Topic 17. Lecture 27. Evolution of Populations and Ecosystems-II

What questions can be addressed by considering Macroevolution of simple phenotypes?

Independently evolving individuals: Gene transmission: 1. Phenotypic plasticity 1. Mutation 2. Non-interactive behavior 2. Maintenance of sex 3. Semelparity and iteroparity 3. Crossing-over 4. Clutch size 4. Systems of mating 5. Dormancy 5. Origin of sex 6. Aging 6. Outcomes of genetic conflicts

Interactions between individuals: Complex population-level phenomena: 1. Warning coloration 1. Multicellularity and coloniality 2. Dispersal 2. Anisogamy and sex allocation 3. Aggression 3. Mate choice 4. Cooperation and altruism 4. Female preferences and male displays 5. Conflicts between gametes and sexes 6. Conflicts between relatives 7. Eusociality

Today, we will consider the second half of these questions.

Interactions between individuals: 1) warning (aposematic) coloration

It is not obvious how can warning coloration originate by natural selection. A single mutant with conspicuous coloration would be eaten soon, because the predators would not have a chance to learn that such coloration means trouble.

Examples of warning coloration:

A wasp A salamander

A nudibranch gastropod A flatworm

A skunk A frog

Mathematical models indicate that selection on novel warning signals is number- rather than frequency-dependent. There exists a threshold number of aposematic individuals below which aposematism is selected against and above which aposematism is selected for.

Interactions between individuals: 2) dispersal

There may be situations when the fitness of an individual would be higher if it does not move, but an allele that causes an individual to move will nevertheless spread in the population. This paradox appears because if an individual does not migrate, it will be likely to compete, within the same local population, with related individuals.

One can say that migrating to another place with some probability is an ESS (evolutionarily stable strategy). A simple ESS is a phenotype such that, if everyone in a population possesses it, a different phenotype cannot be advantageous and, thus, cannot invade.

Interactions between individuals: 3) aggression

Aggression against members of the same population is very common. In different species, conflicts between individuals can have different forms and outcomes, including death of one or both opponents.

Examples of aggressive behavior:

Boxing" walnut flies Betta fighting fish

However, very often conflicts are "ritualized": neither opponent uses all the weapons available. How could this "moderation" evolve? Can it be explained without invoking "bad for an individual but good of the species" group selection arguments?

Examples of ritualized conflicts:

Western diamondbacks Eastern orynxs

Consider only two behavioral phenotypes ("strategies") - hawk (H, always attack) and dove (D, always be nice). When two individuals fight, the winner gets benefit b, and the loser suffers the cost of injury c. Two H's will fight, and the expected payoff for each is (b-c)/2. Two D's will not fight and will split the benefit, and the expected payoff for each is b/2. An H and a D will not fight, so that H gets b and D gets 0. So, the payoff matrix is:

My opponent:

H D

Me: H (b-c)/2 b D 0 b/2

So, what to expect, evolutionarily? If everybody is a D, H is beneficial and will invade the population. However, if everybody is an H, D is beneficial, as long as c > b (avoid fighting altogether, if it is too costly). Thus, evolutionarily stable strategy here is mixed - be a H sometimes and a D sometimes.

There may be better strategies that simple H and D or even their mixture: start fighting, but escalate a conflict only until some point. This probably explains the evolution of ritualized conflicts through individual (not group) selection.

Guinea baboons appear to be honest in In contrast, a lizard Phrynocephalus mystaceus signaling their strengths. pretends to be more dangerous than it is.

This is a complex subject, but, generally, honest signaling can evolve only if any signaling is costly - due to production cost or social cost of the signal.

Still a better strategy is to persecute a weak, and to run away from a strong. OK, but do you want to honestly inform you opponent how dangerous you are?

The highly variable black facial patterns of female paper wasps, Polistes dominulus serve as "badges of status". In staged contests between pairs of unfamiliar wasps, subordinate wasps with experimentally altered facial features ('cheaters') received considerably more aggression from the dominant.

If you try to pretend that you are stronger than you are, they will beat you up.

Interactions between individuals: 4) cooperation and altruism

Individuals very often help each other, even when this is costly. Under what conditions can we expect costly cooperation to evolve? Consider a very simple model. There are only two phenotypes ("strategies") - cooperate (C) and defect (D). If one partner (prisoner) defects and another cooperates, D is released and C gets 10 years. If both defect, each gets 7 years, and if both cooperate, they are released after one year. So, the payoff matrix is:

My opponent:

C D

Me: C -1 -10

D 0 -7

So what is better - to cooperate with your partner or to defect? This is a famous Prisoner's Dilemma. If the partners encounter each other only once, it is always better to defect - no matter what your partner does, your payoff would be higher if you do so.

However, if the same two partners encounter each other many times (repeated Prisoner's Dilemma), this conclusion is no longer valid. Indeed, if constant cooperation of both partners can somehow be established, both partners will benefit, as compared to the case of both of them constantly defecting: there will be only 1 year in jail, instead of 7 years, for each crime.

Here, phenotypes are algorithms: on the basis of what it and its partner did in previous encounters, and individual has to decide whether to cooperate or defect at this time. A very simple phenotype does very well in repeated Prisoner's Dilemma: start from cooperation, and afterwards do what you partner did in the previous round (tit-for-tat).

TFT individual: CCCCCCDDCCCCCCDDDDCCC

Its partner: CCCCCDDCCCCCCDDDDCCCC

Perhaps, it may be even better to be more generous and to forgive occasional defections.

Thus, costly cooperation can evolve by natural selection if a phenotype that practices it has the highest fitness. There are five situations when this is possible:

1) kin selection2) direct reciprocity3) indirect reciprocity4) network reciprocity5) group selection.

A cooperator is someone who pays a cost, c, for another individual to receive a benefit, b. A defector has no cost and does not deal out benefits. Cooperation cannot evolve in any mixed population, because defectors have a higher average fitness than cooperators. However, a population of only cooperators has the highest average fitness, whereas a population of only defectors has the lowest. Thus, natural selection constantly reduces the average fitness of the population. Fisher's fundamental theorem does not apply here because selection is frequency-dependent.

Five mechanisms for the evolution of cooperation:

1) Kin selection operates when the donor and the recipient of an altruistic act are genetic relatives.

2) Direct reciprocity requires repeated encounters between the same two individuals.

3) Indirect reciprocity is based on reputation; a helpful individual is more likely to receive help.

4) Network reciprocity means that clusters of cooperators outcompete defectors.

5) Group selection is the idea that competition is not only between individuals but also between groups.

Kin Selection "I will jump into the river to save two brothers or eight cousins" (Haldane). More precisely, kin selection can lead to the evolution of cooperation if the coefficient of relatedness between the interacting individuals, r, exceed the cost-to-benefit ratio of the altruistic act: r > c/b (Hamiltons' rule). Here, relatedness is defined as the probability of sharing an identical-by-descent allele. The probability that two brothers share the same gene by descent is 1/2; the same probability for cousins is 1/8.

Direct ReciprocityRepeated Prisoner's Dilemma is an example of this situation.

Indirect ReciprocityHelping someone establishes a good reputation. Interacting with somebody who has a good reputation is beneficial, thus, such individuals can be "rewarded".

Network ReciprocityA cooperator pays a cost for each neighbor to receive a benefit. Defectors have no costs, and their neighbors receive no benefits. In this setting, cooperators can prevail by forming network clusters, where they help each other.

Group Selection If small groups of individuals are units of selection, cooperation can evolve, because groups of cooperators have higher fitness.

Some other possibilitiesThere are also some possibilities. For example, cooperators can recognize each others ("Green beard model"). Perhaps, several of these mechanisms contribute to evolution of cooperation in nature (J. Evol. Biol. 20, 415-432, 2007).

Not only complex animals can cooperate. The social amoeba Dictyostelium discoideum is a model for social evolution and development. When starving, thousands of the normally solitary amoebae aggregate to form a differentiated multicellular organism.

Complex population-level phenomena: 1) multicellularity and coloniality Multicellularity evolved in red algae, brown algae, green algae, fungi and animals (not counting "borderline" cases). In green algae, it evolved several times independently.

Volvox sp. Ulva sp. Chara sp.

The origin of multicellularity and coloniality is a complex and murky subject. It seems that the correct way of thinking about this subject is to consider conflicts and cooperation among individual cells (or organisms).

Multicellularity opens a possibility of conflicts between selection at different levels. A dominant mutation causing Apert syndrome is much more common in children of older (>45 years) fathers. Apparently, this is because cells that carry this mutation have a selective advantage within male germline.

Hi, my name is Frans Wallenberg and I have Apert Syndrome. When I was child, maybe 3-4 years old, I got my first surgery for my fingers... www.apert.org/wallenberg/index.html

Complex population-level phenomena: 2) anisogamy and sex allocation

Anisogamy (including its extreme form, oogamy) evolved many times.

Isogamy Anisomagy Oogamy

Why are sperm small and eggs large? The most plausible explanation is disruptive selection on gamete size: small gametes are favored because many can be produced, whereas large gametes contribute to a large zygote with consequently increased survival chances. This model assumes that increases in zygote size confer disproportional increases in fitness.

When two sexes (exogamous classes of gametes) are present, resources are usually allocated to them, by all individuals in the population, in equal proportion. This 1:1 sex allocation evolves owing to the simple fact that a zygote gets 50% of genes from the mother, and another 50% from the father. As a result, 1:1 sex allocation is an EES in simple cases.

Suppose that sex ratio in the population is female-biased. Consider a rare genotype that produces more males than others. Because a son will transmit more genes than a daughter (there is a deficit of males), in the 2nd generation this genotype will be overrepresented.

If there are 4 females for each male, a male, on average, transmits 4 times more genes than a female.

More complex situations are possible in structured populations. For example, if matings occurs within a sibship, an EES is to produce just one male who will mate will all his sisters.

Melittobia digitata, a small parasitic wasp with female:male ratio 20:1. A host larva is usually parasitized by just one female, so that only full sibs can mate each other.

Complex population-level phenomena: 3) mate choice

Why should a female care with whom to mate? Mate choice can exist either due to an immediate benefit or to a delayed benefit of producing offspring with better genotypes.

There are 2 feasible immediate benefits of mate choice:

1) Direct investment - it is better to mate with a vigorous male, who will help to rise kids.

2) Reducing harm - it is better to mate with a male who will do you less harm.

However, immediate benefits can hardly explain all the instances of mate choice. Indeed, a father often contributes nothing but genes to his offspring and a variety of mates can be harmless. Thus, delayed benefits are probably important. Such benefits can be of two kinds:

1) Sexual selection - a choosy females produces more attractive sons, because their father was more attractive ("Fisherian runaway").

2) Nonsexual selection - a choosy female produces offspring with generally superior genotypes, because their father had good genes.

However, both these ideas are not without problems:

1) Fisherian runaway mechanism is very fragile and does not work if there is even a slight cost of choice for a female.

2) Fisher's Fundamental Theorem implies that, at equilibrium, there should be no heritable variation in fitness and no correlation between the quality of a father and his offspring.

However, data demonstrate that heritable variation and parent-offspring correlations in fitness within natural populations are often quite large, probably, due to never-ending influx of deleterious mutations.

Thus, it seems that the ability of good-quality fathers to sire good-quality children is the main reason for the evolution of female mate choice, although this issue is not yet settled.

Complex population-level phenomena: 4) female preferences and male displays

Quite often, females not only choose mates, but do it according to rather bizarre criteria. Indeed, why should anybody want to mate with a peacock?

Clearly, such exaggerated and costly sexual displays can evolve only as a result of coevolution with female choice.

Costly female preferences for males with exaggerated traits that reduce viability can evolve when the exaggerated trait, although maladaptive per se, indicates high overall quality of the male's genotype. The following evolutionary scenario appears to be plausible:

1) Initially, high-quality males have slightly longer tails.

2) Females start using long tails as a clue for choosing high-quality mates.

3) This females choice causes all males to evolve exaggerated tails, that reduce their fitnesses. However, high-quality males can tolerate longer tails.

As a result, a stable female preference for very long tails, and stable exaggeration of tail length over viability optimum can evolve.

This scenario is supported by some data, but the issue is not yet settled.

Complex population-level phenomena: 5) conflicts between gametes and sexes

An egg and a sperm have rather different "interests". An egg needs to be fertilized - but only once, as otherwise it will not develop properly. A sperm needs to fertilize an egg, and has nothing to lose. Consequently, an arms race can occur between the ability of a sperm to penetrate an egg and an ability of an egg to make sure that only one sperm will do this.

After one sperm gets in, the whole egg envelop must instantly become resistant to all other sperms.

Such conflicts are common and often lead to extremely rapid coevolution, within the same genome, of genes with egg- and sperm-specific expression. Protein lysin in red abalone (Haliotis rufescens) is responsible for sperm-egg interaction and evolves extremely rapidly.

Complex population-level phenomena: 6) Conflicts between relatives

Evolutionary interests of genes expressed in relatives can often be very different (only if reproduction is sexual, of course, as otherwise all relatives have the same genotype). Such conflicts can lead to complex phenomena if neither side is in complete control.

Siblicide in the brown booby

The extreme form of sib-sib conflict is siblicide. If the amount of resources is insufficient to support all sibs, killing others may be the only chance for an offspring to survive. In this situation, siblicide may be also in the evolutionary interest of parents, as otherwise they would have no surviving offspring.

There may also be conflicts between parents and offspring. The evolutionary interest of a parent is not to waste resources on weak offspring. In contrast, the evolutionary interest of each offspring is to survive.

In organisms in which developing embryos are independent of the mother, under optimal conditions over 99% of embryos develop successfully. In contrast, in mammals and seed plants the success rate is lower, although an embryo is protected and supplied by mother. In humans, at least 30% of pregnancies are spontaneously terminated at very early stages.

>99% success rate ~70% success rate

A possible reason is that the maternal organism refuses to support embryos that appear to be weak or abnormal. Perhaps, this effect diminishes with the maternal age, because of diminishing chances of having other children.

Complex population-level phenomena: 7) eusociality

Eusociality is an extreme form of altruism, such that many individuals do not reproduce and, instead, help their relatives to raise their offspring. Often, only one female (queen) reproduces in a colony, with other individuals being sterile workers.

Queen and workers of honey bee, Queen and workers of an ant, Apis mellifera Formica fusca

In hymenopterans, workers in a single-queen colony are her sisters and daughters.

Naked mole rat (Heterocephalus glaber) is a eusocial mammal. The queen is the only reproductive female in the colony.  Other individuals serve particular societal roles, such as soldiers and cleaners.

Eusocial sponge-dwelling snapping shrimp, Synalpheus regalis. They live in colonies with tens to hundreds of members and only one reproductive female.

Queen and workers in a termite. All modern species of termites (order Isoptera) are eusocial.

Evolution of eusociality apparently proceeds through kin selection. In hymenopterans, who have haploid males, it may be aided by closer relatedness of a female to her sisters (75% of identical by descent genes) than to her daughters (only 50% of such genes).

Phylogeny of eusocial Hymenoptera (ants, bees, and wasps). Each independent origin of eusociality is indicated by alternately colored clades. Clades with high polyandry (>2 effective mates) are in solid red, those with low polyandry (>1 but <2 effective mates) are in dotted red, and monandrous genera are in black.

The key factor in the evolution of eusociality appears to be monogamy. This is to be expected in eusociality evolved due to kin selection.

Evolution of Ecosystems

A ridiculously short summary

Ecosystems consist of populations of many species. Obviously, properties of an ecosystem are affected by the evolution of constituent populations. Such evolution can easily produce unexpected results. An ecosystem consisting of just two species, a prey and a predator, can exist either in an equilibrium state (if the predator is inefficient) or in a state of stable oscillations (if the predator is more efficient). If the predator is very efficient, the amplitude of these oscillations can become very wide, which can lead to extinction of the predator, due to lower critical density phenomenon (Allee effect). Thus, adaptive evolution of a predator can first destabilize the ecosystem and later even lead to the predator's extinction.

Possible consequences of slow evolution of more efficient predators.

Quiz:

What observations and experiments can be used to establish the mechanisms of evolution of cooperation?