Download The Hormonal and Genetic Basis for Caste Differentiation in Termites

The Hormonal and Genetic Basis for Caste Differentiation in Termites
C. W-R.
Biology 454
Spring 2004
Abstract:
Eusocial insect species are relatively rare in the evolution of the insects.
Hymenoptera have evolved it multiple times but the termites have only evolved it
once. The factors that go into the control of the expression of polymorphic traits are
controlled at a colony level to ensure that enough of each caste type is present to
perpetuate and care for the colony. The transmission of chemicals and symbionts by
anal feeding is believed to play a large role in the social behavior of the termites. In
this paper recent and earlier experiments are reviewed to give an overview on what
is know about caste determination and regulation. This will cover both hormonal
regulation as well as theoretical models of genetic expression to explain the origins
of sociality. Finally the little bit that is known about specific gene expression in
differentiated soldiers will be discussed.
Introduction:
The insect world is known for its amazing diversity, both in terms of species
habitat as well as living strategy. Among the insect there are only a few orders with
eusociality and some scattered sub-social insects. Characteristics of eusociality are
division of reproductive labor, two or more generations living together, and cooperation
in care of the young. Among the Hymenoptera it is estimated that sociality arose at least
eleven times, yet all indications say that it arose only once in the Isoptera (Abe et al.,
1985). Termite society forms at the level of the colony. It is headed by a reproductive
pair, the king and the queen, though in some cases there are multiple reproductive pairs
within the same colony. They remain in the colony and depend upon the worker caste to
take care of their needs through foraging and building the colony. They are capable of
repressing the formation of other reprodutives by secreting chemicals that inhibit the
larva from developing into reproductive castes (Myles and Chang, 1984). The
developmental pathway in the termites can diverge in multiple ways and differs
depending on the family of termites considered. In general the larva can go either the
reproductive route or the sterile route. The reproductive route leads to the development
on a winged alate capable of leaving the colony to attempt to mate and found a colony of
its own, though the success of this founding is relatively low. The sterile route usually
develops as a worker for a few molts and can then further differentiate to a soldier by
way of a pre-soldier phase.
Current evidence suggests that the termites evolved from a wood eating
cockroach. This woodroach presumable already had a social system, as all of its
descendents are social. Even within the termite order there is some variation as to extent
of sociality. Lower termites usually lack a true worker class and instead depend on a
pseudergate (false worker). This pseudergate differs from a true worker in that it has not
become sterile. In the higher termites there is a true worker class, consisting of sterile
workers. Sterile soldiers are present in nearly every species, being secondarily lost in
some of the higher termites. They differ from the soldiers seen in ants in that termite
soldiers do not feed themselves and depend upon the workers of the colony for
nourishment whereas ant soldiers are usually able to partake in at least a few of the
worker activities and are capable of feeding on their own. Also, termite soldiers have
highly specialized morphology, with heavily scoleritized heads and mandibles modified
for the defense of the colony tunnels.
The genetic basis for sociality in hymenoptera is much easier to show because of
their haplodiploidy. This creates a system where the worker sisters are more related to
one another than they would be to their own progeny. Thus they have an investment in
helping the queen raise their sisters. However, all of the termites are diploid, so
coefficients of relatedness will not play as large a role even in cases of high inbreeding
within a colony. Theories for the evolution of sociality in termites are based upon
Hamilton’s rule which considers the relatedness between two individuals (r), the cost to
the individual (C), and the benefit to the recipient (B). If the benefit times the relatedness
is greater than the cost to the individual (B*r>C) then this would allow for the evolution
of altruistic behaviors by allowing the gene to be selected for by the higher fitness of
individuals benefiting from the altruistic behavior. In termites this could relate to their
need to obtain symbiotic organisms from the feces of other colony members. This would
favor termites that clumped together as every time a termite molts it needs to reobtain
symbionts in order to feed.
It is theorized that soldiers evolved after the initial social behavior started based
on the fact that soldiers are present in all termite families and their evolution for the
defense of their colonies indicates their importance to the well-being of the colony. There
is still some debate as to how the caste arose. Some theorize that soldiers arose from
reproductive individuals that were specialized for fighting. Others believe that the soldier
first evolved as a non-sterile soldier from a non-sterile worker and then became a true
soldier. Further evidence shows that because of predation selection pressure it should be
relatively easy for soldiers to evolve. The true worker caste is believed have evolved after
the soldier caste from the pseudergates (Thompson et al., 2003). It is believed that the
extra stability this would provide to the nest in terms of structural integrity is due to foodnest separation. Pseudergates do not leave the colony as often as true workers and mostly
forage on the wood that the colony was founded in. True workers are more likely to
forage and prevent the removal of wood material that weaken the structure of the colony,
preventing collapses from killing the reproductive pair and significantly harming the rest
of the colony.
Since the castes play such a vital role in the perpetuation of termite sociality it is
important to learn how the various castes are created from the same genetic material. So
far, decades of research have gone into the topic and results are still unclear. The role that
juvenile hormone (JH) plays in soldier development is well documented but the pathway
is not understood. Little is known about the pathways that lead to differential gene
expression and the method for their dispersal in the colony. The following sections will
look into research that has been done to try and determine the factors that effect caste
determination and differentiation.
Results and Discussion:
The Role of Juvenile Hormone:
Experiments performed in the 1930’s were the first to show that termites made
use of social pheromones. Primer pheromones are those that induce changes in
morphogenesis that lead to a caste determination. Castes are capable of regulating the
production of other castes, in some cases the soldier’s production is stimulated by the
reproductives of the colony. Soldiers have also been shown to inhibit the production of
other soldiers. The mechanism for this has only been shown in a few species where the
soldiers secrete a terpenic substance from their nasus that inhibits development of more
soldiers and thus controls the ratio of soldiers in the colony. There is even data showing
that in termites lacking the frontal gland to secrete these compounds there is still an
inhibitory effect to soldier development if soldier head extracts are added to experimental
colonies that did not contain soldiers (Korb et al., 2003) They were also able to show that
these chemicals were able to act over a long period of time (6 months with no further
additions of soldier inhibitors) to inhibit the production of soldiers in. The inhibitors were
not able to prevent any soldiers from being formed, as in every case there were a few
soldiers formed per test group. Presumably there is some competition between the
inhibitory effect of the soldiers and the stimulating effect of the reproductives.
JH plays a large role in the development of the soldier caste. Early studies showed
that the implantation of the corpora allata, the structure that is responsible for
synthesizing and secreting JH, into undifferentiated termites is usually sufficient to
induce them to molt into soldiers. There must be a threshold level of JH necessary to
induce the development of only a portion of the termites, and through their inhibitory
effect, prevent the over production of soldiers in the nest. Studies performed by Lanzrein
et al. (Watson et al., 1985) have shown that there is a great deal of variation in the JH
level in eggs laid, which corresponds loosely to periods when one caste is produced
preferentially over others. They believe that eggs could be influenced prior to hatching to
head down either the reproductive or the sterile pathway due to influences of the initial
JH levels present during development. However, they did not see what these eggs
developed into nor did they collect regularly enough to justify these hypotheses. Further
study will need to be much more regimented in collecting and observation of termite
development from eggs with different JH levels if these preliminary results are going to
be determined to have a strong effect on caste determination.
There is also an effect of lethality at high levels of JH concentration. In
experiments performed with several JHs and two juvenoids (synthetic JHs) on two
species of termite the termites showed higher rates of mortality as the concentration of JH
increased (Scharf et al., 2003). Another result they showed was that termite responses
varied to the different JHs and juvenoids. This was true both within and between species.
The different responses to the JHs were interesting because the two species are from the
same genus, though distantly related, thus suggesting that response to a specific JH is not
well conserved evolutionarily. Interesting they also showed that experimental colonies
showed better survival when soldiers where present as part of the population in nearly
every case. In one trial the survival changed from 0% without soldiers to 81.2% with
soldiers present. The authors proposed no hypothesis on this extreme range in mortality
due to the addition of hormones other than to say that the two termite species differed in
their responses to juvenoids, though it could be possible that there is some sort of JH/
juvenoid inhibiting compound secreted by the soldiers that prevents the synthetic
hormone from exerting its full effects on the termites and thus reduces its lethality.
Despite the decades of research that have gone into the response to JH there is
still very little data that has shown to apply broadly across the termite species. The fact
that species within the same genera respond drastically different to the same conditions in
hormones suggests that perhaps each species has developed its own highly specialized
method of caste regulation and biochemical pathways to achieve polymorphic responses.
There is a great deal of literature out on caste determination, much of it decades old,
lacking the refined empirical chemical data that today’s current technology is much more
capable of achieving. More protein assays should be performed to see what effects the
hormones are having at the cellular level. If the effects of JH are to be fully understood,
every step of the signaling pathway needs to be understood starting from the responses at
the JH receptor.
Genetic Influences on Caste:
Since termites lack the haplodipoid genome of the Hymenoptera there must be
some other genetic effect to account for their eusocial behavior. In addition to this there
must be a refined level of genetic control to keep caste specific structures from being
improperly produced. Very little is understood of the termite genome, though it does
seem that males are heterogametic. There does seem to be a common feature in male
meiosis in which rings of DNA are formed and transmitted to all of the same sex siblings
(Roisin, 2001). This could potentially affect relatedness between the nest mates and skew
sex ratios in the worker and soldier castes. Some species exist in which all of the soldiers
are of the same sex and the worker castes display a sexual dimorphism. The linkage of
the chromosomes is not believed to have given rise to sociality, but may have placed
selective pressure on existing parts of termite society especially when combined with sexbiased castes.
Some evidence exists that since sociality is well established in termites a colony
will benefit from increased genetic diversity despite the corresponding loss of relatedness
of the individuals (Goodisman and Crozier, 2003). In some species of termites there are
differences in genotype between foraging and non-foraging workers, hinting that genetics
plays a role in specific behavior if not caste determination. By collecting workers from
the same tree and making the assumption based on previous experiments that all of the
termites from the same tree belonged to a single colony, they collected approximately
thirty colonies and tested to see whether a single mating pair could account for the
diversity seen. Using 6 sites with quantified heterozygosity measurements they estimated
the degree of relatedness between the workers from individual colonies and concluded
that in 72.7% of the colonies sampled two reproductives were necessary to explain the
results. They also believed this to be an underestimation, since the multiple reproductives
would be related and the alleles they pass to their offspring would also likely be passed
on by the other reproductive pairs as well. More importantly they were unable to find any
genetic difference between the worker and soldier castes in most of the localities. In one
location they were able to see substantial differences between the castes from several
colonies, so they concluded that genotype may occasionally play a role in caste
differentiation, though they did not propose a situation in which it would arise in only a
few colonies of the species. It is possible that their assumption that all termites from one
tree are from the same colony is not true and is affecting their data.
So far only one gene has been identified that is specifically expressed in a single
caste. The SOL1 gene was found to only be expressed in the terminally differentiated
soldier mandibular glands and is believed to be a major component of mandibular gland
secretion (Miura, 2004; Miura, 2003). Further investigations hint that this may be
transmitted to other colony members through trophallaxis and have a pheromone-like
function. Although this is a big achievement in identifying genes specific to a caste it is
noted that this gene is a terminal one in the differentiation of a soldier. The entire
pathway leading to this gene needs to be understood to even begin to understand all that
goes into the expression cascade. The most vital step will be to identify those genes that
are directly downstream of the JH induction. Considering the amount of effort still being
applied to understand the cellular pathways of humans it will likely be some time before
more effort is available to be devoted to the study of termite gene pathways. The author
proposes that studies of the homologous genes in Drosophila may yield good results,
though he may be too optimistic because Isoptera and Diptera are distantly related orders,
and Drosophila have no caste system. Therefore it is questionable whether homologous
genes would exist or the pathways that lead to their expression.
Conclusions:
Despite the years of research that have gone into this topic there is an amazing
amount of material that is not known. Studying the responses of single cells in culture
could greatly enhance understanding of signaling. To reach this stage more work needs to
be done to classify the termite genome. Finding out what the sex determining factors are
could be done with RAPDs (Random Amplification of Polymorphic DNA) and AFLP
(Amplified fragment-length polymorphism) techniques. Once more genes and their
products are understood gene arrays can be established to see which genes are induced at
the addition of known and suspected hormones, pheromones, and inhibiting factors. The
sequencing of the Drosophila genome can be used as a good starting point to mapping
and analyzing the termite genome. The genes nearly universally shared by the insects
would already be mostly classified and research can focus on termite specific genes. With
the daunting amount of work still required to achieve these goals and the fact that
regulation seems to be very variable between the different species of termites it will
likely be many more years before final understanding of these processes are understood.
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Ecology. Norwell, Mass: Kulwer Academic Publishers, 2000.
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