Coevolution of mutualisms
Coevolution (strictly):
Reciprocal evolutionary change of interacting species
Mutualism:
Individuals of two species interact with the result that both benefit.
Contrast with “symbiosis”, which is any long-term intimate
relationship between members of two species, whether
mutualistic, parasitic, commensal, etc.
Examples of mutualisms
Symbiotic mutualisms:
Ÿ micorrhizal associations between plants and fungi
Ÿ corals and photosynthetic dinoflagellates
Ÿ lichens (algae and fungi)
Visitor mutualisms:
Ÿ plant-pollinator
Ÿ plants and frugivores
Ÿ cleaner fish and clients
For at least some systems, the extent to which the
associations are truly mutualistic varies with environment.
Darwin’s hypothesis for the coevolution of
flower length and pollinator tongue length
The orchid, Angraecum sesquipedale
Darwin (1859)
On the Origin of Species
http://www.pbase.com/bjramsay/image/90924215
The predicted long-tongue pollinator was later found
The orchid, Angraecum sesquipedale
http://www.pbase.com/bjramsay/image/90924215
Xanthopan morganii praedicta
http://www.flickr.com/photos/kqedquest/3256354461/
Coevolution of flower length/tongue length
A recently-described nectar bat
Anoura fistulata, discovered in the
cloud forests of the Andes of
Ecuador, can extend its tongue twice
as far as those of related bats and is
the sole pollinator of a plant with
corolla tubes of matching length.
Muchhala (2006)
a, Anoura fistulata feeding from a test tube filled with sugared water; its tongue (pink) can extend to
150% of body length. b, Maximum tongue extension and palate length for 11 species of
glossophagine nectar bat. Anoura fistulata is an outlier. c, Ventral view, showing tongue (pink),
glossal tube and tongue retractor muscle (blue).
Darwin’s hypothesis
Whittall & Hodges 2007
Experimental test: shortening of spur length
% pollinia removed (o ) and
stigmas pollinated (o)
Experimental shortening of floral tubes has a
strong negative effect on male (pollinia removal,
black bars) and female (stigma pollen receipt,
open bars) components of fitness in P. biflora
(top) and P. chlorantha (bottom).
Nilsson (1988)
Sphinx ligustri
http://outdoors.webshots.com/pho
to/2441357260026021334gtQzHq
Floral tube length (mm)
Platanthera bifolia
http://commons.wikimedia.org/wiki/Template:Potd/2008-08
Alternative hypothesis, also coevolutionary
Reduced pollen waste
Simulation model:
When long- and short-tongued pollinators are
present and compete for nectar, coexisting plant
species can diverge in corolla tube depth, because
this increases the proportion of pollen grains that
lands on flowers of the right species.
Starting with two plant and two pollinator species, all
of them having the same distribution of tongue
length or corolla-tube depth, variability in corollatube depth leads to divergence in tongue length,
provided that increasing tongue length is not equally
costly for both species. Once the two pollinator
species differ in tongue length, divergence in
corolla-tube depth between the two plant species
ensues.
Alternative hypothesis, not coevolutionary
Whi$all & Hodges (2007) Mutualism as mutual exploitation
There is no evidence that interspecific mutualists are
“altruistic”. There is a potential for conflicts of interest between
mutualists.
Selection may even ultimately result in one party overexploiting the other, and thus change the mutualism to a hostparasite or predator-prey interaction.
What keeps a mutualism stable over the long term? A
prevalent idea is that stable mutualisms involve the evolution
of “sanctions”, mechanisms that prevent the evolution of
overexploitation.
“Sanctions” may evolve in response to mutual exploitation, or
they may evolve in response to other factors, and may even
predate the mutualism.
Yucca - yucca moth mutualism
Yucca species are completely dependent on the yucca
moth Tegiticula for pollination. The moths eat
developing seeds in the fruits.
The female moth emerges, gathers pollen from the
anthers of the yucca (specialized mouthparts). When
ready to lay eggs she flies to a yucca flower, make an
incision into an ovary (piercing ovipositor), lays an egg,
then pollinates the stigma, ensuring development of the
ovaries. Repeats several times within a flower.
The moth larvae feed on the developing seeds. Only a
few seeds are so destroyed within a flower. At maturity,
the larvae leave the seed capsule, drop to the ground,
and pupate.
http://www.cals.ncsu.edu/course/ent525/close/Ostendorff.html
http://www.opsu.edu/UnivSchools/ScienceMathNurs/PlantsGrassh/plants/pasturefiles/pasture30.html
Flowers with many eggs/scars are abcissed
These are thought to represent a
plant “sanction”
Graph shows proportion of retained
flowers for each Tegeticula egg and
scar number category. Dashed lines
indicate grand mean retention in the
entire sample.
Pellmyr and Huth (1994)
The evolution of non-mutualistic yucca moths
Pellmyr, Leebens-Mack and Huth (1996)
Timing of egg-laying by “cheaters”
“Early cheaters”:
After period of abcission
is over
There are also “late cheaters”:
Have very long ovipositor and cut
into full-sized fruits 1-2 weeks later.
http://www.uoregon.edu/~udovic/yucca_photos.html
High seed destruction by “cheaters”
Test of the presence of “sanctions”
in legume-rhizobium mutualism
Rhizobia bacteria fix N2 within the root
nodules of their host legume plants (soybean).
N2 fixation supplies nitrogen needed for plant
growth and photosynthesis. But N2 fixation (at
rates that greatly exceed the nitrogen needs of
rhizobia) is energetically costly to the bacteria.
Rhizobia strains that fix little or no N2 after they
form root nodules on legumes are common in
some soils. Why haven’t these “cheats”
completely displaced cooperators?
Rhizobia experimentally forced to “cheat” by
replacing air (N2:O2, 80:20) with a gas mixture
(Ar:O2, 80:20) containing only traces (1% of
normal) of N2. As predicted by the sanctions
hypothesis, preventing N2 fixation led to a
significant decrease in their fitness, as though
plant is sanctioning.
Kiers et al (2003)
Tests of the presence of “sanctions”
in plant - arbuscular mycorrhizal fungus mutualism
Arbuscular mycorrhizal fungi provide their host plants with mineral nutrients
and other benefits such as protection against biotic (pathogens and
herbivores) and abiotic (e.g., drought) stresses
Fungal hypha
Plant root cell
Arbuscules
Roots
Nutrient exchange and reciprocal protection
Selosse & Rousset (2011) Nature
Carbon
Carbon
Nitrogen
Amino acids
(arginine)
Nitrogen
(NH4+, NO3–)
Phosphorus
Polyphosphates
Inorganic
phosphorus
Tests of the presence of “sanctions”
in plant - arbuscular mycorrhizal fungus mutualism
14C
sucrose
Root
14
Fungal Fungal
hyphae hyphae
C allocation to hyphae
(% of total transferred)
100
Fungal
hyphae
Root
0 mM
sucrose
Root
5 or 25
mM
Kiers et al. (2011) Nature
*
60
40
20
0
0 µM 700 µM
Phosphate supply to fungal compartment
integrated into total PolyP
(dpm mg-1 dry weight)
33Phosphate
*
0 µM 35 µM
35 or 700 M P
33P
0 MP
80
4000
*
3000
2000
1000
0
ns
0 mM 5 mM
0 mM 25 mM
Sucrose supply to root compartment
Experimenters inoculated a single root
(Medicago, a legume) with two different
fungi, which were allowed to grow into
separate environmental compartments.
Then, they enforced each fungus to be
cooperative (or not) by adding some (or
no) phosphorus to its own compartment.
The more cooperative fungus received
more carbon from root cells.
They manipulated plant cooperation by
exposing roots to variable amounts of
sucrose as a carbon source (which
Glomeromycetes only use after plants
hydrolyze it to glucose). The fungi made
more phosphorus available to the roots
that offered more carbon.
Thus, both partners “choose” more
rewarding symbionts, and control
cooperation based on bidirectional
exchange of nutrients.