SCRP 2009
My research
examines the pollination biology and population genetics of Joshua trees (Yucca
brevifolia). If
youÕre not familiar with Joshua trees, they are large, woody monocots (the group
of plants that includes grasses, orchids, and palm trees) that are endemic to
the Mojave Desert region of California, Arizona and Nevada. Joshua trees are
known for their comical (or ugly, depending on your outlook) appearance, and
for their remarkable pollination biology (see below). John C. Fremont, an early
American explorer described them as ÒThe most repulsive tree in the vegetable
KingdomÓ. Later, Mormon settlers saw in their silhouette the figure of the
prophet Joshua, pointing the way to the Promised Land.
Students
working in my lab will work on projects related to one of two aspects of the
biology of Joshua trees. One project, which is currently fairly well developed,
looks at the pollination biology of these remarkable plants. The second project,
which is still in early stages of development, looks at the effects of global
warming on population growth rates. Below, IÕve provided detailed information
about these two projects, along with relevant references and citations, and
some ideas for questions that could be answered in student projects. Students
interested in applying to work in my lab should read the project descriptions
below, and the descriptions of potential student projects.
When
submitting their SCRP application, students should explain in a 3-5 page
essay (as described
on the SCRP
webpage) their ideas for how they might answer some of questions
identified in the project description (below). This essay should do two things:
1. It should present a coherent plan for how student research could address the
question, and 2. It should show that the applicant has done background reading
and research.
Background reading could include reading some of the references listed here,
but should also include other relevant research articles from the primary
literature. These articles might be examples of how other scientists have
tackled similar problems, or general articles about the natural history of the
system, or the theory behind the statistics and experimental design. Of course,
it will be challenging to put together a clear research proposal for a system
that students have only recently read about. The main things that I will be
looking for in reviewing student application are the ability to think clearly
about the problems, and that the applicants have taken some initiative to learn
about the systems and relevant concepts. I also encourage prospective SCRP
students to meet with me before submitting their application to discuss their
ideas.
Joshua Tree Pollination Biology
Joshua
trees (Yucca brevifolia), like all yuccas, are pollinated exclusively by highly specialized
yucca moths. The moths, in turn, lay their eggs exclusively on the flowers of
the Joshua tree, and as the flower develops into a ripening fruit, the mothÕs
larvae feed on the developing seeds. To ensure that the flower will develop and
provide food for her offspring, the female yucca moth deliberately deposits a
load of pollen directly onto the flowerÕs stigmatic surface using specialized,
uniquely derived, tentacle-like mouthparts (Pellmyr 2003). The interaction between yuccas and
yucca moths is therefore the archetypical example of an obligate pollination
mutualism, one which Darwin called Òthe most remarkable pollination system ever
describedÓ (Darwin 1874).
Within this
system, there is thought to be strong reciprocal natural selection
(coevolution) promoting phenotype matching between Joshua trees and their
pollinators. Across species, there is a strong, statistically significant
correlation between the length of the female mothÕs ovipositor (a blade-like
appendage used to cut into flowers when laying eggs) and the thickness of the
flowerÕs ovary wall at the site of oviposition. Likewise, there are strong
functional constraints acting on both moth and pollinator features: the mothÕs
ovipositor must be long enough to reach ovules within the flower, but an
ovipositor that is too long may injure the developing flower, which can prompt
flower to die along with the mothÕs larvae (Marr and Pellmyr 2003). (See Figure 1)
In the
Joshua tree system specifically, recent work revealed that across its range Y.
brevifolia is
pollinated by two distinct, parapatrically distributed moths, Tegeticula
synthetica Riley in
the west, and T. antithetica Pellmyr in the east (Pellmyr and Segraves 2003). These two moths differ
significantly in overall body size, and in the size of the female ovipositor (Pellmyr and Segraves 2003). Recent work has shown that Joshua
trees pollinated by the different moth species differ significantly in overall
floral and vegetative morphology, and differ more than any other feature in the
length of the floral stylar canal – the path through which the female
yucca moth inserts her ovipositor during oviposition (Godsoe et al. 2008). These patterns suggest that floral
style length and moth ovipositor length may experience reciprocal natural
selection (coevolution in the strict sense) favoring phenotype matching.
One way to
test his hypothesis would be to compare the performance of moths of a given
ovipositor length on flowers that differ in style length using a reciprocal
transplant experiment, but to do so would require moving moths between different
populations, keeping the moths alive during transport, and forcing them to
interact with foreign trees. These factors potentially make testing this
hypothesis very challenging. However, the recent discovery of a ~4 km-wide
contact zone where the two species of yucca moth co-occur in Tikaboo Valley,
Nevada (Smith et al. 2008) now makes it possible to address
this question using a Ônatural experimentÕ. Contact zones like that in Tikaboo
Valley have been used in other pollination systems to study the role of natural
selection and host preference in maintaining species boundaries (Fulton and Hodges 1999; Grant 1952;
Hodges and Arnold 1994), but such an approach has not
previously been used in an obligate pollination mutualism.
Within
Tikaboo Valley, trees with different pollinator-associated morphotypes occur side-by-side,
along with some trees that appear to be intermediate between the two types, and
there is greater variation in both style length and ovipositor length than in
any other population. Although moths of both species have been collected on
each of the tree morphotypes in the zone of sympatry, it is unclear whether
female moths show a preference in oviposition for trees whose floral morphology
matches their ovipositor. If reciprocal natural selection favors phenotype
matching in this system, then moths ovipositing on the ÒwrongÓ tree type should
have reduced fitness in terms of offspring that survive to adulthood.
We can
begin to address some of the questions by measuring how often moths move
between the two tree types in the contact zone, and how often the moths
successfully lay eggs on each of the two trees. By attaching plastic cards
coated in glue to receptive flowers we can trap moths as they visit the trees,
and then determine how often each species visit the different tree types. (See
Figure 2). Likewise, we can get a rough idea about how often the two moths oviposit
into the Òwrong flowersÓ by collecting larvae as they emerge from fruits.
Although the larvae of the two species are essentially indistinguishable in
appearance, we can compare mitochondrial DNA, as well as regions of highly
variable DNA called microsatellites, to identify the larvae to species.
My
colleagues at the University of Idaho and I completed an experiment like this
in 2007, with the following results:
A. Moth visitation rates |
|
||
|
Moth species (forewing length) |
|
|
Tree Type |
T. antithetica |
T. synthetica |
· |
Eastern |
10 |
3 |
13 |
Western |
22 |
23 |
45 |
· |
32 |
26 |
58 |
|
|
|
|
B. Larval emergence rates |
|
|
|
|
Larval mitotype |
|
|
Tree Type |
T. antithetica |
T. synthetica |
· |
Eastern |
296 |
3 |
299 |
Western |
15 |
45 |
60 |
· |
311 |
48 |
359 |
Table 1: Estimates of host specificity and
oviposition success of each moth species on each tree type. Intermediate
(hybrid) trees were not included in this experiment. Visitation rates are based
on passive sampling using sticky-cards. Larval emergence rates reflect larvae
collected from fruits of each tree type, identified to species using mtDNA
sequencing.
Whereas eastern trees are visited primarily by T.
antithetica (the eastern moth), western trees
receive almost exactly equal visitation by the two moth species. A similar
asymmetry is seen in the larvae emerging from the two tree types. Whereas 99%
of the larvae emerging from eastern trees are of the eastern moth species (T.
antithetica), a
full quarter of the larvae on western trees are of the eastern moth species.
These preliminary results suggest that western moths (T. synthetica) are either much more ÔchoosyÕ
about which trees they will visit, or have a much more difficult time laying
eggs when they visit their non-native tree (or possibly both). However, we
still donÕt know exactly what mediates host specificity and ovipositon success
in this system, so there are still a lot of questions we would like to answer. Many
of these could be the subjects of student research projects.
1.
Currently,
we differentiate between the two moth species caught in the sticky traps based
on the size of the insects forewings. However, the moths definitely vary in
body size within species, so itÕs possible that we are sometimes mistaking an
individual of one species, for an individual of the other. It would therefore be desirable to know how
reliable body size is in telling the two moth species apart. Is there a way
that we could Ôdouble checkÕ species identifications?
2.
We are
currently using DNA sequencing to distinguish larvae of the two moth species
that emerge from fruits. There are some drawbacks to this, however. DNA
sequencing is very expensive, and takes a lot of time. We would like to develop
a less expensive way to distinguish larvae. One way would be to see if there
are reliable morphological differences that could allow us to tell the two
species apart at the larval stage. Another approach would be to use some less
expensive means of genotyping the larvae. Some possibilities include using
microsatellite DNA, or methods such as ÔPCR RFLPÕsÕ, or regular old RFLPÕs to
distinguish larvae.
3.
As I
mentioned above, at the Tikaboo valley site, there are not only ÒwesternÓ and
ÒeasternÓ trees, but also some trees that are morphologically intermediate, that
might be hybrids. WeÕd like to know how often the moths of each species visit
these hybrid trees. If it really is matching between the flowerÕs style and the
mothÕs ovipositor that makes a difference, you would expect the western moths
to do a little bit better on flowers with medium-sized styles.
4.
Obviously,
one key step in the experiment above is being able to reliably distinguish
between ÒeasternÓ and ÒwesternÓ trees in the hybrid zone. So, it would be
desirable to develop quantitative measures of how reliable different features
are for distinguishing different tree types (see the Godsoe et al paper for
details about different morphological features), and how often morphological
measures of tree type agree with genetic measures.
5.
Lastly,
weÕd like to know whether the geographic location of trees within the contact
zone affects how many moths of each species visit the trees. The contact zone
is fairly small (about 4 KM across), and on either side of the contact zone are
populations of ÒpureÓ eastern or western trees. You might expect that trees
that are closer to –say- the western edge of the contact zone would
receive more western moths, and this could mess up our estimates of host
specificity. How could we test this hypothesis?
Consequences of Global Warming
for Joshua Tree
Based on
the environments where Joshua trees currently grow, we can use climate data to
infer the range of environments that they are theoretically able to occupy (their
fundamental niche). By then combining these Òniche modelsÓ with predictions of
the climate is expected to change over the next century, we can develop
predictions about how the Joshua tree may respond to global warming. Based on
these models, Joshua tree is predicted to be severely impacted by global
warming over the next century (Dole et al. 2003; Shafer et al.
2001); local population extinctions are
projected over much of its current range. Populations at low elevations, and in
the southern portion of the range, including much of Joshua Tree National Park
and the Mojave National Preserve are expected to go extinct.
The time scale
on which these extinctions may occur is unclear, however. If we compare
populations in areas expected to experience local extinctions, with those that
are predicted to retain Joshua trees, there is a striking difference in the
character of the populations. In areas expected to experience population
declines and extinctions, population density is extremely low, and most trees
are very large and (apparently) very old. (See Figure 3). Conversely,
populations at higher elevations are composed primarily of young,
pre-reproductive trees (See Figure 4). This pattern is even more noticeable if
we compare the proportion of the population in different Òsize classesÓ (Table
2).
Size Class |
% of Population |
|
|
4000Õ |
2000Õ |
Seedlings |
75 |
35 |
2 |
8 |
3 |
3 |
6 |
12 |
4 |
7 |
16 |
5 |
3 |
15 |
6 |
1 |
11 |
7 |
0 |
5 |
Oldest |
0 |
4 |
Table 2:
Size class data for Joshua trees near Palmdale, CA.
At the high
elevation site in Table 2, almost all of the trees are in the smallest size
class, and only a small minority of trees is beyond the seedling stage. On the
other hand, at the low elevation site, the majority of trees are past the
seedling stage, and many are very old indeed. These differences in demography
are typical of what we see in human populations experiencing either population
growth (majority or the population is in the youngest age class), or population
decline (majority of the population in older age classes) (Gotelli 2001).
If populations in the warmest
climates are already on their way to extinction, it suggests that the effects
of climate change may be much more dire for Joshua tree than the current models
would predict. The underlying models assume that every place that Joshua tree
currently exists represents an area where the trees can flourish. However, if
many of these areas are actually not suitable, because the current climate is
actually too warm or too dry, the future range of Joshua tree may be even
smaller than we currently expect.
This project is still in its infancy,
however, so there are lots of questions weÕd like to know the answer to.
1. The data presented here represent a
comparison across an elevational gradient in one part of the range. Would we
find similar patterns in other parts of the range?
2. The data here are based on size
classes. However, size classes are not really a very good way to estimate demography.
Just for one thing, maybe trees actually grow at different rates in different
elevations or different climates. So, weÕd like to develop some independent
estimate of tree age. We canÕt use tree rings, because Joshua trees are
monocots, and donÕt have tree rings. One approach that has been useful for
other plants that lack tree rings is to use radiocarbon dating to estimate the
age of trees (Vieira et al. 2005). Could such an approach be used
here?
3. Could the differences in size class
data be used to estimate the rates of population growth and decline in
different populations? What kind of additional information would we need?
4. Another common approach to studying
population growth and population expansion is to use genetic data, such as
microsatellites, to try to measure growth rates (Cornuet and Luikart 1996). Would such an approach be possible
here?
Some Useful References:
Cornuet, J. M., and G. Luikart. 1996. Description and Power
Analysis of Two Tests for Detecting Recent Population Bottlenecks From Allele
Frequency Data. Genetics 144:2001-2014.
Darwin, C. 1874. Letter to J D
Hooker, April 7, 1874 in F. Burkhardt, and S. Smith, eds. A Calendar of the Correspondence of
Charles Darwin, 1821-1882 Cambridge, The Press Syndicate of the University of
Cambridge.
Dole, K. P., M. E. Loik, and L. C.
Sloan. 2003. The relative importance of climate change and the physiological
effects of CO2 on freezing tolerance for the future distribution of Yucca
brevifolia. Global and Planetary Change 36:137-146.
Fulton, M., and S. A. Hodges. 1999.
Floral isolation between Aquilegia formosa and Aquilegia pubescens. Proceedings of the Royal Society of London Series B 266:2247-2252.
Godsoe, W. K. W., J. B. Yoder, C. I.
Smith, and O. Pellmyr. 2008. Coevolution and divergence in the Joshua
tree/yucca moth mutualism. American Naturalist 171:816-823.
Gotelli, N. J. 2001, A Primer of
Ecology. Sunderland, MA, Sinauer.
Grant, V. 1952. Isolation and
hybridization between Aquilegia formosa and A. pubescens. Aliso 2:341-360.
Hodges, S. A., and M. L. Arnold.
1994. Floral and ecological isolation between Aquilegia formosa and Aquilegia pubescens. Proceedings of the National
Academy of Sciences 91:2493-2496.
Marr, D. L., and O. Pellmyr. 2003.
Effect of pollinator-inflicted ovule damage on floral abscission in the
yucca-yucca moth mutualism: the
role of mechanical and chemical factors. Oecologia 136:236-243.
Pellmyr, O. 2003. Yuccas, yucca
moths and coevolution: a review. Annals of the Missouri Botanical Garden
90:35-55.
Pellmyr, O., and K. A. Segraves.
2003. Pollinator divergence within an obligate mutualism: two yucca moth
species (Lepidoptera; Prodoxidae: Tegeticula) on the Joshua Tree (Yucca
brevifolia;
Agavaceae). Annals of the Entomological Society of America 96:716-722.
Shafer, S. L., P. Bartlein, and R.
S. Thompson. 2001. Potential changes in the distribution of western North
American tree and shrub taxa under future climate scenarios. Ecosystems
4:200-215.
Smith, C. I., W. K. W. Godsoe, S.
Tank, J. B. Yoder, and O. Pellmyr. 2008. Distinguishing coevolution from
covicariance in an obligate pollination mutualism: Asynchronous divergence in
Joshua tree and its pollinators. Evolution 62:2676-2687.
Vieira, S., S. Trumbore, P. B.
Camargo, D. Selhorst, J. Q. Chambers, N. Higuchi, and L. A. Martinelli. 2005.
Slow growth rates of Amazonian trees: Consequences for carbon cycling.
Proceedings of the National Academy of Sciences of the United States of America
102:18502-18507.