Intraspecific aggression and colony structure in invasive Myrmica rubra populations

In an recently published article in Myrmecological News entitled “Population structure of Myrmica rubra (Hymenoptera: Formicidae) in part of its invasive range revealed by nuclear DNA markers and aggression analysis”, Hicks & Marshall examine patterns of aggression between introduced populations of the invasive European fire ant in Maritime Canada. Using field-collected nests, the authors performed laboratory assays to characterize aggressive behavior between workers from colonies separated by a range of geographic and genetic distances. Genetic analyses were carried out using six polymorphic microsatellites markers to calculate neutral genetic distance (pairwise FST) among 16 sites of collection, including two in the native range (Germany and England). In a nutshell, the authors report a positive relationship between pairwise genetic distance between source populations and the occurrence of aggressive displays (grabbing and stinging) among paired workers from different colonies.

A Review compiled by Jeff Garnas

Please note that the term supercolony was used throughout the text as defined by Helanterä & al. (2009), who state that “a supercolony is an extreme form of polydomy, where the colony is so large that direct interactions between workers from separated nests become impossible.” Thus, one or more supercolonies may be present in a single site, or single supercolonies can span multiple, discrete sites, particularly in the context of biological invasion.

This is an interesting study and further supports earlier published findings that Myrmica rubra is not truly supercolonial in its invasive range (Garnas & al. 2007, Chen & al. 2018). The hypothesis of supercoloniality in this species emerged from the observation that despite extremely high nest densities (i.e., up to 4 nests m-2 in coastal Maine; Groden & al. 2005), M. rubra workers exhibit minimal observable aggressive behavior within local sites. Myrmica rubra is highly polydomous (its colonies span multiple nests) and polygynous (multiple queens co-occur in single colonies and nests) in North America and in parts of its native range (Elmes 1973, Groden & al. 2005, Fürst & al. 2012). Both of these traits have in some cases been associated with the formation of low-relatedness “supercolonies” and a breakdown in colony borders (van der Hammen & al. 2002). Finally, supercoloniality was once considered to arise as a consequence of ant invasion, where reduced genetic diversity in introduced populations correlates with uniformity in discrimination cues, typically cuticular hydrocarbon signature (Starks 2003). The postulated link between invasive status and supercoloniality has since been cast into doubt, however, due largely to the discovery of 1) supercoloniality in the native range of the Argentine ant and other species, including M. rubra (Huszar & al. 2014); and 2) intact nestmate recognition mechanisms within supercolonies that permit the detection of non-nestmates without triggering an aggressive response (Pedersen & al. 2006, Jackson 2007).


Myrmica rubra forager en route to tend an aphid colony in a paper birch canopy; Mt. Desert Island, Maine. (© Jeff Garnas)

 

That M. rubra does not form supercolonies in eastern North America is an increasingly robust conclusion that may in part reflect relatively high levels of genetic diversity in the ant’s invasive range. According to the authors of the current study, aggression increases with neutral genetic distance between populations. This assertion should be interpreted carefully, however. For example, while colonies from strongly differentiated populations did reliably exhibit aggression toward one another when workers were paired in arena assays, the inverse was not always true. This may reflect the reality that the relationship between neutral genetic distance and aggression is not precisely clear. For example, populations that are moderately to strongly differentiated (via lack of gene flow and/or as a consequence of genetic bottlenecks, drift and/or admixture) may still share a common “identity,” either via selection for uniformity (Starks 2003) or if colony odor and detection genes are fixed. On the flipside, relatedness may be low between randomly selected colony pairs even when selected from highly interconnected or otherwise similar populations, where pairwise estimates of genetic distance are negligible.

 

It is interesting to note that in the current paper, aggressive responses between colonies from minimally differentiated populations were more challenging to predict than those among highly differentiated populations. Two out of five colony pairs (40%) from minimally divergent populations (pairwise FST 0.04 and 0.05 respectively) displayed largely aggressive responses (Fig. 2). The logistic regression curve (blue line in Fig. 2) predicts non-zero aggression at the y-intercept, where FST = 0. It is important to note that the logistic regression curve should be interpreted carefully as the points at each level of FST represent twenty assays with different workers from the same colony pairs and are therefore not truly independent statistically. Still, this result is consistent with the finding that colonies of M. rubra on Mt. Desert Island, Maine do in fact display moderate aggression even within local populations, albeit at a lower frequency and intensity than colonies collected from discrete sites on the island (Garnas & al. 2007). Also, while aggression is often measured as relative frequency and duration of aggressive behaviors, this complex response is often simplified to a binary variable (aggressive vs. not aggressive). This is perhaps appropriate but likewise glosses over the fact that gradations of aggression do apparently exist both within and among colonies and populations, and that such responses are to some degree context-dependent (Buczkowski & Silverman 2005).

 

Logistic regression using form data extracted from Hicks & Marshall 2018 (Table 5). Each dot represents the outcome of paired worker aggression assays (yes or no, 1 or 0). Each color/pairwise FST combination represents a single paired colony (20 worker assays per colony pair). Points are jittered for visibility.

 

The hypothesis of supercoloniality in invasive M. rubra populations was a reasonable one given the species’ impressive nest densities and highly polygynous and polydomous habit (which blurs the lines between adjacent nests and colonies and complicates expectations of relatedness). However, Hicks and Marshall have further confirmed that this idea clearly lacks empirical support and should no longer be considered. Individual populations of M. rubra exhibit relatively high levels of genetic diversity, which in some populations is higher than levels detected in native populations (based on heterozygosity estimates from this study). Pairwise genetic distance estimates likewise peak somewhere around 10 km and are therefore highest among relatively nearby sites within the invasive range (Fig. 3). This ant has been introduced at least four times into maritime Canada from different parts of Europe (Hicks & al. 2014). Multiple introductions and the resulting heterogeneous distribution of source “lineages” (with or without admixture) is increasingly recognized as common for many invasive taxa, including ants (Garnas & al. 2016, Bertelsmeier & al. 2018). The ecological and evolutionary consequences of such complex patterns of spread is a fascinating area of active research (recently reviewed in Garnas et al. 2016 and in Garnas 2018). Explicit consideration of invasion history and patterns of local and regional genetic diversity and identity may shed light on our understanding and interpretation of observed variation in inter-colony aggression in invasive ants. Interestingly, however, colony organization in M. rubra appears to be at least superficially similar to that in Finland, where colonies are also highly polydomous and show low worker relatedness. According to recent research (Sorvari 2017), Finnish colonies readily accept unrelated queens, particularly into worker-only nests. Myrmica rubra might represent a case where ecological context is a primary driver of the expression of social phenotype, which appears to be relatively plastic in this and other ant species.

Genetic distance estimates (pairwise FST) as a function of the natural log of geographic (Great Circle) distance. Site coordinates and pairwise genetic distance matrix extracted from Tables 1 and 4 in Hicks & Marshall 2018.

 

References

Bertelsmeier, C., Ollier, S., Liebhold, A.M., Brockerhoff, E.G., Ward, D. & Keller, L. 2018: Recurrent bridgehead effects accelerate global alien ant spread. – Proceeding of the National Academy of Science U S A 115: 5486-5491.

Buczkowski, G. & Silverman, J. 2005: Context-dependent nestmate discrimination and the effect of action thresholds on exogenous cue recognition in the Argentine ant. – Animal Behavior 69: 741-749.

Chen, W.E.N., O’Sullivan, Á. & Adams, E.S. 2018: Intraspecific aggression and the colony structure of the invasive ant Myrmica rubra. – Ecological Entomology 43: 263-272.

Elmes, G. 1973: Observations on the density of queens in natural colonies of Myrmica rubra L. (Hymenoptera: Formicidae). – Journal of Animal Ecology 42: 761-771.

Fürst, M.A., Durey, M. & Nash, D.R. 2012: Testing the adjustable threshold model for intruder recognition on Myrmica ants in the context of a social parasite. – Proceedings of the Royal Society B-Biological Sciences 279: 516-522.

Garnas, J.R. 2018: Rapid evolution of insects to global environmental change: conceptual issues and empirical gaps. – Current Opinion in Insect Science 29: 93-101.

Garnas, J.R., Auger-Rozenberg, M.A., Roques, A., Bertelsmeier, C., Wingfield, M.J., Saccaggi, D.L., Roy, H.E. & Slippers, B. 2016: Complex patterns of global spread in invasive insects: eco-evolutionary and management consequences. – Biological Invasions 18: 935-952.

Garnas, J.R., Drummond, F.A. & Groden, E. 2007: Intercolony aggression within and among local populations of the invasive ant, Myrmica rubra (Hymenoptera: Formicidae), in coastal Maine. – Environ Entomol 36: 105-113.

Groden, E., Drummond, F.A., Garnas, J. & Franceour, A. 2005: Distribution of an invasive ant, Myrmica rubra (Hymenoptera: Formicidae), in Maine. – Journal of Economic Entomology 98: 1774-1784.

Hicks, B.J. & Marshall, H.D. 2018: Population structure of Myrmica rubra (Hymenoptera: Formicidae) in part of its invasive range revealed by nuclear DNA markers and aggression analysis. – Myrmecological News 28: 35-43.

Hicks, B.J., Pilgrim, B.L. & Marshall, H.D. 2014: Origins and genetic composition of the European fire ant (Hymenoptera: Formicidae) in Newfoundland, Canada. – The Canadian Entomologist: 1-8.

Huszar, D.B., Larsen, R.S., Carlsen, S., Boomsma, J.J. &Pedersen, J.S. 2014: Convergent development of ecological, genetic, and morphological traits in native supercolonies of the red ant Myrmica rubra. – Behavioral Ecology andSociobiology 68: 1859-1870.

Jackson, D.E. 2007: Social evolution: pathways to ant unicoloniality. – Current Biology 17: 1063-1064.

Pedersen, J.S., Krieger, M.J., Vogel, V., Giraud, T. & Keller, L. 2006: Native supercolonies of unrelated individuals in the invasive Argentine ant. – Evolution 60: 782-791.

Sorvari, J. 2017: Acceptance of alien queens by the ruby ant Myrmica rubra (Hymenoptera: Formicidae): Gene flow by queen flow. – European Journal of Entomology 114: 230-234.

Starks, P. 2003: Selection for uniformity: xenophobia and invasion success. – Trends in Ecology and Evolution 18: 159-162.

van der Hammen, T., Pedersen, J. & Boomsma, J. 2002: Convergent development of low-relatedness supercolonies in Myrmica ants. – Heredity 89: 83-89.

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