Behavioral Ecology and the Evolution of Altruism - Sinauer Associates

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2
Behavioral Ecology and
the Evolution of Altruism
Not so long ago, I traveled to the Pantanal, a vast
network of marshes and grasslands located largely in
southwestern Brazil. As I followed my host and guide,
Lucas Leuzinger, he pointed out narrow sandy trails
cutting through the scruffy grassland in which we were walking. Hur-
rying along these straight and narrow paths were large numbers of
pale reddish termites, some of which were carrying bits of dried veg-
etation back to their colony’s home, while others were larger, darker
in color, and armed with formidable jaws (Figure 2.1). We were look-
ing at two kinds of termites that belonged to the same species. The
smaller workers were carrying food items that would provide their
fellow termites back at the colony with calories and nutrients. The
workers were accompanied by soldiers, which were there to defend
the workers from ants and other small predators that attack termites.
Amazingly, none of the workers or the soldiers in the colony would
ever reproduce. Instead they would spend their entire lives working
for others, generally one large reproducing female and her much
smaller male partner, the queen and king of the colony, as well as a
new generation of brothers and sisters that would eventually try to
found colonies of their own.56
There are several thousand species of termites, some of which
form colonies of millions of individuals and build immense durable
structures of packed earth that take your breath away (Figure 2.2).
All of these groups, large or small, are composed mostly of sterile
These sterile worker
individuals that do not reproduce but are willing and able to build
weaver ants labor together
to make leaf nests for the the colony’s home, to forage for the resources needed to feed their
repro ductive benefit of
other ants. Why? fellow termites, and to care for the queen and king as well as the
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16 CHAPTER 2
FIGURE 2.1 A group of worker
termites escorted by a single large
soldier back to their colony. None
of the termites will ever reproduce—a
Darwinian puzzle. Photograph by the
author.
eggs laid by the queen, then tend the young immature termites that hatch
from those eggs.
The Darwinian puzzle provided by sterile castes of termites should be obvi-
ous: how can individuals evolve if they are unable to reproduce given that
hereditary differences in individual reproductive success are necessary for
natural selection to occur? And this puzzle applies to more than the termites
because all ants, some wasps, and some bees also form groups with nonre-
producing workers. Among these eusocial insects is the familiar honey bee.
Indeed, most of us are more familiar with this species than we would pre-
fer; when a honey bee worker stings us in defense of her hive
mates, she dies. Her death comes about because her barbed
stinger catches in our skin such that when the bee pulls away
from us, her sting apparatus remains behind to pump toxins
into our body (Figure 2.3).
The honey bee’s suicidal sting is a classic example of self-
sacrificing behavior that helps individuals other than the bee’s
own progeny (and honey bee workers almost never produce
their own offspring).37 There are other cases of this sort, such
as worker ants that stay outside the nest to seal off the nest
entrance in the evening, even though this activity means that
they will die before morning.4,45 Likewise, when colonies of
the grenade ant are under attack, the workers break open their
abdomens, spilling a gluey substance onto the intruders, a sui-
cidal line of defense for the colony.28
In many social insects, the worker caste is composed of
females with atrophied ovaries, which make them incapable
of reproduction. In cases of this sort, the workers have totally
lost the ability to reproduce personally and instead help other
members of their colony reproduce (such as the queen or the
FIGURE 2.2 A huge number of tiny sterile termites built this im-
mense home for their colony in Western Australia. The 3-meter tall
mound probably contains just one reproducing queen and one king.
Photograph by the author.
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BEHAVIORAL ECOLOGY AND THE EVOLUTION OF ALTRUISM 17
(A) (B)
FIGURE 2.3 Sacrifices by social insect workers. (A) In a nasute (pointed-
nose) termite colony, soldiers incapable of reproducing attack intruders
to their colony at great personal risk and spray these enemies with sticky
repellents stored in glands in their heads. (B) When a honey bee stings a
vertebrate (but not other insects), she dies after leaving her stinger and the
associated poison sac attached to the body of the victim. A, photograph by
the author; B, photograph of Bernd Heinrich’s knee by Bernd Heinrich.
future kings and queens produced by the colony). Self-sacrifice of this sort is
what behavioral ecologists refer to as altruism, and it was for a long time very
difficult to see how reproductive suicide could spread by natural selection.
In fact, for most behavioral biologists the widespread occurrence of altruism
represented the premier Darwinian puzzle of them all, which is why we will
tackle this phenomenon now.
Explaining Altruism: Intelligent Design?
Because sterile castes are very hard to explain, the colonies of eusocial insects
have attracted much attention. Among the large group of scientists interested
in social insects are a few adherents of intelligent design theory. Advocates
of intelligent design assert that the extraordinary complexity of social insect
colonies is the kind of thing that cannot be explained by evolutionary theo-
rists. Therefore, so the argument goes, social insect societies, which look as if
they had been designed to serve some function, really have been formed by
some sort of intelligent entity for the purpose of working together efficiently.
According to this view, the several castes of termites cooperate within their
colony in much the same way that a watch has many interconnected parts, all
of which have to interact in a particular way if the watch is to be an accurate
timepiece. A watch requires an intelligent designer, a human; by the same
token, a termite or ant colony supposedly also requires an intelligent designer.
Richard Dawkins destroys this analogy in his book The Blind Watchmaker.9
But for our purposes let’s focus on the fact that the “intelligent designer”
that intelligent design theorists have in mind must be a supernatural being
of some sort. We can say this with considerable confidence, in part because
a federal judge, John Jones, ruled in 2005 that intelligent design theory is a
religious theory, not a scientific one, and as such, intelligent design theory is
intended to be taken on faith and not tested in the manner of a scientific theory
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18 CHAPTER 2
or hypothesis.17 Indeed, intelligent design advocates never use their theory
to specify exactly what complex adaptations are designed to do. Without a
testable hypothesis, science is not possible.
Judge Jones’s decision has significance for education policy because many
school boards, like the one in Dover, Pennsylvania, where the judge delivered
his ruling, have tried to present intelligent design theory in high school sci-
ence classes. Judge Jones said, “No.”17 Religion is not science and therefore
scientists need not concern themselves with intelligent design theory, except
as it poses a threat to legitimate science education in our schools.
Discussion Question
2.1 Let’s say that intelligent design theorists are correct in claiming that
certain features of living things, such as termite societies composed of
20 million cooperating individuals or the long and convoluted biochemi-
cal pathways involved in the production of critical cellular compounds, are
so complex that they cannot be explained by evolutionary theorists. Why
would Darwinists aware of the logic of the scientific method still be justified
in rejecting the assertion that these cases in themselves constitute reason to
accept intelligent design theory?
Altruism and For-the-Benefit-of-the-Group Selection
The modern scientific analysis of altruism really began in 1962 when V. C.
Wynne-Edwards published his book Animal Dispersion in Relation to Social
Behaviour. Wynne-Edwards did everyone a favor by formally proposing that
social attributes, including altruism, had evolved to benefit the group or spe-
cies as a whole.58 According to his theory of group selection, groups or species
with self-sacrificing (altruistic) individuals are more likely to survive than
those without altruists, leading to the evolution of group-benefiting altruism.
A classic example of the application of group selection theory to produce a
hypothesis involves the territorial behavior of many birds in which territory
holders breed but those unable to secure territory do not (Figure 2.4). Wynne-
Edwards explained the behavior of nonterritorial individuals as group-bene-
fiting altruism, with these birds holding back in order to avoid depleting the
food supply on which the entire species depends for its long-term survival.
By much the same token, the sterile castes of social insects might refrain from
reproducing in order to help their colonies persist in environments in which
resources were difficult to secure.
Soon after Wynne-Edwards’s book was published, George C. Williams
challenged this for-the-benefit-of-the-group type of selection in Adaptation and
Natural Selection,52 arguably the most important book on evolutionary theory
written since The Origin of Species. Williams showed that the persistence of a
hereditary trait, and the genes underlying the development of that trait, were
much more likely to be determined by differences in the reproductive success
of genetically different individuals than by survival differences among geneti-
cally different groups. We can illustrate his point with reference to Hanuman
langurs. Imagine that in the past there really were male langurs prepared to
risk serious injury, even death, in order to attack infants, an action that would
reduce the numbers in their band and conceivably promote the survival of the
group. In such a case, group selection would be said to favor male infanticide
because the group as a whole would benefit from the removal of excess infants.
But in this species, Darwinian natural selection would also be at work, pro-
vided that at any time there were two genetically different kinds of males—
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BEHAVIORAL ECOLOGY AND THE EVOLUTION OF ALTRUISM 19
(A) FIGURE 2.4 The territories of an Australian songbird. (A) The
southern emu-wren. (B) A diagram of emu-wren territories over 3 years
at one location. Roads appear as dark lines; permanent bodies of
water are shown in blue. Although the exact locations of the territories
change somewhat from year to year, only pairs with exclusive territories
reproduce in this species and most other birds as well. A, photograph
by Geoff Gates; B, after Maguire.26
(B)
2000 2001 2002
N
300 m
one that practiced infanticide for the good of the group and another that
“permitted” other males to pick up the tab for population reduction. If the
nonkillers lived longer and reproduced more, which of these two types would
become more common in the next generation? Whose hereditary material
would increase in frequency over time? Would infanticide long persist in such
a population of langurs?
This kind of thought experiment, really a test of the logic of group selection
theory, convinced Williams and nearly all his readers that Darwinian selection
acting on differences among individuals within a population or species will
usually have a stronger evolutionary effect than group selection acting on dif-
ferences among entire groups. If group selection favors a trait that involves
reproductive self-sacrifice while natural selection acts against it, natural selec-
tion seems likely to trump group selection,52 as we have just seen in our hypo-
thetical langur example. There have been attempts to develop more convinc-
ing forms of group selection theory, but they have failed to persuade the vast
majority of behavioral ecologists (Box 2.1).
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20 CHAPTER 2
BOX 2.1 Altruism and group selection
Ever since the debate between Wynne-Edwards and Wilson and others (going back to Wynne-Edwards) have
Williams, some scientists, especially David Sloan Wilson, argued that because social insects live in colonies, they
have argued that it is still possible that group selection are ideal candidates for an analysis based on some
might occur under some conditions.12,53 Although form of group selection.55 Here the basic argument
the term group selection has been applied to many is again that colonies with more self-sacrificing
different evolutionary processes,51 there is little doubt individuals will be favored by group selection if groups
that competition among genetically different groups can with more altruists outcompete rival groups and so
have genetic consequences over time, thereby affecting contribute more genes to the next generation. But
the course of evolution. So, if you wish, you can calculate most students of social insects and other social animals
the contribution of alleles to the next generation by use the alternative (but mathematically equivalent)
quantifying the changes in allele frequencies within perspective derived from kin selection theory.
groups rather than by adding up the genes passed on David Sloan Wilson has complained that the preference
by the individual members of that species. But only for kin selection theory stems from prejudice against the
genes replicate themselves; groups of individuals and rejected Wynne-Edwardsian version of group selection.54
individuals by themselves are vehicles that can contribute But as Stuart West and his colleagues have pointed out,51
to the transmission of genes, but they are not replicators kin selection theory is very widely accepted primarily
themselves.5,10 As a result, it doesn’t matter if you use a because it has helped so many researchers develop
group-based method of gene accounting or a system testable hypotheses for puzzling social behaviors
based on individual-level kin selection (see page 23); the exhibited by creatures as different as termites, bacteria,
two methods are mathematically equivalent.27,39 and humans. Because the theory has played a major
The question then becomes, when should group role in helping us understand all aspects of sociality,
selection theory be used to explain complex social especially altruism,42 kin selection theory is featured
behavior, instead of kin selection theory? David Sloan here to the exclusion of group-based alternatives.
Discussion Questions
2.2 Lemmings are small rodents that live in the Arctic tundra. Their
populations fluctuate wildly. At high population densities, large numbers
leave their homes and travel long distances, during which time many die,
some by drowning as they attempt to cross rivers and lakes. One popular
explanation for their behavior is that the travelers are committing suicide to
relieve overpopulation. By heading off to die, the suicidal lemmings leave
shelter and food for those that stay behind. These surviving individuals will
perpetuate their species, saving it from extinction. What theory was used to
produce this hypothesis? How would George C. Williams use Gary Larson’s
cartoon (Figure 2.5) to illustrate the logical problem with group benefit
selection?
2.3 In some ant species, several unrelated females may join forces to
found a colony after they have mated. The females cooperate in digging
the nest and producing the first generation of workers, but then they start
fighting until only one is left alive. The survival rate of colonies founded by
lone females is very low.1 How might you interpret the behavior of mul-
tiple founders as the product of for-the-good-of-the-group selection? If
the behavior of the several queens is the product of natural selection, not
Wynne-Edwardsian group selection, what prediction can you make about
the interactions between the females during the colony establishment
phase prior to the fight-to-the-death phase?
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BEHAVIORAL ECOLOGY AND THE EVOLUTION OF ALTRUISM 21
Altruism and Indirect Selection
So, if we are to explain the altruism exhibited by sterile worker
termites or ants in Darwinian terms, we have to produce a hypoth-
esis in which the apparent self-sacrificing behavior of these work-
ers actually has an evolutionary benefit for them as individuals.
But what could this be if workers and soldiers do not reproduce?
In The Origin of Species, Darwin confronted several problems
for his theory of natural selection illustrated by insect societies,
one of which was the puzzle of worker sterility.38 Darwin saw
a fairly simple solution to this puzzle in the form of an analogy
with domesticated cattle. Although you cannot breed the tastiest
steers, because they are dead, you can let the parents (or other
relatives) of the butchered Black Angus or Herefords with desir-
able attributes remain in the breeding stock even as their offspring
are shipped off to the abattoir. Those that are slaughtered are the
equivalent of workers, in that they fail to reproduce, but their
hereditary attributes (nicely marbled beef, efficient conversion of
grass into muscle, and the like) can persist if their parents go on to
produce the next generation of breeders as well as the sacrificed
animals.
William D. Hamilton reshaped this argument using an under-
standing of heredity far superior to that available to Darwin.18
His theory was based on the premise that individuals reproduce FIGURE 2.5 Gary Larson’s cartoon
of presumably suicidal lemmings
with the unconscious goal of propagating their distinctive family genes more
headed into the ocean. Note the lem-
successfully than other individuals. Personal reproduction contributes to this
ming with the inner tube.
ultimate goal in a direct fashion because parents and offspring share genes in
common. But helping genetically similar individuals other than offspring—
that is, one’s nondescendant relatives—survive to reproduce can provide an
indirect route to the very same end (Figure 2.6). It does not matter which bod-
ies are carrying certain genes; a trait becomes more common if the allele that
promotes the development of that attribute becomes more common.
FIGURE 2.6 How to achieve indirect fit-
ness. By adopting two nephews and a niece,
this woman could be propagating her genes
indirectly because relatives share rare family
alleles with one another. (Here we assume
that the children would not have survived
or reproduced as much had they not been
adopted.)
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22 CHAPTER 2
To understand why, the concept of the coefficient of relatedness is critical.
This term refers to the probability that an allele in one individual is present in
another because both individuals have inherited it from a recent common ances-
tor. Imagine, for example, that a parent has the genotype Aa, and that a is a rare
form of the A gene, which is to say that A and a are two alleles of the gene in
question. Any offspring of this parent will have a 50 percent chance of inheriting
the a allele because any egg or sperm that the parent donates to the production
of an offspring has one chance in two of bearing the a allele. The coefficient of
relatedness (r) between parent and offspring is therefore 1/2, or 0.5.
The coefficient of relatedness varies for different categories of relatives.
For example, a man and his sister’s son have one chance in four of sharing
an allele by descent because the man and his sister have one chance in two of
having this allele in common, and the sister has one chance in two of passing
that allele on to any given offspring. Therefore, the coefficient of relatedness
for a man and his nephew is 1/2 × 1/2 = 1/4, or 0.25. For two cousins, the r
value falls to 1/8, or 0.125. In contrast, the coefficient of relatedness between
an individual and an unrelated individual is 0.
With our knowledge of the coefficient of relatedness between altruists and
the individuals they help, we can determine the fate of a rare “altruistic” allele
that is in competition with a common “selfish” allele. The key question is
whether the altruistic allele becomes more abundant if its carriers forgo repro-
duction and instead help relatives reproduce. Imagine that an animal could
potentially have one offspring of its own or, alternatively, invest its efforts in
the offspring of its siblings, thereby helping three nephews or nieces survive
that would have otherwise died. A parent shares half its genes with an off-
spring; the same individual shares one-fourth of its genes with each nephew
or niece. Therefore, in this example, personal reproduction yields r × 1 = 0.5
× 1 = 0.5 genetic units contributed directly to the next generation, whereas
altruism directed at three relatives yields r × 3 = 0.25 × 3 = 0.75 genetic units
passed on indirectly in the bodies of relatives. In this case, the altruistic tac-
tic is adaptive because individuals with this characteristic pass on more of
the altruism-promoting allele to the next generation than individuals with an
alternative hereditary trait.
Discussion Question
2.4 If an altruistic act increases the genetic success of the altruist, then
in what sense is this kind of altruism actually selfish? In everyday English,
words like altruism and selfishness carry with them an implication about
the motivation and intentions of the helpful individual. Why might everyday
usage of these words get us into trouble when we hear them in an evolu-
tionary context? If an individual just happened to help another at reproduc-
tive cost to itself, should the behavior be called altruistic under the evolu-
tionary definition of the term?
Another way of looking at this matter is to compare the genetic consequences
for individuals who aid others at random versus those who help close relatives.
If aid is delivered randomly, then no one form of a gene is likely to benefit the
bearer more than any other, and the carrier of an altruism allele pays a price for
the help that raises the fitness, that is, the number of genes contributed to the
next generation, of individuals with other forms of the gene. But if close rela-
tives aid one another preferentially, then any alleles they share with other fam-
ily members may survive better, causing those alleles to increase in frequency
compared with other forms of the gene in the population at large. When one
thinks in these terms, it becomes clear that a kind of natural selection can occur
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BEHAVIORAL ECOLOGY AND THE EVOLUTION OF ALTRUISM 23
BOX 2.2 Key terms used by evolutionary biologists in the study of altruism
Altruism: Helpful behavior that lowers the helper’s Indirect fitness: A measure of the genetic success of
reproductive success while increasing the reproductive an altruistic individual based on the number of relatives
success of the individual being helped. (or genetically similar individuals) that the altruist helps
reproduce that would not otherwise have survived to do so.
Direct selection: The process of natural selection that
occurs when hereditarily distinctive individuals differ in the Inclusive fitness: A total measure of an individual’s
number of surviving offspring they produce or number of contribution of genes to the next generation by direct and/
genes they pass on to subsequent generations. or indirect selection.
Direct fitness: A measure of the reproductive or genetic Group selection: The process that occurs when groups
success of an individual based on the number of its differ in their collective attributes and the differences affect
offspring that live to reproduce. the survival chances of the groups.
Kin (or indirect) selection: The process that occurs when Behavioral strategy: An inherited behavior pattern that
hereditarily distinctive individuals differ in the number of is in competition with other hereditarily different behavior
nondescendant relatives (not their offspring) they help patterns in ways that have the potential to affect an
survive to reproduce. individual’s inclusive fitness. An example of a behavioral
strategy is the willingness of individuals to assist close
relatives even though their help reduces their direct fitness.
when genetically different individuals differ in their effects on the reproductive
success of relatives. Jerram Brown called this form of selection indirect selec-
tion (now often called kin selection), which he contrasted with direct selection
for traits that promote success in personal reproduction (Box 2.2).7 Although
there have been claims that kin (indirect) selection theory should be discarded
in favor of an alternative approach,32 few researchers agree, for reasons spelled
out by Andrew Bourke in Principles of Social Evolution.5
Discussion Question
2.5 We can, if we wish, consider the coefficient of relatedness with
respect to those genes on the X chromosome rather than a single gene
or the complete genome. All women have two X sex chromosomes. Their
sons and daughters each get one X from their mother. An adult son may or
may not pass on that X to his children. If he does not and instead gives an
offspring his Y chromosome, he will create a grandson (XY) for his mother.
That grandson will not carry his grandmother’s X chromosome. (Where then
did his X chromosome come from?) What about the X chromosomes in the
granddaughters of the paternal grandmother? What is the significance of
the fact that the survival chances of grandsons with paternal grandmothers
living nearby are much less than the odds of survival for granddaughters
with paternal grandmothers nearby15—(several traditional societies pro-
vided the relevant data.) Does the paternal grandmother’s effect on the sur-
vival of her granddaughters generate indirect selection or direct selection?
Kin Selection and Inclusive Fitness Theory
As I mentioned earlier, Darwin provided a tentative explanation for the
evolution of sterile workers in termites and other social insects, namely that
selection acting on other (reproductively competent) family members could
result in the spread of self-sacrificing traits in the relatives of those reproduc-
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