Plant-animal interactions and coevolutionary syndromes

I. Coevolution

A. Coevolution. A change in one species acts as a new selective force on another species, and counteradaptation of the second species, in turn, affects selection of individuals in the first species.

This has been studied most extensively in predator-prey relationships and in symbiosis.

Often what appears to be coevolution may actually result from interactions with many species (not just the obvious two) where it is difficult to determine importance of various selective forces. This has been called diffuse coevolution.

B. Examples:

1. The association between passionflower vines and the butterfly species is a classic example of coevolution acting on a complex of species.

  • The vines produce toxic chemicals to reduce damage to young shoots and leaves by the larvae of these herbivorous insects.
  • Butterfly larvae of can tolerate these chemicals due to digestive enzymes which break down the toxic chemicals (a counteradaptation).
  • Females of some species avoid laying eggs (which are bright yellow) on leaves where other yellow egg clusters have been laid; reduces intraspecific competition on individual leaves.
  • Some species of passionflowers develop large, yellow nectaries which resemble eggs; an adaptation that may divert egg-laying butterflies to other plants.
  • These nectaries, as well as smaller ones, also attract ants and wasps which prey on butterfly eggs and larvae.

2. Monarch and milkweed species complex (see work by Lincoln Brower)

This butterfly acquires a cardiac glycoside from members of the genus Asclepias. Because of their milky sap, these are commonly referred to as milkweed plants. The plants produce this toxin as a defense against herbivory, but the Monarch has the ability to sequester the toxin in fatty tissues so that it makes the butterfly unpalatable while not poisoning the butterfly.

The Monarch has the longest regular migration of any insect. "Two migratory populations of the monarch butterfly occur in North America. The western population breeds west of the Rocky Mountains during the spring and summer and migrates to numerous overwintering sites, mainly along the California Coast. The second, much larger, eastern population breeds over several generations east of the Rocky Mountains and in the autumn migrates southwards to overwintering sites in the high peaks of the TransverseNeovolcanic Belt, south of the Tropic of Cancer in central Mexico. The autumn migration has been assumed to occur only in a southwesterly direction with some wind drift eastwards, but probably involves a gradual shifting from south to west as proposed in the figure above. Migration across the Gulf of Mexico and through Florida and Cuba to Guatemala remains hypothetical." (Figure and text from Brower, L.P. 1997. J. Exp Biol. )

3. Ehrlich and Raven: Generalized reciprocal evolutionary relationship between butterflies and their food plants. They coined the term "evolutionary arms race." Reciprocity of selection and adaptation through evolutionary time is central to this concept.

Ehrlich, P. R. & P. H. Raven. 1965. Butterflies and plants: a study in coevolution. Evolution 18:586-608.
  • Paul Ehrlich (co-author of The Population Bomb) and Peter Raven (currently the director of the Missouri Botanical Garden) published this landmark paper. They examined coevolution between butterflies and plants. Herbivory. Defined coevolution as interaction between two major groups of organisms with a close and evident ecological relationship.
  • Evaluation of the kinds of plants fed upon by the larvae of certain butterflies leads to the conclusion that secondary plant substances play the leading role in determining patterns of utilization.
  • In turn, butterflies have evolved the ability to use these substances.

Reciprocal coevolutionary relationship between butterfy species and their food plants.

Note that recent work on beetles shows that they have followed a similar evolutionary trajectory, and perhaps may be by far the best example of reciprocal coevolution.

II. Herbivory and plant defenses

Definition : eating of any part of a plant

A. Classification of defenses

    Biochemical origin:

    All are sugar derivatives (indeed all plant products start out at sugars)
    Plus lipids ->     Steroids, Alkaloids, Terpenoids
    Plus Amino Acid ->     Alkaloids, Coumarins, Flavenoids, Tannins, Toxic Amino Acids

B. Quantitative vs qualitative: a dichotomy

 Quantitative Qualitative
Complex, large molecules small, simple molecules
High percentage of plant dry weight <2% of plant dry weight
Permanent tissues of the plant new tissues, reproductive tissue, meristem
perennial and long lived plants short-lived plants, annuals
present in primitive groups advanced groups

Examples:

 Quantitative Qualitative
cellulose alkaloids (e.g., nicotine, caffiene, THC, etc.)
hemicellulose toxic amino acids
lignin cyanogens
tannins glucosinolates
silica protease inhibitor
spines and thorns terpenoids


C. Constitutive vs inducible defenses

    1. Constitutive: permanent protection - reduce digestibility & toxins.

    2. Inducible: Protease inhibitors are elaborated in response to herbivore attack. Sometimes this is difficult to prove, but many other nondefensive compounds are known to be inducible. These include wound hormones (e.g., >1% of soluble protein in potatoes and tomatoes is dedicated to wound repair). Recently, alkaloid and coumarin synthesis have been shown to be inducible.

D. Diversity

  • There are many, many more compounds known than have been studied.
  • Each plant has > 1 defense. These may vary during different lifestages - e.g., protection for a seed is likely to be different from the protection used in the developing seedling, which is likely to be different from the protection used in the mature adult.

III. Mechanisms of herbivory

Note that plants are a source of carbon and nitrogen for herbivores. The nitrogen content of plant material is a strong correlate of herbivory.

A. Introduction to digestion:

  • Teeth - fragmentation
  • Avoidance - well developed taste
  • Breakdown of cellulose is accomplished via an expanded foregut or hindgut and requires symbionts with the ability to break the 1,4 subunit linkages in carbohydrates.

B. Microbial farms

    1. Ruminants - cellulose and a diverse array of hydrocarbons are broken down to smaller biochemical units - large volume retention and slow transit time.

    2. Cecal digesters - rapid transit time, and large volume throughput. Examples include elephants, horses, & howler monkeys.

    3. Foregut - Colobus monkeys - intermediate to the other two forms - determinants are fluid volume and retention time

4. Insects -Why is this caterpillar so flashy?

a. Intracellular - mycetocytes - specialized cells that break cellulose bonds.

b. Extracellular - alimentary canal protozoans

c. Fungal gardens - termites, bark beetles, and leaf cutter ants (large volume and high retention time, but external to the organism). Many ants here in Florida are fungal gardeners.

d. Inoculation by parent is necessary for the next generation to acquire the symbiont necessary for the fermentative digestion of cellulose.

C. Detoxification

    1. P450 cytochrome. (older term = Mixed Function Oxidases) (coded for by the P450 cytochrome part of the herbivore genome)

    a. Catalyze oxidative reactions - produce polar products that are soluble and thus easily bound and excreted.

    b. Nonspecific and broad-spectrum

    c. Induced by exposure to novel compounds

    2. Generalists are better at neutralizing novel toxins


Spider monkeys are generalist fruit eaters. They roam widely through the canopy of tropical forests, and opportunistically harvest fruit.


Howler monkeys are generalist leaf eaters. They show considerable ability to detoxify novel compounds, and they exhibit intraspecific territoriality once they begin to harvest the leaves from a given tree. Their volume of food consumption must be considerably higher that that of Spider Monkeys. Why?

Which of these two monkeys has tastier meat ? Why ?

3. Humans eat a wide variety of cyanogenic foods, including maize, paddy rice, sweet potato, unrefined sugar, oats, wheat, barley, apples, millet, and peanuts. Apparently, we detoxify these with P450 generated oxidases. It seems clear that cyanogens are used to discourage predators.

D. Use as Food

Amino acid in a bean : L-canavanine - 12% of bean wt. in fruit of a tropical legume (in this case, a tree). The beetle uses this amino acid as a nitrogen source, although it would be lethal to most other herbivores.

E. Sequester

F. Choice and avoidance: the concept of phagy

Polyphagy->oligophagy->monophagy: gradient toward fewer and more specific countermeasures

Polyphagy: taste induces P450 activity

Polyphagy compared to monophagy: investment in defense is higher in the former, whereas finding food may be a problem for the latter.

 

IV. Ecological correlates of quantitative and qualitative defenses.

Defense is a plant's ability to protect itself : complex function of diversity and quantity chemicals found in leaf material, as well as physical defenses such as spines.

A. Feeny : Apparency Theory is another dichotomy, but in this idea plant traits are expressed over evolutionary time.

    May Berenbaum (University of Illinois) - highest concentration of highly toxic compounds in spring and early successional species.

    Phillis D. Coley (University of Utah) - mixed evidence - pioneer and persistent trees - found increased concentration of tannins in leaves of both stages of succession.

Unapparent Plants Apparent Plants
few herbivores many herbivores
strong selection on plants diffuse selection on plants
strong selection on animals diffuse selection on animals
coevolution - strong with few interacting genomes many genomes interacting
defenses: qualitative, highly toxic defenses: structural, quantitative, mainly deterrent
defense is against the "generalist" herbivore defense is against both "generalist" and "specialist"

B. Feeding Specificity

    1. Fine grained

    Fine grained - many choices
    Coarse grained - 1 choice of source over entire lifetime - thus can adjust countermeasures to a narrow range of defenses

    a. Herbvores of Serengeti:

  • Larger animals eat more fiber because they have larger stomachs and thus a tendency for longer retention time and fermentative digestion.
  • Large animals are less selective with respect to plant forage species.

    b. Leaf cutter ants (Azteca)

  • Ants use leaf material to culture a fungal garden, which is then used for food.
  • Human applications: Rejection of specific leaves can often be traced to a single chemical and this chemical selects against generalist leaf cutter ants. If the chemical has antifungal properties, it may be useful to us. Thus the leaf cutter ant is type of bioassay.
  • Tropical trees often contain many simple toxins, which is evidence against Feeny's argument of evolutionary apparency.

    Point: Plants have mixed "strategies" of defense

2. Coarse grained - life on 1 host

  • The tropical Morpho butterfly was used during the 1800s as a source of pigment for US currency (this may be an urban "bio" myth). Note the missing section of the back of the wings indicating that this individual was almost lunch for a bird.
  • In nature, blue is usually a structural color, meaning that it comes from the refraction of light on the scales of the butterfly's wings. Regardless of whether or not this butterfly uses refraction or an actual pigment, inclusion of the color in priniting of legal tender would make the money extremely difficult to duplicate.
a. Butterflys specialize on unapparent plants.

This is predicted because

1. ecological requirement of living on 1 plant during the insects entire life
2. small body size

Thus mother butterflys are selected to find the best host when it comes time to lay her eggs.

b. Feeding Specialization Hypothesis:

  • Polyphagous herbivores handle chemicals less efficiently than do oligophagous and monophagous herbivores.
  • Scriber (1983) measured efficiency in terms of growth rate.

V. Evidence for coevolution in herbivory systems

A. Ehrlich and Raven

  • Their paper placed coevolution in the context of a community of organisms.
  • Many examples of chemical "dependency" and species-specific associations are assumed, but not proven; many other examples are based on spotty records; taxonomic affinities of many of the butterfly families are poorly known. Hmmm, do these problems invalidate their proposal?
  • Most important feature : reciprocal evolution (also called coupled character evolution).

B. Berenbaum: 4 points in favor of coevolution argument :

1. Mutation and recombination in angiosperms produce novel secondary substances.
2. By chance, these substances alter the suitability of plant as food
3. Plants are released from predation and enter a new adaptive zone
4. Insects evolve resistance and enter a new adaptive zone

Coumarins in the Umbelliferae are a good circumstantial case in point.

C. Coevolution revisited

A second definition by Roughgarden: The simultaneous evolution of ecologically interacting populations.

Considerations:

1. Generation time of host and herbivore: determines the opportunity for coevolution.

2. Gene for gene evolution - This is coupled character evolution in which single-gene (Mendelian) traits change quickly. For example, MFOs can be specific for a particular compound and may act in a fashion that is biochemically the reverse of the enzymatic process that made the compound in the plant. Indeed, Berenbaum has speculated that the detoxifying compound and the toxin may in fact be coded for by the same part of the genome in the animal and the plant, respectively.

3. Selection on polygenic traits. It is more difficult for coevolution to occur when selection involves multiple traist. Thus adaptation by some butterflies may require a long time.

D. Schemsky 1983

Doug Schemsky (University of Washington) has argued that it is a fallacy that all mutualisms are reciprocally coevolved. He agreed with the concept of simultaneous evolution of interacting populations (Roughgarden's definition); but he also noted that this definition ignores the fact that reciprocal interactions can be sequential, and that the selection can operating at the level of particular traits.

1. Coupled Character Evolution: selective effects between taxa are present at the level of individuals and characters. - i.e. individuals with a specific characters are selected as a consequence of individuals of another species with a specific character.

e.g., Plants with yellow corollas select for bees which prefer yellow corollas by producing more nectar.

2. Uncoupled Character Evolution: individual selection is divorced from any reciprocity in the characters driving the selection.

e.g., plants with yellow corollas select for bees which are long distance dispersers of the pollen, but which may not necessarily prefer yellow corolla plants. Bees which are long distance dispersers select flowers which produce large amounts of nectar, but may be of any color. Thus yellow flowers end up producing large quantities of nectar, and bees end up visiting yellow flowers and carrying pollen long distances as a coincidence.

VI. Pollination systems

A. Most bee-pollinated plants are pollinated by a few polylectic bees.

Many bee taxa which exhibit host-plant specialization are not the primary pollinators of their hosts. It is a selective advantage for most angiosperms (flowering plants) to have more than one pollinator.

The high diversity of insect visitors to any particular plant species probably overrides the selective effects of particular plant specialists. Despite this, there are a large number of pollen specialists (e.g., orchids and euglossine bees), which implies speciation. Why?

1. Host-switch hypothesis: Reproductive isolation ensues after an incipient (bee) species switches host. This may require few genetic changes if that plant is also the mating site.

2. Fragmentation hypothesis: Widely foraging species is fragmented during years when the preferred pollen source is absent.

Summary:

(1) Subdivided population structure in the plants (hypothesis 1 & 2) could lead to specific selective pressures on pollination characteristics that influence pollen flow between subpopulations. Where progeny fitness of the plant is correlated with pollen flow distances, we expect strong selection on floral characters that may attract specific pollinators. These characters could coevolve with pollinator preferences.

(2) The orchids deserve special attention because (1) species are scarce and widely dispersed, and (2) they use sex as a means of attracting pollinators. Many orchid species are designed to momentarily trap a euglossine bee as it seeks nectar. The entrapment results in pollen collected previously from a conspecific orchid being transferred to the stigmatic parts of the plant. Note that euglossine bees are solitary bees, rather than social bees, and that the orchids attract them by in some way (odor and morphology) resembling the sign-stimulus of the opposite sex. This is especially true for foraging male bees.

B. Birds and mammals as pollinators.

e.g., hummingbirds, sunbirds, bats.

Most vertebrate pollinators will visit a variety of plants (often within a guild or specific morpho-type), but they are rarely as highly specialized as insect pollinators. Note that there is often (but not always) an abundance of species with tubular corollas that may be visited by a single species of hummingbird.
 

VII. Seed dispersal systems

Alice the tapir was (sadly) an important seed dispersal agent on Barro Colorado Island, Panama. Tapirs are important dispersers of seeds that reach the forest floor. Some of these seeds are digested by Alice and her kin, but most are passed through the gut, resulting in acid scarification of the seed coat. This, in turn, makes the seed capable of imbibing water and germinating. Tapirs are cecal digesters. Toucans are important dispersers of fruit in most Neotropical forests.

Unlike the temperate zone, there is virtually no seed bank in the soils of the tropics. This is because tropical seeds either germinate or are consumed by seed predators (often beetles) within a short time. The dormancy period imposed by winter conditions allows many temperate zone seeds to escape this predation.

Janzen, D.H. 1970. Herbivores and the number of tree species in tropical forest. American Naturalist 104: 501-528.

Tropical trees have 3 life history characteristics:

1. Low density of adults of each species

2. Long distances between conspecific adults

3. Coexist with a high number of tree species

Hypothesis: these characteristics are the result of seed predation - Any event that increases the efficiency of the predators at eating seeds and seedlings of a given species will lead to a reduction in population density of the adults of that species or increased distance between new adults and their parents.

Thus, in the tropics, selection should favor trees which get their fruits dispersed far.

Efficiency (quantity) and Quality (percent which arrive at appropriate site) are two factors that cannot be controlled. Thus, co-evolution is very loose in this system, and in no way a gene-for-gene interation.

Seed dispersal systems are rarely specialized because:

1. Plants do not provide rewards insuring site-specific dispersal.

2. There may be small variation among dispersal agents in the quality of dispersal.

3. Unpredictability of germination safe sites.

4. Advantages to the tree of utilizing a diversity of dispersal agents - if fruits are designed for only one agent, and it goes extinct, then the fitness of the tree species decreases.

VIII. Ant-plant systems

A. Ants and their acacia trees.

Dan Janzen (currently at the University of Pennsylvania) won the Crafoord award (awarded by the same group that awards the Nobel Prize) for this work on ant-plant coevolution. This was a landmark study that defined the possibilities of coevolution on a grand scale.

Janzen, D. H. 1966. Coevolution of mutualism between ants and acacias in Central America. Evolution 20: 249-275.

plants: Acacia; ants: Pseudomyrmex.

  • The ant is dependent upon the acacia for food and domicile,
  • The acacia is dependent upon on the ant for protection from phytophagous insects and neighboring plants.

Characteristics of swollen-thorn acacias:

1. Enlarged stipular thorns normally tenanted by ants,


2. Enlarged extra-foliar nectaries,

3. Modified leaflet tips called Beltian Bodies (eaten by ants as a protein source),

4. Year round leaf production and maintenance even in areas with a strong dry season when most other trees are deciduous

Ants:

Obligate ants: there are no Pseudomyrmex that are mutualistic with both an acacia and another species of plant.

There are 6 to 8 species of ants that are obligate on Acacia in Central America

Workers attack any other insects on the acacia and normally are successful in driving them off by biting and stinging.

Ants also attack plants which touch the swollen thorn acacia.

Acacia:

Thus the acacia grows in a cylindrical space free of other plants and protected from fire.

During early growth, seedling progressively produces larger thorns, more leaflets with Beltian bodies, and larger foliar nectaries until it has these morphological properties of a mature acacia.

Once occupied, the acacia grows very rapidly as an emergent or canopy member during the first six to eight years of undisturbed regenerating second-growth vegetation. Unoccupied swollen-thorn acacias show severe defoliation and loss of growing shoot tips. It is then heavily shaded and vines may overtop it.

Conclusion: "The obligate acacia-ant may thus be regarded as a multipurpose characteristic of the acacia, maintained by swollen thorns, Beltian bodies, enlarged extra-foliar nectaries, and year-round leaf production"

B. The "singing" caterpillars and attack ants

A variation on the ant-acacia theme. P. J. DeVries (University of Oregon). A remarkable three-way interaction between a plant species, the herbivorous larvae of a butterfly, and plant-tending ants.

DeVries, P. J. 1990. Enhancement of symbioses between butterfly caterpillars and ants by vibrational communication. Science 248: 1104-1106.

IX. Mimicry and crypsis

Mimicry is a phenomenon in which a mimic bears a superficial resemblance to another species, the model.

Occurs in both predatory and prey species.

Defensive mimicry in prey usually involves aposematic models, but crypsis is also common as in the katydids shown above.

This eyelash viper is extremely cryptic against the lichen-covered bark of tropical trees. The name derives from the skin above the eyes, which looks like an eyelash. Humans walking by are often struck in the face, and thus this snake is considered quite deadly. A few years ago, I had a dramatic encounter with this species while moving a branch out of my way on the trail.


What are these?

Batesian mimicry: A palatable species mimics an unpalatable model.

The mimic must be much less abundant than the model to be effective since predators must learn the coloration indicates a bad or harmful food item. - Viceroy Butterfly (?), Rosey Boa.

The Viceroy Butterfly has long been consider to be a Batesian Mimic of the Monarch butterfly. Ritland and Brower in Nature (1991, 350: 497-498) present experimental data that the Viceroy is also unpalatable and should therefore be considered a Müllerian mimic. The selective regime necessary for each form of mimicry is very different.

Müllerian mimicry: Two or more unpalatable species resemble each other, e.g., Coral snakes and their mimics.

How did aposematic coloration evolve? Kin selection may be an answer - see your text.

Closely related kin would gain additional advantage since predators learn more quickly to avoid prey with this coloration.

Aggressive mimicry: (1) Predators also use mimicry to lure prey, or, (2) dangerous predator mimics a benign species in order to avoid alarming prey.

The tongue of snapping turtles resembles a wiggling worm which attracts small fish into capture range.

Eyespots on a tropical moth. Is this "sign-stimulus" (a stereotypic morphology or behavior that produces a highly predictable response by the observer) also an example of mimicry?