole story. There are two possible, fundamentally different,
mechanisms of evolution of aging when potential fitness gain from old individuals is low:
1) Simple neglect: late performance deteriorates without any associated improvements, due
to accumulation of age-specific deleterious mutations that affect only old individuals (MA =
mutation accumulation).
2) Tradeoff: deterioration of late performance increases early performance, if the amount of
resources allocated on maintenance decreases, more can be allocated on reproduction (AP
= antagonistic pleiotropy).
In other words: is aging a part of the optimal life history, due to hard constraint that
prevents evolution from improving early and late performance of the same individual?
Suppose that we did all what is possible to postpone aging without compromising early
performance - by how much aging will be postponed? Extreme answers are:
1) indefinitely (MA)
and
2) not at all (AP)
but the truth is probably somewhere in between (J. Evol. Biol. 20, 433-447, 2007).
Antagonistic pleiotropy is supported by data from artificial selection experiments and from
analysis of longevity-enhancing mutations in D. melanogaster. The artificial selection
experiments used selective breeding from old individuals.
In one of these experiments, the mean
longevity of females increased by
25% after 15 generations, but the
early-life fecundity was depressed.
Discovery of single-gene mutations
that confer extended longevity also
provide support for the AP model.
B - control population,
O - population selected for reproduction at old age.
The MA also received some experimental support. A unique prediction of this model is that
MA should lead to age-related increases in inbreeding depression and in the genetic
variance of fitness components.
Age-specific estimates of additive genetic
variance in fitness, with standard error bars.
Perhaps, both AP and MA
mechanisms are important for
the evolution of aging, but
more data is needed (TREE 8,
458-463 AUG 2006).
Gene transmission: 1) mutation
Does mutation occur "out of necessity" or deliberately? A thought experiment: if there were
no cost of DNA handling fidelity, would evolution lead to zero or to non-zero mutation rates?
In other words, are the natural mutation rates minimal feasible or optimal? We do not know
the answer.
One the one hand, most of non-neutral mutations are deleterious, so that reduction of the
mutation rate can be favored by selection. On the other hand, occasional beneficial
mutations are very important, and are necessary for evolution.
If natural mutation rates are the minimal ones that are not yet involved with prohibitive cost,
evolution occurs only because laws of physics prevent evolution of zero mutation rate which would stop all future evolution.
Gene transmission: 2) maintenance of sex
“We do not even in the least know the final cause of sexuality; why new beings should be
produced by the union of the two sexual elements, instead of by a process of
parthenogenesis?" (Darwin, 1861). Sexual forms are often capable of asex (apomixis,
parthenogenesis): facultative asex is quite common. In particular, many forms
independently evolved "cyclical asex":
A sample of cyclical asexuals: a monogonont rotifer, an aphid, and a cladoceran.
However, sex is only rarely lost completely, and when it happens, obligate asexuals are
usually evolutionarily young. We known just two examples of "ancient asexual scandals":
Bdelloid rotifer
Darwinulid ostracod
So, what prevents, in almost all cases, the complete loss of sex? Asex is much more
efficient as a means of self-propagation. Moreover, in the case of 50:50 resource allocation
between males and females, asex confers a two-fold advantage.
A rare clone of asexual females will DOUBLE its frequency every generation. Clearly, sex
must confer a large, short-term advantage.
Sex apparently does not confer any immediate physiological benefits.
Thus, sex can only be advantageous due to genetic changes it causes in the offspring.
However, sex does not "improve" genotypes directly - it does not change allele frequencies.
Thus, sex could only confer an indirect advantage, by increasing genetic variation and thus
making selection more efficient.
However, for this mechanism to work, two conditions must be met:
1) some factor(s) must create non-random associations between distributions of alleles at
different loci - sex can only randomize genotypes and, without such associations, it would
have no impact.
[AB] = [A]x[B]; [Ab] = [A]x[b]; [aB] = [a]x[B]; [ab] = [a]x[b]; dAB = 0; sex does nothing!
2) some factor(s) must make sure that overrepresented genotypes have LOW fitnesses otherwise, reshuffling these genotypes by sex could only be deleterious.
If [AB] > [A]x[B], sex could be advantageous only if w AB if low!
There are two feasible reasons why each of these two conditions could be met. Thus, we
arrive to a general 2x2 classification of hypotheses on the maintenance of sex:
What makes distributions of alleles
at different loci non-independent:
genetic drift
selection
What makes overrepresented
genotypes maladapted: changing environment
(positive selection)
deleterious mutations
(negative selection)
ES
MS
ED
MD
ES = environmental stochastic,
ED = environmental deterministic,
MS = mutational stochastic,
MD = mutational deterministic.
There are some hypotheses that do not fit into this classification, but they appear to be
unlikely. Thus, let us consider the four classes of hypotheses: ES, ED, MS, and MD.
ES (environmental stochastic, or Fisher-Muller) hypothesis. Sex is beneficial because it can
bring together beneficial mutations that appeared in different genotypes.
This mechanism could only work if many positive selection-driven allele replacements occur
at the same time. Apparently, this is not the case.
The same is probably true for a variety of the ED (environmental deterministic) hypotheses selection can hardly fluctuate in the way that could make sex advantageous.
Thus, let us consider a variety of stochastic hypotheses that involve deleterious mutations
(some of them also involve beneficial mutations). We already encountered them.
(a) Accumulation of weakly deleterious mutations by background selection. In a large, nonrecombining population at mutation-selection balance, only Y chromosomes free of strongly
deleterious mutations will contribute to the ancestry of future generations. The effective
population size (Ne) of the Y can therefore be greatly reduced. This reduces efficiency of
selection and increases the rate of fixation of weakly deleterious mutations.
(b) Muller's ratchet. This process involves the stochastic loss of all Y chromosomes carrying
the fewest number of deleterious mutations from a finite population. In the absence of
recombination and back mutation, this class of chromosomes cannot be restored. The next
best class then replaces it (i. e. the class of chromosomes with the next fewest number of
deleterious mutations). This class can in turn be lost, in a succession of irreversible steps.
Each such loss is quickly followed by the fixation of a deleterious mutation on the Y.
(c) Genetic hitchhiking by favorable mutations. The spread of a favorable mutation on a nonrecombining Y-chromosome will drag to fixation any deleterious mutation initially
associated with it. Thus, hitchhiking requires that selection coefficients for beneficial
mutations are larger than for deleterious alleles. Successive adaptive substitutions on an
evolving Y chromosome can lead to the fixation of deleterious mutations at many loci.
(d) Lack of adaptation on the non-recombining Y chromosome. The rate of adaptation on a
non-recombining chromosome can be greatly reduced, owing to interference of positive
mutations with linked deleterious alleles. If selection coefficients for beneficial mutations
are of the same magnitude or smaller than those for deleterious mutations, only beneficial
mutations on Y-chromosomes free of deleterious alleles can contribute to adaptation.
Evolutionary advantage of sex can be due to the same factors that cause degeneration of
non-recombining sex chromosomes. However, all these mechanisms are long-term: loss of
sex can be penalized only after a long delay. This appears to be a fatal flaw.
MD (mutational deterministic) hypothesis. Sex is beneficial because it increases variance of
the number of deleterious mutations in genotypes, making narrowing negative selection
against them more efficient.
The most efficient forms of selection, truncation and truncation-like, are narrowing and,
thus, undermine their own efficiency. Sex can restore it, by randomizing the distribution of
deleterious alleles within the population, and greatly diminish the mutation load.
This mechanism can work under two conditions:
1) U > 1, as otherwise L is low even without sex. Recent data indicate that U > 1.
2) Narrowing selection (truncation-like selection, selection with synergistic epistasis)
against deleterious mutations - this is controversial.
We still do not know why sex is the prevailing more of reproduction in eukaryotes.
Gene transmission: 3) crossing-over
Generally, crossing-over within sexual population is favored under the same conditions that
favor sex over asex. However, in order to make crossing-over in a multochromosome
genome substantially beneficial, some really strong selection must operate. A simple graph
shows why this is the case:
If the genetic load is less than 50%
under truncation selection, the
immediate impact of crossing-over
which increases the variance of the trait
under selection is to reduce fitness.
Only if the genetic load is over 50%
under truncation selection, the
immediate impact of crossing-over is to
increase fitness.
Thus, we the ubiquity of crossing-over is even more mysterious than the ubiquity of sex. It
is wrong to claim that crossing-over is simply necessary for meiosis.
Gene transmission: 4) systems of mating
Usually, sex is accompanied by differentiation of gametes. Two kinds of gamete classes are
particularly important:
1) Female (large) and male (small) gametes, a phenomenon known as anisogamy. The male–
female dichotomy has evolved independently in nearly all clades of multicellular organisms.
2) Exogamous classes of gametes different from female-male dichotomy (mating types).
They are common in ciliates, basidiomycetes, and flowering plants.
Inbreeding depression, is the likely cause of the evolution of such classes. Other
mechanisms of inbreeding avoidance, including social taboos, are also common.
Gene transmission: 5) origin of sex
We have no direct data on the origin of sex, because it probably evolved before
diversification of modern eukaryotes. Still, there is a plausible scenario for gradual origin of
sex from asex:
1) Asexual ploidy cycle - alternation of genome duplications and reductions. Such cycles are
known in several protozoans.
2) Origin of outcrossing by occasional cell fusions, followed by genetic reduction due to
random chromosome loss.
3) Origin of regular amphimictic life cycle and crossing-over (from the already present
mechanisms of DNA repair).
Nobody knows whether this is what actually
happened - but there is no reasons to claim
that gradual origin of sex by natural selection
is impossible.
Gene transmission: 6) outcomes of genetic conflicts
Without sex, all genes that constitutes a genotype are in the same boat, forever. In contrast,
sex makes different genes from the same genotype independent. This opens a possibility for
conflicts between different genes in sexual populations.
An example of a genetic conflict:
Mitochondria are inherited maternally. An allele of a mitochondrial gene that forces the
organism to produce only ovules would spread in the population.
Left: this is what a nuclear gene wants we will soon see, why.
Right: this is what a mitochondrial gene
wants.
A genetic conflict occurs when the
spread of an allele lowers the fitness
of its bearer.
Segregation distorters (SD) is a
common class of selfish alleles that
create genetic conflicts by distorting
fair Mendelian segregation.
Segregation distorters are known in
Drosophila, mouse, and many other
organisms.
Selfish elements involved in conflicts are often efficiently suppressed. Male killing, in which
maternally inherited micro-organisms distort the sex ratio by killing male embryos, is the
most deleterious form of sex ratio distortion for the host, leading to the double fitness cost
of mortality and failure to produce the rare sex.
Suppression of male killer wBol1 evolved recently
in many populations of Hypolimnas bolina.
Independent evolution of selfish elements and their
suppressors in different lineages may create
Dobzhansky-Muller incompatibilities between them.
How important are genetic conflicts in general? If individual genes are selfish and can
pursue their own evolutionary "interests", should we regard organisms just as temporary
assemblages of genes of very limited importance?
Probably, the answer is negative: asexuals, protected from tyranny of individual genes
pursuing their own interests are not much different from sexuals.
Left: A bdelloid rotifer fully asexual for ~100
My, master of its genes.
Right: A monogonont
rotifer - facultatively
asexual, but going
through sex regularly.
There are also more complex conflicts that involve different organisms - parent-offspring,
male-female, etc. They will be considered later.
Quiz:
Propose an experiment that could finally determine what evolutionary mechanism is
responsible for the maintenance of sex (I need ideas for the next grant application).