So far ...

In this course we have mainly discussed evolution within species, and evolution leading to speciation. Evolution by natural selection is caused by the interaction of populations/species with their environments.

Today ...

However, the environment of a species is always partly biotic. This brings up the possiblity that the "environment" itself may be evolving. Two or more species may in fact coevolve. And coevolution gives rise to some of the most interesting phenomena in nature.

What is coevolution?

At its most basic, coevolution is defined as evolution in two or more evolutionary entities brought about by reciprocal selective effects between the entities. The term was invented by Paul Ehrlich and Peter Raven in 1964 in a famous article: "Butterflies and plants: a study in coevolution", in which they showed how genera and families of butterflies depended for food on particular phylogenetic groupings of plants.  We have already discussed some coevolutionary phenomena:

  • For example, sex and recombination may have evolved because of a coevolutionary arms race between organisms and their parasites; the rate of evolution, and the likelihood of producing resistance to infection (in the hosts) and virulence (in the parasites) is enhanced by sex.
  • We have also discussed sexual selection as a coevolutionary phenomenon between female choice and male secondary sexual traits. In this case, the coevolution is within a single species, but it is a kind of coevolution nonetheless.
  • One of our problem sets involved frequency dependent selection between two types of players in an evolutionary "game". The "game theory" underlying this idea could be either between species (as in interspecific competition) or within species (different morphs of the same species) competing for a resource such as food or females. Evolutionary interactions such as this will often produce coevolution.
  • In the rest of this lecture, we will be referring only to between-species coevolution.  Because a very large part of all evolutionary biology involves coevolutionary interactions, we have to pick and choose the examples we treat.  We can choose from among many types of adaptive radiation, or of parasite/host evolution (e.g. coevolution of vertebrates and their diseases).  However, many of the best-studied examples which we shall discuss are to be found among the organisms with most species, insects.

    Coevolution and interspecific interactions

    Coevolution might occur in any interspecific interaction. For example:

    However, tight interspecific interactions do not always lead to coevolution. Mimicry, for example, can be a parasite/host interaction (in Batesian mimicry) or a mutualism (Müllerian mimicry, see earlier lecture). Mimicry creates exactly the kinds of ties between species that might lead to coevolution, but in practice there are rather good reasons why adaptation may be unilateral rather than coevolutionary:
    Palatable Batesian mimics adapt to the unpalatable model by copying its pattern, but the model may not be able to escape its parasite.  The first model individuals with a new, non-mimicked pattern would also lose the protection of their own species' warning pattern. Thus we can hypothesise that "coevolutionary chase" is an unlikely outcome of Batesian mimicry.

    In Müllerian mimicry the most abundant and noxious species will also be trapped by its own pattern; any individuals that mimic a rarer or less noxious species will lose the protection of their own species' pattern even though, once the new mimetic pattern became common, both species would ultimately benefit. In contrast, the rarer or less noxious species always gains by mimicking the more common or noxious species, because its own species' protection is weaker than the other's. Mutual convergence is therefore unlikely because of these difficulties for the initial mimetic variants, in spite of the fact that the outcome, once achieved, is mutualistic.

    Thus, mimicry is a good example showing that coevolution does not always result from interspecific interactions. In mimicry, perhaps surprisingly, the outcome seems almost always to produce unilateral adaptation by one species to the other.

    In general, there is much discussion about the likelihood of coevolution in cases where more than one species is involved in an evolutionary interactions. An "Ockham's Razor" approach to proving coevolution requires that we should first disprove the simpler hypothesis of unilateral adaptation.

    Types of coevolution

    Answers to the question "How likely is coevolution?" depends what you mean by coevolution! Various types have been proposed:

    In specific coevolution, or coevolution in the narrow sense, in which one species interacts closely with another, and changes in one species induce adaptive changes in the other, and vice-versa. In some cases, this adaptation may be polygenic; in other cases, there may be gene-for-gene coevolution, in which the mutual interactions are between individual loci in the two species.

    Specific coevolution may of course be short-lived, but if the interaction is very close, as in many host-parasite systems, concordant speciation or cospeciation may result; where the speciation in one form causes speciation in another. Of course, cospeciation doesn't necessarily require coevolution.  For example, a very unimportant but highly host-restricted parasite may always speciate whenever its host speciates, without the parasite causing any evolutionary reaction in the host.

    In diffuse coevolution, also called guild coevolution, whole groups of species interact with other groups of species, leading to changes that cannot really be identified as examples of specific, pairwise coevolution between two species. For example, a group of plant species may be fed on by a particular family of insects, which may frequently (in evolutionary time) change hosts. The plants may evolve defensive adaptations, such as defensive chemistry, or physical defenses such as spines, which work against large numbers of the species. In time, some of the insects may be able to overcome the plant's defences, leading to further evolution by the plant, and so on.

    Another related type of evolution is called escape-and-radiate coevolution. Here, an evolutionary innovation by either partner in a coevolutionary interaction enables an adaptive radiation, or speciation due to the availability of ecological opportunity. For example, it is easy to imagine that this could be a result of the diffuse kind of herbivore-plant coevolution described above.

    It is interesting that Ehrlich and Raven almost certainly did not mean specific coevolution in their original paper about the evolutionary interactions between butterflies and their host plants. Some people today even go so far as to say that they were not talking about coevolution at all.

    Concordant and non-concordant phylogenies

    Phylogenies are very useful in the study of coevolution.  If the phylogenies of two closely associated groups, such as host and parasite, are concordant (see overhead), this may imply:

    In other cases, phylogenies may not be concordant, because the parasite may be able to switch between host lineages fairly frequently (see examples on overheads).

    Host/parasite and predator/prey coevolution

    However, as we have seen, even contemporaneous cospeciation with concordant phylogenies does not prove that two lineages have coevolved.  Instead, we can look at individual adaptations of the interacting species to get an idea of whether coevolution has taken place.  Here are some examples:

    Defences of plants against herbivores

    Plants have many complex chemicals, called "secondary chemicals", which are not obviously used in normal metabolism.  Ehrlich and Raven and others subsequently interpreted this "secondary chemistry" as an example of defensive adaptation by the plants. Many of these compounds (for instance, tannins and other phenolic compounds, alkaloids like nicotine, cocaine, opiates and THC, or cyanogenic glycosides) are highly toxic.  Many animals such as insects have adapted to feeding exclusively on plants with particular defensive chemistry.  If the plants evolved secondary chemistry to avoid insects, and insects evolved to handle the plant chemistry, then  plant/insect coevolution has occurred.

    However, critics argue that:

    To find evidence for coevolution, we must show that specific poisons or other defenses work against specific insects, or that they become less necessary when the insects are not present.

    Ant-acacias. Good evidence for insect/plant coevolution is found in the Central American plant known as "bullshorn Acacia", Acacia cornigera.  This plant is similar to other members of the genus Acacia (thorn trees in the pea family), in that it has large spines which presumably protect it against mammalian herbivores (another example of coevolution, presumably against mammalian browsers).  However, it lacks the cyanogenic glycosides (cyanide-producing chemicals) found in related Acacia and the thorns in this species are particularly large and hollow, and provides shelter to a species of Pseudomyrmex ant. The plant also provides proteinaceous food bodies on the tips of the leaflets, which sustain the ant colonies. These ants are particularly nasty (I can tell you from personal experience!), and are well able to deter even mammals with their wasp-like stings.  It has been shown experimentally that the ants will also remove any caterpillars from the leaves that they patrol.  The ants even remove vines and plants from around the base of the tree, creating a bare patch on the soil.  Plants of the bullshorn Acacia which have not been occupied by ant colonies are heavily attacked by herbivores and often have vines growing in the branches.

    Related Acacia species lack hollow thorns and food bodies, and do not have specific associations with ants.  They also have many cyanogenic glycosides in their leaves.  This data strongly supports the idea that the bullshorn Acacia has evolved a close, mutualistic association with the ants in order to protect themselves from herbivores (and also plant competitors).  It also supports the idea that the cyanogenic glycosides found in other species have a defensive role; a role which has been taken over by Pseudomyrmex in the bullshorn Acacia.

    Egg mimicry in Passiflora. Similarly, we have already given examples of egg-mimicry in Passiflora, which protects plants against species of Heliconius butterflies.  Female Heliconius avoid laying eggs on plants already occupied by eggs, because first instar larvae of Heliconius are highly cannibalistic; the plants exploit this habit of Heliconius by creating fake yellow eggs as deciduous buds, stipule tips, or as part of the "extrafloral nectaries" on young leaves.  Clearly, the plant, whose defenses of cyanogenic glycosides, alkaloids, and a host of other secondary compounts, have been breached by Heliconius, has counterevolved new defenses against this genus.

    Heliconius-egg mimicry in Passiflora

    Predator-prey coevolution

    Predators have obviously evolved to exploit their prey, with hunting ability being at a premium.  Mammalian predators, for example, must be fast, strong and cunning enough to be able to catch their prey.  It is almost as obvious that prey have evolved to protect themselves from predators.  They may have a variety of defenses:

    Clearly these features also represent examples of coevolution.  We have already pointed out that it is thought unlikely that mimics coevolve with their models in Batesian or Müllerian mimicry systems.  These mimicry systems are nonetheless examples of coevolution, but with their predators rather than with their mimics!

    Some very specialized coevolved pollination systems

    Two of the most famous are figs and fig-wasps, and Yucca and Yucca moths (Tegeticula).

    In both cases, the larvae are seed/flower eaters, which reduce the fertility of the flowers or inflorescences they infest.

    In both cases, the plant is completely dependent on its herbivore for pollination.  The arrangement is therefore a tightly coevolved mutualism, in which the plant relies exclusively on the insect for pollination, and the insect relies exclusively on the plant for food.

    In the case of the Yucca moth the mutualism has sometimes broken down, and some clades of the moth have reverted to a parasitic mode of life -- they oviposit in the plant, but do not pollinate -- the ancestral condition for the moths.

    These examples are interesting because they represent cases where mutualisms have become so specific that they almost rival the ancient prokaryotic mutualisms of mitochondria and chloroplasts with archaebacterial cells, to produce what we now know as eukaryotes.

    Coevolutionary competitive interactions and adaptive radiation

    It is an ecological principle (Gause's principle) that related species must differ in some part of their ecology. If two species have identical or nearly identical resources, competitive exclusion will result, and the less well adapted species will go extinct.

    If this is true, and it probably is, the reverse should also occur.  If a species colonizes an area where its competitors do not occur, then it may experience ecological release, and grow to very large population sizes.  Not only that, the colonists may also experience disruptive selection, followed by speciation. The process can be repeated for multiple species, which evolve apart from one other to form an adaptive radiation.

    Many examples of this principle are known in island colonists.  For example, we have already come across the Darwin's finches of the Galapagos islands, which have evolved into a whole range of seed-feeding and insectivorous forms.  A similar, although much more diverse radiation occurs in the Hawaiian archipelago: the Hawaiian honeycreepers.

    Sometimes, the islands are "ecological islands" rather than actual islands.  A number of lakes in the North temperate zone were left behind during the retreat of the ice.  These lakes have in the last 10,000 years been colonized by a variety of fish.  In many cases of stickleback and the trout family, multiple forms have now been produced in each lake or large fresh water body.

    Sticklebacks in Canada (Gasterosteus) often produce benthic (deep water) and limnetic (shallow water) forms (see overhead), which appear to have specialized feeding differences.  These forms also keep to their own habitat, and may mate assortatively.

    Similarly, the Atlantic char (Salvelinus)  in Thingvallavatn, Iceland's largest lake, have produced no less than FOUR different trophic forms; similar examples are known from Norway and Ireland for other salmonids.

    Adaptations leading to ecological release, and "escape and radiate" coevolution

    As well as the colonization of new habitat, the possession of a unique adaptation may also allow adaptive radiation to colonize a new "adaptive zone" opened up as a result.  There is good evidence for this:


    Evolutionary interactions between species, and coevolution show that the complexity of genetic evolution goes on increasing, even beyond the species level.  Coevolution represents an area where genetics, ecology, phylogeny all interact.  To understand the evolution of life fully, the interactions between individuals and species must be explored at many levels.

    One thing is clear; the majority the diversity of life and life forms is not just due to adaptation to static environments; biotic interactions are probably much more important.  The biotic environment is itself constantly evolving, leading to orders of magnitude more diversity possible than could be produced by evolutionary adaptation to simple physical conditions.

    Further reading

    Ehrlich, PR, Raven, PH 1964. Butterflies and plants: a study in coevolution. Evolution 18, 586-608.
    Farrell, BD 1998. "Inordinate fondness" explained: why are there so many beetles? Science 281, 555-559.
    Futuyma, DJ 1998.  Evolutionary Biology.  Chapter on coevolution.
    Thompson, JN 1994.  The Coevolutionary Process. Chicago University Press.

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