Transcript Escape-and-radiate coevolution

Evolution of plant-herbivore relationships
Photo G. Weiblen
Cospeciation resulting in congruent phylogenies.
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
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.
Escape and radiation concept: plants develop new defence [yellow, orange],
their speciation rate increases, herbivores develop counter-defence and colonize them
Futuyma & Agrawal, 2009, PNAS 106: 18054–18061
Evolution of plant defense traits and herbivore specificity
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 herbi vores,
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 wil l 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
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
Phyllobrotica beetles and Scutellaria hosts:
parallel (or sequential?) evolution
S. galericulata
P. quadrimaculata
Farrell & Mittter 1990
Tetraopes beetles and Asclepias hosts: an example of escape-and-radiate coevolution?
Farrell & Mitter 1998
Blepharida beetles on Bursera plants: secondary
chemistry explains multiple host colonizations
different secondary chemistry marked by different colour
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
Becerra 1997
Bursera phylogeny
Asclepias defense strategies: life history traits and phylogeny
A. californica
A. exaltata
A. asperula
Phenogram recognizing three defense strategies
based on 7 traits:
Distribution of defense strategies on Asclepias phylogeny
Agrawal & Fishbein, Ecology, 87 Suppl., 2006, S132–S149
A: soft leaves, many trichomes, high latex
B: tough leaves, low water content, medium latex
C: soft leaves, low latex, high cardenolides
Asclepias defense strategies: phylogenetically unstable
Agrawal & Fishbein, Ecology, 87 Suppl., 2006, S132–S149
Phylogenetic and physiological response
may not be necessarily the same
Asclepias syriaca
Latex and trichomes:
- no correlation within species (Asclepias syriaca)
- a positive correlation across 24 species of Asclepias
Agrawal and Fishbein 2006
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
Herbivore species
Many herbivores have polyphyletic diets generated by multiple host colonisations
Plant species
Swiss Alps: 231 most abundant plant species vs. all butterfly species
Pellissier et al. 2013, Ecology Letters
Where to find genuine plant - insect coevolution?
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
male
female
Fig inflorescence: flowers are hidden inside
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
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
butyric acids
salicylaldehyde
from salicin
monoterpene
iridoids
Termonia et al. 2001
Mass extinction (Cretaceous-Tertiary boundary): specialists die first
Labandeira et al. 2002 PNAS 99:2061
angiosperms
conifers
Cycadales
1 - 5: colonizations
of angiosperms
Beetles: high species
diversity associated
with feeding on
angiosperms
Farrell 1998
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
Nosil 2002
Generalist to Specialist
Specialist to Generalist
No. of mouthpart
classes
No. of insect
families
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?
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
Crescentia alata
Enterologium cyclocarpum
Similar role played by
forest elephants in Africa
Leaf-cutting ants:
an accident of evolution?
Atta nest
before
after