Evolution of plant-herbivore relationships

Photo G. Weiblen

Host-shift speciation resulting in congruent phylogenies, but with shorter branches in the parasite lineages

de Vienne et al. New Phytologist (2013)doi: 10.1111/nph.12150

Cospeciation resulting in congruent phylogenies.

Host-shift speciations, resulting in incongruent phylogenies.

de Vienne et al. New Phytologist (2013)doi: 10.1111/nph.12150

Evolution of insect-plant associations: by descent or colonization

plant

insect

Association by descent Association by colonisation

Sequential evolution: the evolution of herbivorous insects follows the evolution of plants while the plant evolution is not affected by herbivores.Coevolution:the evolution of plant lineages influences the evolution of herbivore lineages and vice versa

How the fig - wasp relationships evolved?

Coevolution: reciprocal evolutionary change in interacting species

Escape-and-radiate coevolution 1. Plants evolve by chance (via mutation, recombination) a new toxin/deterrent.2. New chemical leads to protection from herbivores.3. Protected plants enter a new adaptive zone, in which they are free to radiate.4. Herbivores evolve (via mutation, recombination) ways to deal with new toxin.5. Herbivores enter a new adaptive zone and are free to radiate.6. The cycle is repeated.

Futuyma & Agrawal, 2009, PNAS 106: 18054–18061

Escape and radiation concept: plants develop new defence [yellow, orange],their speciation rate increases, herbivores develop counter-defence and colonize them

If most herbivores are generalists, and only a subset of the plant species pool can defend or tolerate the dominant enemies, then plant species composition will shift to become dominated by those species that share these defence and tolerance traits. In this figure, green squares, red stars and orange circles represent different defence traits that confer tolerance of herbivory in plants within a community, and thin lines indicate a species has been eliminated from a community by the herbivore. If defence traits are conserved (a), heavy herbivore pressure will drive phylogenetic clustering within the community. For example, large mammalian herbivores consume a wide variety of plants, yet grasses are able to tolerate high herbivory pressure and in the presence of these large herbivores, quickly dominate communities. If herbivores are excluded, plant composition changes, and trees or forbs can take over (McNaughton 1985, Pringle et al. 2007). However, if such traits that confer tolerance or defence are convergent, generalist enemies will drive the phylogenetic community structure towards overdispersion (b). If specialists exert a large proportion effect on plant fitness within a community, this will result in strong patterns of density dependence (Janzen 1970, Connell 1971). This should increase local diversity by favouring rare species which can escape their natural enemies more often than more abundant species. Furthermore, if related plants have qualitatively similar defence strategies (trait conservatism) (c), strong Janzen–Connell regulation in a community could limit the co-occurrence of closely related species and promote the co-occurrence of distantly related species at neighbourhood scales, causing community phylogenetic overdispersion (Webb et al. 2006). In this figure, specialist enemies can eat

only plants from the pool that have similar defence traits, similar to Becerra (1997). (d) If plants defence traits are convergent, however, Janzen–Connell regulation by specialist enemies will promote random patterns in plant communit phhylogenetic structure.Cavender-Bares et al. Ecology Letters, (2009) 12: 693–715

Evolution of plant defense traits and herbivore specificity

Gall wasps (Cynipidae): second largest radiation of gallers, 1300 spp.

Most of species on woody plants, particularly oaks (a), species on herbaceous plants mostly on Asteraceae (b)

Phylogenetic conservatism in the position of galls on host plants

Cynipid gallers Andricus on oaks in Europe: evolutionary conservatism in gall type

inquilines do not induce their own galls, feed inside galls of other spp.

Host plants of gallers

P. quadrimaculata

S. galericulata

Phyllobrotica beetles and Scutellaria hosts: parallel (or sequential?) evolution

Farrell & Mittter 1990

Farrell & Mitter 1998

Tetraopes beetles and Asclepias hosts: an example of escape-and-radiate coevolution?

Becerra 1997

Blepharida beetles on Bursera plants: secondary chemistry explains multiple host colonizations

Host selection by beetles can be better explained by plant similarity in secondary metabolites than by plant phylogeny

Bursera phylogeny does not correspond with phylogeny of its beetles

Bursera phylogeny

different secondary chemistry marked by different colour

A. californica

A. exaltata

A. asperula

A: soft leaves, many trichomes, high latexB: tough leaves, low water content, medium latexC: soft leaves, low latex, high cardenolides

Asclepias defense strategies: life history traits and phylogeny

Phenogram recognizing three defense strategies based on 7 traits:

Distribution of defense strategies on Asclepias phylogeny

Agrawal & Fishbein, Ecology, 87 Suppl., 2006, S132–S149

Agrawal & Fishbein, Ecology, 87 Suppl., 2006, S132–S149

Asclepias defense strategies: phylogenetically unstable

Latex and trichomes: - no correlation within species (Asclepias syriaca) - a positive correlation across 24 species of Asclepias

Agrawal and Fishbein 2006

Phylogenetic and physiological response may not be necessarily the same

Asclepias syriaca

Herbivores feeding on latex-rich Asclepiadaceae - Apocynaceae colonize preferably other latex plant lineages

Number of colonization of plants from various orders by herbivores feeding on latex-rich Asclepiadaceae - Apocynaceae plants: insects retain their taste for latex

Many herbivore lineages retain broad preferences for certain plant lineages

Many herbivores have polyphyletic diets generated by multiple host colonisations

Plant species

Her

bivo

re s

peci

es

Pellissier et al. 2013, Ecology Letters

Swiss Alps: 231 most abundant plant species vs. all butterfly species

The plant - insect mutualisms where • the insect pollinates flowers • then oviposits to some of them so that the larval survival depends on successful pollination

Ficus - Agaonidae wasps

Yucca - Tegeticula moths (Yponomeutidae)

Trollius - Chiastocheta (Anthomyiidae) flies

Glochidium - Epicephala (Gracillariidae) moths

Where to find genuine plant - insect coevolution?

Fig inflorescence: flowers are hidden inside

male female

Ceratosolen wasps: Oviposition to fig flowers through stylus

Yucca plants - Tegeticula moths

Epicephala sp. (Gracillariidae) and Glochidium (Euphorbiaceae)

Kato et al. 2003. PNAS 100:5264

Termonia et al. 2001

Is narrow host specialization an evolutionary dead-end? Specialized Chrysomela beetles dependent for anti-predator defence on metabolites

from their hosts develop a new chemical defense

salicylaldehyde from salicin

monoterpene iridoids

butyric acids

Mass extinction (Cretaceous-Tertiary boundary): specialists die first

Labandeira et al. 2002 PNAS 99:2061

angiosperms

Cycadales

conifers

1 - 5: colonizations of angiosperms

Farrell 1998

Beetles: high species diversity associated

with feeding on angiosperms

Host specificity: is narrow specialization determined by speciation dynamics?

Transition from a generalist to a specialist is more likely than reverse transition

0 0.5 1

Proportion of speciation events

Generalist to Specialist Specialist to GeneralistNosil 2002

While number of insect families is steadily increasing through evolution, there has not been any major inovation in mouthparts dor almost 100 million years:

has everything been already invented?

No. of mouthpart classes

No. of insect families

Extinction of large mammalian herbivores in past 130,000 years:what are ecological consequences?

What were ecological roles or recently extinct megafauna?

Janzen & Martin (1982) NEOTROPICAL ANACHRONISMS: The Fruits the Gomphoteres Ate

Large recently extinct fauna, such as gomphoteres in S. America,could be important consumers and dispersal agents of large fruits

Similar role played by forest elephants in Africa

Crescentia alata Enterologium cyclocarpum

Leaf-cutting ants: an accident of evolution?

before

after

Atta nest