Download Yucca-Moth and Yucca Plant Obligate Mutualism

Connor Cowdrey
Insect Behavior Review Article
Yucca-Moth and Yucca Plant Obligate Mutualism
The Yucca moth has an obligate mutualism that has severed as a perfect model for ecologists
and insect behaviorists to study and ponder over for over a century. This mutualism is considered to be
obligate, because without it, neither species would survive. The Yucca moths comprise of three genera,
Tegeticula, Peroxidae, and Parategeticula. The Yucca plants are scattered across the globe in hot arid
climates, with the majority of plants being in North America, South America, and Central America. This
obligate mutualism has been an active area of study largely by ecologists seeking to explain why
excessive exploitation doesn’t occur on one end of the mutualism. When species coexist via a
mutualistic driver, it is easy to assume that one side of the relationship could undermine and overtake
the mutualism to benefit themselves more than their ecological best friend. If an event like this were to
happen, the entire community and population of both species would change drastically in genotype,
phenotype, and allele frequencies (Dodd and Linhart, 1994). The primary research that has been
performed on this relationship tends to focus on how these populations stay at equilibrium, and why
they do not, or cannot, exploit one another. It is important to understand the ecological consequences
of exploitation in a mutual relationship, and it is also important to compare those ecological
consequences with instinctual behaviors that are not necessarily under the control of the insect. An
insect cannot think about the future the same way a human being can, it cannot assess possible
outcomes of scenarios that involve a large scale ecosystem like mankind can, even mankind gets these
predictions wrong. What is controlling the behavior observed in the wild between the Yucca moth
species, and the Yucca plant hosts? If either one of these parties over expresses exploitation, the entire
symbiotic relationship could be ruined for future generations. This is a question that ecologists and
behaviorists have asked themselves for a long time; most species act on instinct that allows them to
make the most favorable decisions to increase overall fitness, and will allow them to pass the most
genes on to the next generation, but these species cannot do this without disrupting the delicate
mutualism they have developed. How do external factors, ones that are neither Yucca moth pollinators,
nor Yucca host species, affect the obligate mutualism observed in the wild? This question has also been
addressed over the years, and studied to assess how folivorous insects may tip the balance the
mutualism, and how “bogus” Yucca moth species may influence the mutualism in one direction or the
other. Is the mechanism behind this mutualism mechanical or chemical, what drives the Yucca moths to
continue pollinating the Yucca plants, and what stops the Yucca plants from aborting fruits that have
Yucca moth larvae on them? This question has been studied the most, and provides a lot of insight on
how the obligate mutualism stays in equilibrium between the two parties. All of these topics have been
reviewed, summarized and analyzed to assess how this relationship really works throughout this review.
The obligate mutualism described in most literature is between each of the Yucca moth species,
and their designated host plant, the Yucca plant. The Yucca moths are responsible for the fertilization of
the Yucca plant, as the Yucca plant does not have any other identified pollinators. The Yucca moth flies
into the Yucca plant itself, it balls up pollen into a tiny sphere, and uses specialized mouth parts to stuff
the ball of pollen into the stamen of the receiving Yucca plant. This is a behavior that has been refined
over thousands of years, and as a result, only the Yucca moth is capable of doing this for the Yucca plant
(Holland and DeAngelis, 2001). This explains why the Yucca plant is so reliant on the Yucca moth, but
what does the plant do to enforce this behavior, and what does the plant have to offer the moth in
return to coax it into fertilizing the plant? The Yucca plant serves as mating arena for the moth, male
and female moths will join together inside and around the Yucca plant; this serves as an easy way for a
Yucca moth to find a mate, they do not need to rely on making high pitches sex noises like crickets do, or
having showy displays as we see in some birds, they simply have to meet at their mating arena
(Segraves, 2008). In addition to providing a sex dungeon for the Yucca moths, the Yucca plant also serves
as a nanny to the Yucca moth larvae. While the Yucca moth is pollenating the Yucca plant, it takes some
time to carefully lay eggs inside the Yucca plant; these eggs will hatch in a climate controlled
environment, with an abundance of seeds to eat, and with the protection of the Yucca plants sharp
leaves to serve as protection against birds and other larger animals (Tyre and Addicott, 1993).
From here it may be easier to view this as a risky relationship, why doesn’t one end of this
mutualism exploit the others genes and instincts? If the Yucca moth were to lay just a few more eggs, its
fitness would increase drastically given the abundance of seeds in the Yucca plant for the larvae to feed
on (Marr and Pellmyr, 2003). Oddly enough, this isn’t a behavior that is seen in the wild very often, what
is stopping this from happening? On the other end of the spectrum, if the Yucca plant selectively
aborted the seeds that were damaged by the Yucca moth while it was ovipositing, the plant would
reduce its energy expenditure, and would have a greater fitness by allowing undamaged fruits to
develop while starving the moth larvae (Addicott and Bao, 1999). Once again, this is something unseen
in the wild, though selective abscission and seed abortion are common and known to be utilized by
Yucca plants. There must be a balancing factor keeping these species in check, and solidifying the
obligate mutualism to be that of a fair one. Fortunately, most of the literature concerning these two
organisms discusses this exact paradox, and why no exploitation is observed in nature.
Years of research from across the globe has been collected and designed to try and find an
explanation for the lack of exploitation in this mutualism; it seems that both intrinsic and extrinsic
factors are contributing to the fairness of this interaction. The most prominent idea in the literature is
that of population equilibrium; if one species tries to cheat, it will start a population decline in the other
species, and a population increase in its own species. These two species rely on each other, so by
helping themselves, they hurt the other, which will eventually hurt themselves. This idea was
demonstrated nicely by J. Nathaniel Holland and Donald L DeAngelis who said “it is clear that if
pollinator populations are large, then, because many eggs are laid, costs to plants are large, whereas, if
pollinator populations are small, gross benefits are low due to lack of pollination”. General ecological
ideas are being discussed here, but the consequences are very large. Through basic population analysis
and the idea of survivorship, it would be unfavorable for either species to try and “cheat” the other
species out of its part of the bargain. Though this idea is a nice one, plants do not have the logical
thinking, nor do moths for that matter, to make these kinds of judgments based on future possibilities.
This means that mechanical, chemical, and situational responses and mechanisms must be in place for
the obligate mutualism to still be intact, and for both species to not become extinct.
Mechanical factors that play role in this mutualism are easy to study, and there have been major
discoveries showing that mechanical stress on Yucca plants by Yucca moths can be a signal to induce
floral abscission which can account for up to 95% of Yucca moth egg death (Shapiro and Addicott, 2004).
Abscission is the act of shedding a particular organ or tissue, this can easily be described by the lizard
escape mechanism we are all familiar with; when a lizard gets caught by a predator, and it may abscise
its tail in order to escape with hope of redrawing the tail again at a later time. Yucca plants do this same
thing, except instead of abscising a tail; they may abscise floral parts or abort infested fruits (Shapiro and
Addicott, 2003). When a Yucca moth gets over-zealous and lays too many eggs while ovipositing inside
the Yucca plant, the Yucca plant may abort the infested fruit effectively starving the young moth larvae
(Wilson and Addicott, 1998). This is a response to highly damaged plant tissues in the Yucca plant, which
is a result of too many eggs being laid in the tissues of the plant (Marr and Pellmyr, 2003); the Yucca
moth lays its eggs less than a centimeter under the surface of the plant’s tissue, which inherently causes
some plant damage (Segraves, 2003). This mechanism to cope with mechanical stress must be one of
the largest drivers controlling the mutualism; some populations have even adapted to live in higher
elevations in order to reduce mechanical stress. These populations have become very good at living in
higher elevations, where there are less pollinators, but less larvae survival rate as well; being able to
become pollinated, while saving energy is an odd, but not unexpected adaptation seen in Yucca plants
(Dodd and Linhart,1994) There is a cost to benefit ratio that must be analyzed chemically by the Yucca
plant to determine whether or not aborting the fruits will lead to too much moth larvae death; if too
many larvae die, the plant is less likely to be fertilized in the future which will reduce the overall fitness
of the Yucca plant, as well as the Yucca moth (Humphries and Addicott,2000). Though this chemical
analysis process is under researched and somewhat of an anomaly of how the plant manages these
types of decisions, there must be a mechanism preventing the Yucca plant from making future fitnesshindering abscissions. With the same idea, Yucca moths must also be directed by chemical cues that
limit the amount of eggs they can lay inside the Yucca plant; if they lay not enough they will have a
lower than possible fitness, if they lay too many, the Yucca plant may abort the fruits that are supposed
to be feeding the Yucca moth larvae (Marr and Pellmyr, 2003). It has also been recorded that Yucca
plants with low pollen quality may decide to abort their fruits; this would allow for genetic diversity and
high fecundity to remain a priority; as Yucca moth density increases, the pollen quality goes down
(Addicott, 1998). Reid D. Wilson and John F. Addicott tried to determine if selective abscission of flowers
was the stimulus to induce particular oviposition strategies in Yucca moths. They used two species, one
that had a natural “deep” ovipositing behavior, and one that had a natural “shallow” ovipositing
behavior; they found that “deep” ovipositing behavior caused a higher percentage of abscised flowers
and aborted fruits in the Yucca plant, with a longer period of time, the “deep” Yucca moths may have to
start depositing eggs more shallow into the plant in order to maintain a competitive advantage (Wilson
and Addicott, 1998).
Chemical factors also play a large role in this mutualism that has been observed for so long.
Before any reproduction by either species can be executed, the two species need to come in contact
with one another. By the use of a Y-tube analyzing technique, researchers Glenn P. Svensson, Olle
Pellmyr and Robert A. Raguso were able to test the olfactory responses of Yucca moths to volatile
compounds released by the Yucca plant. This group of researchers collected the scent from living Yucca
plants at night, when the moths are most active; this scent was compared against ambient air in the
trials of attraction in the Y-tube. They state in their report that “the sent from virgin Yucca glauca is
sufficient to attract its obligate pollinator Tegeticula yuccasella” (Svensson et al., 2011); they also noted
that both sexes of moth were able to detect the floral volatiles and were attracted to them. This is
important because both sexes of the Yucca moth must be able to find each other, instead of chasing
each other’s pheromones, they chase the scent of their host plant in order to meet up and mate. These
moths mate inside the host flowers of the Yucca plant itself, having a scent to follow to meet a potential
mate is adequate evidence that the Yucca plants need the pollination by these specific pollinators
enough to have developed a mechanism to act as a beacon for nearby Yucca moths. Also, Svensson and
his colleagues noticed that female Yucca moths did not discriminate between virgin flowers and hand
pollinated flowers; this shows that there is no chemical change in the Yucca plant that would deter
multiple pollination events (Svensson et al., 2011)(Leebens-Mack, 1997). Because the flowers do not
stop emitting the chemical olfactory cues, the selection pressure for “fair” moths becomes even
stronger. Moths, like nearly every animal, are a competitive species; increasing your own fitness is
important, but limiting the fitness of competing individuals is also important, because survival of genes
is about relative fitness within a population. If a moth were to exploit its abilities in laying too many
eggs, and the Yucca plant aborts the fruits that are supposed to feed the larvae laid inside the flower,
not only is your fitness dramatically decreasing, but when a more “fair” individual comes to the same
flower because of the constant release of olfactory cues, and the Yucca plant does not abort it’s fruits,
the fitness of your competitor is increasing dramatically. Through natural selection and population
equilibrium genes that encourage excessive exploitation from moth species must have been lost due to
this basic concept of competitive “fairness”.
The system in place that is contributing to the under exploitation of one species to the other is a
fairly complex assemblage of mechanical and chemical signals utilized by both the Yucca moth and its
host, the Yucca plant. These factors are driven largely by ecological stability and have adapted to
prevent the extinction of both contributors involved in the obligate mutualism (Holland and DeAngelis,
2001). However, some external factors have been discovered that may interfere with this seemingly
perfect relationship, ones that test the foundation of a system that seems to be only so stable before
the “tipping point” that could cause both parties to become extinct. One such factor is that of the
“bogus yucca moth”, there are three genera of Yucca moth, only two are actual pollinators of the Yucca
plant; the third, Prodoxus lack the specialized mouthparts needed to actually pollinate the Yucca
flowers, this results in what would be the equivalent of an over exploiting Yucca moth in the mutualism.
Researchers David M Althoff, Kari A. Segraves and Jed P. Sparks studied this interaction to see if it would
throw off the mutualism eventually. They determined that mutualisms are not always pairwise, and that
external factors can play a role in the mutualism without throwing it off course; the bogus Yucca moth
still lays its eggs in the flowers of the Yucca plant, but does not provide any pollination, thereby
increasing energy expenditure by the Yucca plant with no reward of being pollinated as expected
(Segraves et al., 2004). After measuring reproductive traits such as flowering characteristics, seed set
and seed germination, they came to the conclusion that though this bogus Yucca moth is an exploiter, it
doesn’t actually throw off the mutualism (Segraves et al., 2004). This type of moth is not a new one, so
any affect it may have on the mutualistic relationship between true Yucca moths and Yucca plants has
already been compensated for in the population and the interaction between these two organisms. This
bogus Yucca moth was also studied by William F. Morris, Judith L. Bronstein, and William G. Wilson who
stated “many mutualisms host “exploiter species that consume the benefits provide by one or both
mutualists without reciprocating. Exploiters have been widely assumed to destabilize mutualisms, yet
they are common” (Morris et al., 2003); they continue to claim that “when facing strong interspecific
competition, exploiters cannot invade and coexist with the mutualists if intraspecific competition in
pollinators and exploiters is weak” (Morris et al, 2003). This shows that the exploiting Yucca moth
species may be able to survive the 3-way coexistence as long as the competition is relatively low
between the Yucca moth and the Bogus Yucca moth; the mutualism will not be thrown off balance, as
long as the scarcity of Yucca moths continue, and there isn’t a dramatic increase in Yucca moth
population – of which would be nearly impossible unless the Yucca moth was also exploiting the Yucca
plant resources. This seems to be a “self-check” on the mutualism based on external factors. Another
potential problem for this mutualism is the abundance of folivorous insects that live in the same
climates as the Yucca plant. Researcher Kari A. Segraves studied how folivorous insects may limit the
cost of mutualism for the Yucca and the Yucca plant. H. densus is a folivorous beetle that consumes
plant material as a source of nutrients, though in the process, it tends to eat insect eggs as well
(Segraves, 2007). One could imagine that the death of plant tissue and moth eggs would lower the
fitness of both species, but Segraves discovered that by calculating general population statistics, the
beetle was not drastically increasing the amount of energy used by either the Yucca moth, or the Yucca
plant. This mutualism seems to not care about the outside world, with so many disruptions that could
potentially throw the mutualistic equilibrium off balance, the mutualism still survives. This isn’t
surprising considering the age of both the Yucca moth and Yucca plant species that are around today,
they haven’t died off yet – and they shouldn’t die off anytime soon.
References:
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