[News from the North] Subterranean Termites: The Evolution of a Pest

Termites are soft-bodied, mostly blind, make easy prey for ants and other insectivores, and are vulnerable to drying-up in open air. In addition, individual termites need to remain in contact with their colony mates for survival, or else perish alone. Despite these characteristics, termites are still here! But how can this be? How can individual termites be so frail, yet their colonies, and entire lineage, be so long lived?

The answer to this question can be found in their social biology. Like ants, and some bees and wasps, termites live in well-integrated societies where individuals are dependent on each other for survival. They each perform different tasks that, collectively, meet the needs of the colony. Even the task of reproduction is divided up among them. Most individuals within a termite colony are effectively sterile, and they simply help their reproductive relatives rear offspring on their behalf. On matters of survival and reproduction, the colony collective is much stronger and more effective than the individual.

This social way of life has served termites well, as evidenced by their sheer antiquity. In an evolutionary sense, termites branched off from a cockroach ancestor approximately 200 million years ago. That makes termites the most ancient of social insects. Taxonomically speaking, termites are cockroaches.

The evolutionary history of termites has several implications for pest control today. First, they have the peculiar habit of eating wood. While most animals are unable to digest the tough materials found in wood, termites can exploit this resource to their benefit with the help of gut microorganisms. No doubt this rare niche has put some species on a crash course with human constructs. They are merely feeding on, and living in, the wooden bits to survive, as they have for millennia.

Second, their sociality affords them a factory-like division of labor that renders termites very efficient at surviving and reproducing across a wide range of habitats, including urban habitats. Just like workers on an assembly line at a car plant, where each individual specializes in a stage of production, termites divide up tasks within the colony. For termites, the focus is on perpetuating the colony, or making offspring. Hundreds, thousands or millions of eggs can be laid and raised within the living factory, which itself may be decentralized to include more than one reproductive center, or assembly line.
 

Damage Via Division of Labor.

So now we know how termites do it: their sociality and their penchant for wood are biological qualities that predispose some species to associate with human habitation and persist as a resilient collective force.

Let’s take the living factory analogy further. The factory is efficient because human managers study the process and assign roles as needed to minimize costs and maximize profits. Termites have no such foresight or ability, but their wood-eating, offspring-making societies are nonetheless efficient, almost as if they did have managerial oversight. For termites there is no such calculation, but instead these social insects follow evolved rules of thumb that they run in response to cues from their environmental and social surroundings. For example, when Termite A bumps into Termite B, Termite A’s response might be: “If I recognize Termite B is a colony mate, I’ll cooperate with him. If he’s not a colony mate, I’ll defend against him!” In the latter case, may the best termites win in these competitive encounters.

This simple rule or ability to recognize kin explains how termites keep their colonies intact and separated from each other. Only workers from the same colony, or kin group, cooperate. Non-kin are typically agonistic towards each other. If colonies are kin groups, as they typically are, then colonies should to some extent be competitive with each other, and keep each other’s territories in check.

Subterranean termites on your customer’s property are always a problem, but at least the colonies are circumscribed and can be targeted effectively by directing treatment towards the reproductive center of the colony if possible.

As bad as it is, the homeowner’s problem would be worse if the colonies simply blended into giant supercolonies that were larger, spread across multiple properties and defied any localized treatment.

This, unfortunately, is what seems to happen in some urban settings. The Eastern subterranean termite, for example, can abandon its normal behavioral rule of thumb to form kin colonies and defend territories. Instead they form indiscriminate supercolonies that amass and transform underground to spread across large areas. This makes them especially difficult to localize and treat, and evermore resilient because they can potentially join-up with neighboring populations into an ever bigger scourge.

At Western University, London, Ontario, Canada, we study this aspect of termite pest biology — how evolution and the genetics of kinship can explain how Eastern subterranean termites have been able to invade urban Toronto, and spread across its core and suburbs despite intense efforts to control them. We think that the Toronto supercolony is different from the American native population from which it came, as these termites lost their natural ability to recognize kin, and with it, the ability to regulate its colony membership or size. We are currently testing one possible explanation, and with it, we hope to uncover new ways to circumvent their future spread and make conventional control methods more effective.
 

All in the Family?

Canada has a relatively cold climate for a large part of the year, and we don’t have many termite species here. But we do have one introduced species that is a voracious pest. With the generous help of pest controllers, we began sampling Eastern subterranean termites from infested homes and neighborhoods throughout Toronto, and across other municipalities in the southwest portion of the Canadian province of Ontario.

The Toronto story began in 1938, when termites were first reported in the dock-lands precinct where one small invasive population had inadvertently arrived as stowaways on a shipment from across Lake Ontario. Its precise origin is unknown, but from this “ground zero” termites have spread throughout the city, and continue to do so. In a mere 80 years, Reticulitermes flavipes has invaded hundreds of city blocks and neighborhoods, and remains a species of civic concern.

What makes the termites of Toronto difficult from a pest controller’s perspective is that they do not appear to follow the “kin recognizing” rule of thumb. If you take termites from one part of the city and put them together with termites from miles away, they do not show any competition or territoriality. They perceive each other as colony mates, or kin, even though in any practical sense, they aren’t. This lack of recognition among the introduced termites of Toronto means they don’t form colonies with defined boundaries. Instead, they simply intermingle indiscriminately as if they were one big family. Termite A thinks that Termite B is her brother, even though their genealogy might be as much as 80 years removed. This is a long time in generations for a short-lived insect. Are the Eastern subterranean termites of Toronto the biggest termite “colony” in the world? Maybe not, because similar phenomena have been reported in other cities in which the species has invaded, for example, Paris, France.

This small behavioral difference in how termites conduct themselves can make a big difference to strategizing their eradication. If one homeowner pays for a treatment, he might be successful in deterring termites from his property temporarily, but block-wide or city-wide coordination would seem to be a more appropriate approach for any long-term eradication success.

At Western University we are using genetic analyses to determine why these termites don’t appear to discriminate on the basis of kinship. First, we have used a type of genetic marker called microsatellite DNA to test our suspicion that — yes, all of the termites in Toronto came form a single invasive source. In a research paper that we recently published in the journal Environmental Entomology (Scaduto et al 2012, 41: 1680-1686) we showed that Ontario as a whole has at least three genetic populations (i.e., three distinct lineages of microsatellite DNA), but the metro Toronto population itself is most likely from a single source.

What does this have to do with supercolonies? Well, here’s the idea...if Toronto’s termites all came from one source 80 years ago, then in a sense they are all related, hence their lack of kin discrimination is partially explained. Termite A and Termite B have not shared a common ancestor but nonetheless they are distantly related. So, they might perceive each other as distant kin. But this explanation is unsatisfying because native populations that have not undergone a genetic bottleneck, as the Toronto termites have, do not do this. In the native range Termite A and B would more likely be foes, not friends.

A more complete explanation could be proposed in the following way. If termites, in their ancient past, were selected to recognize kin on the basis of genetic alleles (variants of a gene) that each individual carries, then loss of these alleles through a genetic bottleneck might have stripped the Toronto population of this ability. Termites of Toronto and Paris might therefore be “blind” to kinship. They can’t tell who is a relative and who is not, and the default appears to be in favor of treating everyone as if they were close kin. Too bad the opposite weren’t true. If the default setting in the absence of information was to assume foe rather than friend, they might all have killed each other.

We believe this is what has happened in Toronto, and potentially elsewhere, that subterranean termites have invaded urban habitats to form supercolonies. Despite their tremendous success at invading the reaches of Toronto, they have done so from a genetically diminished starting point.
 

Genetics and Pest Control.

What is the mechanism by which these kin recognizing alleles in the eastern subterranean termites work? Well, we can consider each colony’s unique set of alleles (its genotype) to be like a coat of arms that communicates family membership. Within a colony, individual termites may have slightly different combinations of alleles, but on the whole they are similar and thus kin. That is, they share the same coat of arms. Remove the unique features of the coat, or unique alleles from the genome, and they fail to differentiate. Instead of two clans warring, they buddy up and join forces.

Just exactly which genes are involved? We don’t know yet but we are trying to find out. There are candidate genes that might play a role in kin recognition, such as those that affect the composition of hydrocarbons on the surface of the termite’s cuticle. Alternatively, kin recognizing alleles might be those that affect chemical cues like residues and pheromones that termites use for social communication and recruitment. Regardless, we hope to uncover some of these genes and alleles using genomic information that we are currently generating.

Specifically, we are shifting from our prior use of microsatellite DNA to a more sophisticated technology called RNA-Sequencing analysis. We hope that this new genomic data, when assembled and analyzed, can be used to compare what genes are present and expressed between Toronto and other termite populations within Canada and the United States.

These genes for kin recognition, if they exist, are thought to be a bit complicated in the sense that they need to be rare to be effective (to provide a unique family coat of arms). Yet this effectiveness leads to greater reproductive success for the colony and, in turn, reduces their rarity. In this evolutionary paradox: the rarest alleles are the most successful, and by virtue of this success, become more common in the gene pool. Once common, the same allele becomes less effective and, as a consequence, more rare. This cycle of bust to boom again, is a pattern that is typical of what geneticists would call “balancing selection.” RNA-Sequence data allow us to test this criterion by characterizing the diversity of alleles present at each locus (the position of each gene on a chromosome) across the whole termite genome. If our analysis is successful, then we will have screened the termite genome for regions that might contain the very genes involved. Ultimately, we hope to confirm or reject the idea that supercolonial termites from Toronto are genetically barren at kin recognition genes, relative to colonial termites from their native range.

With our RNA-Sequence data, it should be possible for us to single-out the genes evolving in this manner. Those genes are of interest to us, and we hope to you. If we had them, it might be possible to target them, somehow, and force invasive supercolonial termites to return to their normal colonial ways? This potentially could reduce colony sizes drastically; compromise their ability to re-colonize treated areas and re-introduce a measure of competition among different colonies. This all would make conventional pest control more effective. Or, better yet, it might be possible to exploit these kin recognizing genes and make termites follow a self-destructive rule of thumb. Instead of “cooperate with all other termites as if they were kin,” as it currently stands, how about “kill all other termites as if they were non-kin.” As we further our understanding into termite genomics, we will continue to update the pest control community of our results. Stay tuned with us on this exciting journey of discovery.

The authors are with the Department of Biology, Western University, London, Ontario, Canada.