EEOB 400: Lecture 15

Coevolution

Coevolution

What is coevolution?

Two (or more) species: 1) exert selective pressures on each other, and2) evolve in response to each other

Because each species is evolving in response to the other, one important feature of coevolution is that the selective environment is constantly changing

When does coevolution occur?

Selective pressure will be strongest when there is a close ecological relationship

“Close” ecological relationship = usually specialists rather than generalists

Important ecological relationships that give rise to coevolution:

1) predators & prey 2) parasites & hosts 3) mutualists 4) competitors

predator

prey

parasite

host

+ - + -mutualist A

mutualist B

+ +competitor A

competitor B

- -

How do we study coevolution?

Like most evolutionary questions, it can be studied at various levels:

Adaptations of individuals Interactions between species Broad evolutionary patterns

Coevolution

Coadaptation Reciprocal adaptations of two species

Could refer to species, adaptations possessed by individuals, genotypes, etc.

Lycaenid caterpillars secrete “honeydew” that ants drink Ants defend caterpillars against parasitic waspsHoneydew secretion and defense are coadaptations

Does coadaptation demonstrate coevolution?

Biologists often have a strict definition of coevolution: evidence of parallel evolution between taxa is required

Fig-wasp mutualism

Fig trees (Ficus)

~750 tropical species, all of which depend entirely on wasps for pollination

Figs are not fruits – they are specialized inflorescences with hundreds of unisexual flowers

Fig-wasp mutualism

Fig wasps (Agaonidae)

Males: suited only for boring holes and mating

Females: adaptated for flying, burrowing into figs, and laying eggs in fig oocytes

Coadaptations

- Receptive figs produce scents that are specific to a particular pollinator species- Shape of ostiole specific to head shape of particular wasp species (lock-and-key)- Morphology of individual flowers specialized to a particular wasp species

Male Female

Female wasp enters via ostioleand oviposits infemale flowers

Male flowers

Female flowers

Flower styles aredifferent lengths –wasps only ovipositin ones w/ short styles

Pollen

Fig-wasp mutualism

Don’t worry…the wasps leave before the fruit is ripe to eat

Fig-wasp mutualism

Seed dispersal

Although pollination is very host-specific, seed dispersal is usually not

Over 1200 different vertebrate species are known to eat & disperse fig seeds

Accordingly, we would expect fig-disperser coevolution to be much weaker

Fig-wasp mutualism

A twist to the story…parasitism

In addition to pollinating wasps, figs are associated with parasitic wasps

Parasitic wasps do not enter the ostiole and do not pollinate the fig’s flowers

Instead, they use a long ovipositor to puncture the fig and lay eggs from outside

Parasites reduce fitness of figs and pollinator wasps

- By ovipositing in flowers that would otherwise produce pollinator wasps

- By directly predating pollinator wasps in some species

- By ovipositing in flowers that would otherwise produce seed for the fig

Cophylogeny

Congruent phylogenies due to cospeciation – strong evidence for coevolution

Fig-wasp mutualism

Cospeciation

Congruent

Host jumping Duplication “Missing the boat”

Incongruent

Figs Wasps

A statistical method known asphylogenetic reconciliation analysis tests the hypothesis that two phylogeniesare more different than expected by chance

Fig-wasp mutualism

Cospeciation

Figs and pollinator wasps show a very high degree of cospeciation

Despite pressure fromparasitic wasps, fig –pollinator specificityis maintained

Indicates a very tight ecological relationship

Weiblen & Bush (2002) Mol. Ecol. 11:1573-1578

Cospeciation

Figs and parasites do not show as strong evidence for cospeciation

Weiblen & Bush (2002) Mol. Ecol. 11:1573-1578

Host jumping

Host duplication

“Missing the boat”

Fig-wasp mutualism

Fig-wasp mutualism

Figs are coadapted to both pollinators and parasites

Figs must balance their own reproductive success against the need to maintainpollinator specificity and reduce impact of parasites

Some ancestral figs solve this problem byproducing flowers with styles of differentlengths so at least some will produce seed

Parasites oviposit through fig and intooutermost layers of oocytes

Pollinators oviposit from within the fig and into innermost layers of oocytes

Fig-wasp mutualism

Figs are coadapted to both pollinators and parasites

Figs must balance their own reproductive success against the need to maintainpollinator specificity and reduce impact of parasites

Functional dioecy

Some species produce figs with eitherall long or all short styled flowers

A will produce pollen and pollinator eggs,so it is functionally male (= no fig seed)

B will produce only seed (and parasiteeggs), but to do so it has to smell like Ato trick pollinator females into entering

This strategy doesn’t eliminate parasitism,but it guarantees that seed will be set

Note that mutualism is not all “warm and fuzzy”…mutualists will always try to maximize their benefit (pollination) and minimize their cost (loss of seed production)

Plant-insect coevolution

Cospeciation in a plant-herbivore system

Tetraopes beetles eat milkweed plants in the genus Asclepias cospeciation

Plant-insect coevolution

Cospeciation in another plant-herbivore system

Blepharida beetles eat Bursera plantsPlant Beetle

Becerra (1997) Science

Plant-insect coevolution

Cospeciation in another plant-herbivore system

Blepharida beetles eat Bursera plants

There is a high degree of host-specificity

Then why so much host-jumping?

Why not cospeciation like in Tetraoptesbeetles and milkweed plants?

Becerra (1997) Science

Plant Beetle

Host specificity is determined by the chemical defenses of the plant

Four major chemical classes of plant defenses against herbivory(indicated by colors)

These chemical classes do notcorrespond to plant clades (top)

The bottom figure shows beetlephylogeny with branches codedfor the chemical type of the host

The phylogenies are incongruentbecause host switching can occur as long as the beetle switches to anew host with chemical defenses towhich it is already adapted

Plant-insect coevolution

Becerra (1997) Science

Cophylogenies

Congruent phylogenies can arise for more than one reason

Today we are discussing congruence as a result of cospeciation

But recall that congruence is also predicted by vicariance biogeography

A

B

C

D

E

IncongruentCongruentCongruent

Plant-pollinator coevolution

Flower and fly or moth pollinators

Many flies and moths have outlandish proboscises to extract nectar from similarly outlandish flowers

Darwin received a specimen of the orchid Angraecumsesquipedale and predicted from it that there mustexist a pollinator with a proboscis measuring 10-12”

This prediction was not confirmed until 1903 withXanthopan morgani moth

Host specificity drives coevolution

A flower “wants” its pollen spreadto other flowers of the same species

Flower evolvesFly responds

Extravagant traits cancoevolve in response

A coevolutionaryescalation

Plant-pollinator coevolution

Mutualisms can be exploited

Figs 2-4 = flower species that produces nectar

Figs 5-6 = mimic orchid that “cheats” Anderson et al. (2005) Am. J. Botany 92: 1342

Mutualisms can be exploited by “cheaters” that collect benefits but avoid costs, as in the case of the deceptive orchid Disa nivea

D. nivea mimics a nectar-producingflower to fool the flyProsoeca ganglbaueri

Plant-pollinator coevolution

Ant mutualisms

Ants and insects that produce “honeydew”

Ants participate in dozens of mutualisms and show coadaptations for each

Many different insects provide ants with “honeydew” – source of nutrition for theants that has no other function for the insect – specifically coevolved for ants

In return, ants defend insects from parasites and predators

Ants tending a lycaenid caterpillar Ant drinking honeydew from an aphid

Ant mutualisms

Ants and acacia trees

Pseudomyrmex ants protect acacia trees from herbivores – in return, the acaciafeeds the ant with nectar and protein rich Beltian bodies, and provides a place forthe ants to live in the acacia’s modified thorns

Ant-fungus mutualism

Attine ants (~210 species) have cultivated fungal gardens for over 50 million years

Benefits to the ant: Fungi produce nutritional “gongylidia” that areharvested by ants to feed their larvae

Fungi can digest cellulose, ants can not

Captive colony of Atta mexicana tending to a fungal garden

Atta cephalotes collecting leafcuttings for their fungal garden

Benefits to the fungi: Ants remove plants and otherfungi that compete for nutrientsand provision fungi with leaves

Ants cultivate actinomycetebacteria that produce antiboioticsagainst Escovopsis fungi, which would otherwise parasitize the mutualist fungi Ant with pockets

of bacteria

Ant mutualisms

Ant-fungus mutualism

To simplify the system in a diagram:

Ant Cultivar (gardened fungus)

Bacterium (actinomycete)

Parasite (Escovopsis fungi)

+ +

+ +

Parasite kills cultivar

Antibiotics kill parasite

-

-

Mutualism

Mutualism or commensalism

A four-way symbiosis – but do these species coevolve?

Ant mutualisms

Currie et al. (2003) Science 299: 386-388

Coevolution – Patterns of parallel evolution between ants and fungal cultivars

…and between these two groups and Escovopsis parasites !!

Ant mutualisms

Host-parasite coevolution

Coevolution – Thus far we have seen examples from mutualism interactions

Pocket gophers (Geomyidae) are are parasitized by lice (Mallophaga)

Clear pattern of cospeciation – this example also shows how rates of evolution can be compared (b) to provide further evidence for coevolution (letters in b = branches in a)

Coevolutionary arms races

“Arms race”

Coevolving species have to constantly “improve” to meet each new adaptation with a “better” adaptation of their own

Escalation

Coadaptations become increasingly powerful, yet species are not any betteradapted because the selective landscape is constantly changing

This may sound familiar: it is Van Valen’s Red Queen Hypothesis: - running as fast as possible just to stay in the same place

An inherent feature of coevolution

We often think of “arms races” as occurring between predators and prey, or between parasites and hosts – this makes intuitive sense

But it is not really that different in mutualists – each mutualist will be best adaptedwhen it receives the maximum benefit while paying the minimal cost

Coevolutionary arms races

An arms race in a predator-prey interaction

Taricha granulosa newts have powerful tetrodotoxins(TTX) that are secreted as protection from predators

Thamnophis sirtalis garter snakes are the only major predator of this newt – they have evolved resistance to TTX

Escalation

Toxins produced by newts are hundreds of times more powerful that necessaryto kill any other predator (including humans), but snakes are resistant

Can we find evidence for coevolution?

Brodie et al. (2002) Evolution 56:2067-2082

Coevolutionary arms racesSnake populationsoutside of newt’s rangehave low resistance

Brodie et al. (2002) Evolution 56:2067-2082

Snake populationsvary in resistanceto newt toxins

A geographic mosaicwith two coevolutionary“hotspots”

Coevolutionary arms races

Brodie et al. (2002) Evolution 56:2067-2082

Snake resistance ispredicted by newttoxicity, as expectedif these species arecoevolving

An arms race in a predator-prey interaction

The extremely high toxicity of Taricha granulosa, which is hundreds of times more toxic than necessary for most predators, is a result of an escalating armsrace with one species, Thamnophis sirtalis

Evidence for coevolution

Local coadaptation

Snakes and newts are locally coadapted: - snakes have not evolved resistance in populations outside of the newt’s range - populations with high newt toxicity have high snake resistance

Snails and their castrating trematode parasites

In three separate studies, parasites were better able to infect snails from their ownpopulation than hosts from other populations – parasites are locally coadapted

Curt Lively’s research: http://www.indiana.edu/~curtweb/Research/local_adaptation.html

Inferring an arms race from fossils

Shells of fossil gastropods

Difficult to infer coadaptation from fossils because we can’t observe interactions

But we can use characteristics that reflect predator-prey interactions

When a shell is repairedfollowing a failed predationattempt, it leaves a clearpattern evident in fossils

The incidence of shell repair increases through time, suggesting predation isbecoming more intense

Gastropods “cement” themselves to the substrateas an adaptation againstpredators

The incidence of mobilegastropods that lack ameans of attachmentdecreases over time

Gastropods with thickenedor narrowed apertures are better able to survive predation events

The incidence of thickenedor narrowed aperturesincreases over time

Fossils and the Red Queen

Probability of extinction

The fossil record also supports another important theoretical point:

Probability of extinction is constant through the course of evolution

Why is this important?

It shows that evolution is not progressive – taxa that have been around longerhave not become “better adapted” and thus better able to avoid extinction

Supports the Red Queen model and implicates coevolution as a major force: Organisms have to keep running (evolving) just to stay in place (avoid extinction)

Coevolution and radiation

Haldane’s reply: “An inordinate fondness for beetles"

Biologist JBS Haldane was once asked by theologians: “What could one conclude about the Creator from a study of His creation?”

Why are beetles so speciose?

Over half of all beetles are phytophagous (feed on plants), and a large number ofthese herbivorous beetles feed on angiosperms (flowering plants)

Farrell (1998) hypothesized that specialization on different angiosperm species led to the radiation of beetle species

Farrell (1998) Science 281: 555-559

Coevolution and radiation

The increase in herbivorous beetle genera correlates with the exponential increase of angiosperms beginning in the Cretaceous

Radiation of angiosperms

Why are beetles so speciose?

Phytophagous beetles are a monophyletic group, but specialized feeding on angiosperms has evolved multiple times within phytophagous beetles

Beetles feed on:

CycadsConifersAngiosperms (dicots)Angiosperms (monocots)

(A) Curculionoidea (B) Chrysomeloidea

Farrell (1998) Science 281: 555-559

Many more beetle genera occur in clades that feed on angiosperms

Coevolution and radiation

Why are beetles so speciose?

Specialization on angiosperms leads to rapid beetle speciation via coevolution

Radiation of angiosperms

Evolutionary changes in plant host lead to incredible beetle radiations

It is important to note that this samepattern is observed in five different clades, indicating that the change inhost type is driving this pattern

Coevolution and radiation

Farrell (1998) Science 281: 555-559

Coevolution

Why is coevolution important?

We can simplify ecology as consisting of 2 types of interactions

1) Abiotic – interactions with temperature, light, nutrients, humidity, etc.

2) Biotic – interactions with other organisms

Coevolution occurs only as a direct result of biotic interactions

A simple question about the importance of coevolution:

If change in the physical environment ceased, would evolution come to a stop?