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Invasive Ants and Supercolonies

I wrote this a couple of months ago as part of a university course in Ethology. I have been meaning to post it ever since, however first I wanted to make a few revisions. There are some major problems with the essay that I had been meaning to fix before posting it here, but I simply haven't had the time. So here it is, largely unedited (albeit with a few changes that my teacher, who judged the essay "well written and scientifically mature", haven't seen). I have written a short glossary of terms at the end for the benefit of those with no education or special interest in biology. It's rather brief and incomplete though so feel free to ask about anything that's unclear.


Invasive Ants and Supercolonies: the Social Organisation of Invasive Linepithema humile and Solenopsis invicta

 

Felicia E. M. Gilljam

Ethology 10 credits, Department of Zoology, Stockholm University, 2006

 


The eusociality of ants is likely a big contributor to their widespread success around the globe. What could compete with such large groups of coordinated individuals? Possibly, only other ants are up to the task. Extensive polygyny, where each nest contains multiple reproductive queens, and loss of intraspecific aggression is often invoked as an important factor in the success of two common and well-studied invasive species, the Argentine ant and the red fire ant. However, the ultimate explanation to the differences in social organisation between introduced and native ants of these species remains uncertain.

Introduction

Two of the most well-studied species of ant, the red imported fire ant (Solenopsis invicta), and the Argentine ant (Linepithema humile), both originated in South America but have colonised large parts of the world with Mediterranean climate, their dispersal probably largely facilitated by humans. These species are considered pests on a variety of levels. Not only do they have urban and agricultural consequences as they invade homes and destroy crops, but their presence also has severe effects on the ecology of their new habitats. A study by Porter & Savignano (1990) shows that the presence of S. invicta drastically lowered species richness of native ants at a study site in Texas, as well as the biodiversity of arthropods other than ants. The red fire ant can also be considered a medical problem, as it is generally aggressive and the often multiple stings can lead to anaphylaxis, which may lead to death (McCubbin & Weiner 2002).

Both the red fire ant and the Argentine ant are extensively polygyne (i.e. having multiple egg-laying queens in one nest) in their introduced ranges, and it is likely that this, coupled with colony propagation by budding rather than obligate founding of new nests by lone queens, has been paramount to their success as invasive species. The loss of a single reproductive individual will not affect a polygyne nest as severely as a monogyne one, which means that it is difficult to control these species the way one manages other ants. Another important factor is that invasive Argentine ants and red fire ants frequently form so called supercolonies (Tsutsui & Suarez 2003), where many nests appear to work together with little if any intraspecific aggression. This lends them a great advantage, especially in interspecific interactions: unrelated but non-aggressive Argentine ants produce more eggs and workers, spend more time foraging and are less likely to abandon baits in the presence of competing ant species (Holway & Suarez 2004).

Supercolonies pose a problem for the evolutionary biologist: while the occurrence of eusociality, where many sterile individuals help their reproductive siblings, can be largely explained by means of kin selection, this theory is not applicable to extensive polygyny and supercolonies. Colonies of S. invicta in the United States normally contain a large number of unrelated queens compared to native colonies, where queens are few and closely related (Ross et al. 1996). A similar shift in social organisation can be observed in L. humile, which in its native range lives in small colonies and displays high intraspecific aggression, whereas the introduced ants appear to be largely unicolonial, with no intraspecific aggression even between ants that come from nests many hundreds of kilometres apart (Tsutsui & Suarez 2003).

In the following sections I will review this problem, bringing up proposed mechanisms for nestmate recognition, and how and why these mechanisms may have been altered in L. humile and S. invicta. As kin selection is dependent on the recognition of individuals with a similar genetic make-up, the workings of these recognition mechanisms is central to the understanding of ants. And understanding what might very well be the key to the invasive success of Argentine and red fire ants could prove to be our key to success in fighting the invasion.

Nestmate recognition

Eusocial insects usually live in family groups. The evolutionary origin of eusociality is commonly thought to be daughters helping their mothers rear siblings rather than reproduce on their own. The phenomenon is widespread among hymenopterans (more specifically ants, wasps and bees). This is often attributed to their haplodiploid genetic make-up, which results in sisters being more related to each other (sharing approximately 75% of their genes if they have the same father) than to their own offspring (with which they share 50%). The success of eusociality – where a “worker caste” helps a reproductive individual (the queen) instead of reproducing on their own – is dependent on there being functioning mechanisms for kin recognition. As nests are normally inhabited by one family group, nestmate recognition works as an alternative to kin recognition.

Ants and other hymenopterans have been shown to utilise a variety of chemical compounds for nestmate recognition. Many of them are cuticular hydrocarbons, and it is thought that these waxy substances originally evolved as an aid for desiccation resistance. The hydrocarbons are not proteins and their genetic basis is unknown (Tsutsui 2004). Liang & Silverman (2002) reports that the recognition cues of L. humile may be influenced by diet, such that ants from unrelated colonies that normally display aggressive behaviour towards each other ceased this after being reared on matching diets. However, other studies have failed to show similar results (Giraud et al. 2002).

It is however clear that while there is a clear genetic component of nestmate recognition, there is also a degree of learning or imprinting present in hymenopterans. Newly eclosed ants (just emerged from pupa) will imprint on the odours around them and use this template to judge conspecifics throughout their lifespan. It also appears that aggressive behaviour may change due to experience. Closely situated colonies will result in many worker encounters, which may cause the workers to reduce the amount of aggressive behaviour (the so called dear enemy strategy). Alternatively, in cases where asymmetrical aggression (where one colony is normally the attacker and the other a recipient of aggression) occurs, experience may change the workers’ behaviour to become more symmetrical (Thomas et al. 2004). As the recipient is nearly always the loser it will benefit a colony close to an aggressive conspecific to become more proactive.

When studying polygynous ants, it is important to remember that multiple queens in a nest does not necessarily mean that nestmates are unrelated to one another. The evolution of polygyny may be viewed as an analogue to the evolution of eusociality: when ecological factors place heavy constraints on the success of lone reproductives (e.g. a lack of suitable nesting sites), it may be better to join a nest rather than start a new one, even if it lowers the fecundity of individual queens (Ross 2001). A young queen may join her mother’s nest, kin selection placing no restraints on this. It is when you find multiple unrelated queens within a nest that polygyny is more difficult to explain.

The unicoloniality of L. humile

As previously stated, there is evidence that the Argentine ant introduced in the United States is extensively unicolonial, if not completely (Buczkowski et al. 2004). In Europe, Giraud et al. (2002) reports the existence of two supercolonies, the larger of which ranges from Italy to the Spanish Atlantic coast, covering a distance of 6,000 km, which makes it the biggest colony recorded. Although not truly unicolonial – a social organisation where no intraspecific aggression would occur – the size of these colonies makes L. humile stand out as one of the most cooperative organisms to date.

The question is how it came to be that this species, which in its native range lives in much smaller colonies (the biggest of which may reach 100m), ended up forming such large supercolonies. Tsutsui & Suarez (2003) argue that a severe genetic bottleneck has occurred during the Argentine ant’s introduction to the United States and California. They show that the genetic diversity is much greater in the native range than the introduced, and this could potentially explain the loss of intraspecific aggression. As nestmate recognition likely has a strong genetic basis, there needs to be a certain amount of variation in genetic makeup for ants to be able to differentiate between nestmates and non-nestmates. If this variation is lost, it is possible that what is left is similar enough that ants, upon encountering conspecifics from other nests, perceive them to be more closely related than they are.

This is not to say that ants within one supercolony are genetically identical. Ingram & Gordon (2003) show that there exists genetic structure in the introduced range. It is however uncertain if there is enough variation for the ants to recognise non-nestmates as such.

Interestingly, populations of L. humile in the southeast of the United States show a greater genetic variation than the supercolony of California. They also display a much higher degree of intraspecific aggression. Buczkowski et al. (2004) suggest that this is due to different patterns of invasion; the southeast may have been colonised repeatedly and separately by different South American populations. Also, lower winter temperatures and competition with S. invicta may explain a more measured invasion success in the southeast compared to California.

The situation in Europe is slightly different. The Argentine ant in southern Europe appears to have undergone some loss of variation, but the bottleneck events have not had such a pronounced effect as to explain the loss of intraspecific aggression. Giraud et al. (2002) instead hypothesise that upon introduction to Europe, the Argentine ant experienced relaxed ecological constraints, freed of native parasites and predators, and colonies could grow uninhibited. The main hindrance would then be intraspecific aggression. Colonies with a variety of recognition cues would spend a lot of time and effort on fighting, whereas colonies harbouring the most common alleles would have an advantage.

This sort of positive frequency dependent selection would eventually lead to a kind of genetic cleansing, whereby uncommon recognition cues are selected against and eventually disappear, enabling the ants to form giant supercolonies. Evidence of a similar phenomenon has subsequently been found in the United States (Tsutsui et al. 2003, reviewed in Tsutsui 2004). Ants from bigger supercolonies would often act as aggressors and attack ants from more genetically diverse but smaller colonies, this uneven distribution of costs producing a selection pressure for unicoloniality.

The green beard of S. invicta

While the origin and cause of unicoloniality in L. humile remains uncertain, and several different mechanisms appear to be at work, compelling evidence has been found for a rather more simple and elegant solution in the red fire ant S. invicta. Like the Argentine ant, S. invicta is mostly multicolonial in its native range, forming small colonies with high degrees of relatedness and high levels of intercolony aggression (Ross et al. 1996). The introduced ants however show a distinct polymorphism in social organisation. The polygynous form readily accepts new queens and show little aggression between colonies, whereas the monogyne form is multicolonial and will kill any intruding queens (reviewed in Tsutsui & Suarez 2003).

This polymorphism appears to be connected to a specific locus, GP-9 (General Protein-9), or an as yet undiscovered locus in strong linkage disequilibrium with GP-9 (Keller & Ross 1998, Krieger 2004). Two alleles are present at this locus in introduced ants: homozygotes for the B allele are monogynous, whereas heterozygotes are polygynous. Worker ants with the bb genotype appear to be very uncommon, and bb queens fail to reach reproductive age. Bb queens are smaller than BB and lack sufficient nutrient reserves to found their own colony. They may however enter an already polygynous colony and start laying eggs there. Additionally, Ross & Keller (2001) have shown that it is the genotype composition of workers that determines whether a nest is polygynous or monogynous, and that only 5-10% of the workers need to be heterozygous for the nest to behave polygynously.

Analysis of the GP-9 locus has shown that its product is most likely a Pheromone Binding Protein (PBP), which indicates that it may be involved in nestmate recognition (Krieger 2004). In short, the b allele of GP-9 fulfils all the criteria of a “green-beard gene”. Coined by Richard Dawkins, the green-beard effect refers to a gene that gives an individual a distinct phenotype, enables it to recognise this phenotype in others, and causes it to behave altruistically towards other individuals possessing the phenotype (Dawkins 1976). The beauty is that it can readily explain altruism between otherwise unrelated individuals, and in the case of red fire ants, does just that.

It is still not known what precise mechanism GP-9 is involved in. It could be that the b allele results in a deficient recognition mechanism, leading workers to treat all conspecifics the same. That would however not explain why a polygynous nest will not admit a BB queen.

The polygynous form of S. invicta was found in the United States 20 years after the first monogynous colonies. Either, the polygynous form does not exist in the native range, or it was introduced later. The latter alternative seems unlikely, however, as the polygynous form has a competitive advantage and will displace the monogyne form as well as other ant species.

The GP-9 locus has been investigated in other species (e.g. S. geminata) but a gene similar to the b allele has not been found (Krieger 2005).

Conclusions

Argentine ants and red fire ants share important elements of social organisation that appear to be the key behind their success as invasive species. However, as we have seen, what caused the formation of supercolonies may be drastically different in the two ants.

What does the future hold for these invasive species? A problem with the explanation for the lack of diversity in the introduced populations of Argentine ant being positive frequency dependent selection is that it is difficult to imagine how genetic diversity (on recognition cue loci) is maintained in native populations (Tsutsui 2004). Called Crozier’s paradox, this problem could partly be addressed by reproductive parasitism. In the face of such social parasitism, whereby reproductive individuals will enter the nests of unrelated conspecifics (or in some cases other species), selection should act to increase label variety and specificity. With this in mind, it is conceivable that L. humile and S. invicta will eventually reach a point where the selfishness of genes makes itself known again, and unicoloniality becomes less common.

Until then, for purposes of pest control, more research will be needed on the population biology of these species. As the formation of supercolonies has had such a great impact on the invasion success, it seems likely that a way of controlling this behaviour may be our best solution. Also, it may help prevent future invasions by other ant species, if we can detect the phenomenon in its infancy.

 

Acknowledgements

I would like to thank [Anonymous] and profmoriarty for excellent proofreading.

 

References

Buczkowski G, Vargo EL & Silverman J. 2004. The diminutive supercolony: the Argentine ants of the southeastern United States. Molecular Ecology 13:2235-2242.

Dawkins, R. 1976. The Selfish Gene. Oxford: Oxford University Press.

Giraud T, Pedersen JS & Keller L. 2002. Evolution of supercolonies: The Argentine ants of southern Europe. Proc Natl Acad Sci 99:6075-6079.

Holway DA, Suarez AV. 2004. Colony-structure variation and interspecific competitive ability in the invasive Argentine ant. Oecologia 138:216-222.

Ingram KK, & Gordon DM. 2003. Genetic analysis of dispersal dynamics in an invading population of argentine ants. Ecology 84:2832-2842.

Keller L & Ross KG. 1998. Selfish genes: a green beard in the red fire ant. Nature 394:573-575.

Krieger MJB. 2004. To b or not to b: a pheromone-binding protein regulates colony social organization in fire ants. BioEssays 27:91-99.

Liang D & Silverman J. 2000. “You are what you eat”: Diet modifies cuticular hydrocarbons and nestmate recognition in the Argentine ant, Linepithema humile. Naturwissenshaften 87:412-416.

McCubbin KI & Weiner JM. 2002. Fire ants in Australia: a new medical and ecological hazard. Medical Journal of Australia 176:518-519.

Porter SD & Savignano DA. 1990. Invasion of polygyne fire ants decimates native ants and disrupts arthropod community. Ecology 71:2095-2106.

Ross KG. 2001. Molecular ecology of social behaviour: analyses of breeding systems and genetic structure. Molecular Ecology 10:265-284.

Ross KG, & Keller L. 2001. Experimental conversion of colony social organization by manipulation of worker genotype composition in fire ants (Solenopsis invicta). Behav Ecol Sociobiol 51:287-295.

Ross KG, Vargo EL & Keller L. 1996. Social evolution in a new environment: The case of introduced fire ants. Proc Natl Acad Sci 93:3021-0325.

Thomas ML, Tsutsui ND, & Holway DA. 2004. Intraspecific competition influences the symmetry and intensity of aggression in the Argentine ant. Behavioral Ecology 16:472-481.

Tsutsui ND. 2004. Scents of self: The expression component of self/non-self recognition systems. Ann Zool Fennici 41:713-727.

Tsutsui ND & Suarez AV. 2003. The Colony Structure and Population Biology of Invasive Ants. Conservation Biology 17:48-58.

Tsutsui ND, Suarez AV & Grosberg RK. 2003. Genetic diversity, asymmetrical aggression, and recognition in a widespread invasive species. Proc Natl Acad Sci 100:1078-1083.

Glossary
Eusocial: Social organisation with caste distinctions; one or few reproductive females (queens) helped by their sisters or daughters that are sterile (workers).
Monogynous: Nests containing one queen.
Polygynous: Nests containing several queens.
Colony: A usually small aggregation of nests.
Supercolony: A very extensive colony.
Unicolonial: Hypothetical unicolonial ants would never fight each other. No truly unicolonial ant species exists (that we know of), but the Argentine ant comes close.
Conspecific: An individual of the same species.
Haplodiploid: Females contain two sets of chromosomes (like most animals) but males hatch from unfertilised eggs and only contain one set. (Haploid: only one set; Diploid: two sets.)
Frequency dependent selection: Natural selection that favours different variants of a gene depending on their frequency - positive FDS favours the common variant. An example of negative frequency dependent selection is the balance of sexes; if there is an abundance of males, it is better to be female, and vice versa.
Polymorphism: More than one variant/morph (genetic or phenotypic) exists.
Phenotype: The observable characteristics of an organism.
Allele: Different variants of a gene.
Locus: The point on a chromosome where a specific gene is located. Often used to mean a gene including all its variants (alleles).
Linkage disequilibrium: A bit of a complicated genetic term that I can't explain in brief, it's not particularly important either way.
Homozygote: Having two copies of the same allele at a specific locus (ie BB or bb).
Heterozygote: Having two different alleles at a specific locus (ie Bb).

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