The possible role of ant larvae in the defence against social parasites

Abstract

Temporary social parasite ant queens initiate new colonies by entering colonies of host species, where they begin laying eggs. As the resident queen can be killed during this process, host colonies may lose their entire future reproductive output. Selection thus favours the evolution of defence mechanisms, before and after parasite intrusion. Most studies on social parasites focus on host worker discrimination of parasite queens and their offspring. However, ant larvae can also influence brood composition by consuming eggs. This raises the question whether host larvae can aid in preventing colony takeover by consuming eggs laid by parasite queens. To test whether larvae could play a role in anti-parasite defence, we compared the rates at which larvae of a common host species, Formica fusca , consumed eggs laid by social parasite, non-parasite, nest-mate, or conspecific non-nest-mate queens. Larvae consumed social parasite eggs more than eggs laid by a heterospecific non-parasite queen, irrespective of the chemical distance between the egg cuticular profiles. Also, larvae consumed eggs laid by conspecific non-nest-mate queens more than those laid by nest-mate queens. Our study suggests that larvae may act as players in colony defence against social parasitism, and that social parasitism is a key factor shaping discrimination behaviour in ants.

Brood recognition and discrimination in ants

“…One explanation for precise discrimination between nestmate and non-nestmate eggs in F. fusca is the potential threat of intraspecific parasitism, which occurs when a founding queen takes over an established conspecific colony and hijacks its workforce. Low relatedness among F. fusca nestmate queens (Hannonen et al 2004;Bargum et al 2007) and the fact that even larvae seem to discriminate between nestmate and nonnestmate eggs (Pulliainen et al 2019) support the idea that intraspecific parasitism shapes discrimination abilities in this species. Together, these results underline that phylogeny, ecology and within-colony social context are major factors mediating conspecific brood discrimination.…”

“…Nevertheless, a study on egg signature mixtures in Formica ants showed that egg chemical profiles are highly variable and potentially provide sufficient information for discrimination between matrilines within nests (Helanterä and d'Ettorre 2014). Whether or not this information is used likely depends on species-specific biology: in contrast to F. exsecta, F. fusca is a common host to ant social parasites and displays excellent discrimination abilities (Helanterä and Sundström 2007;Helanterä and Ratnieks 2009a;Chernenko et al 2011Chernenko et al , 2013Helanterä et al 2011;Martin et al 2011;Pulliainen et al 2019). Contrasting patterns of brood discrimination in different species may thus be linked to differential selection pressures.…”

“…This species is a common host to temporary social parasites, whose queens found their colonies in the host nest (Punttila 1996). In populations with high parasite pressure, F. fusca exhibits excellent discrimination abilities, and both adult workers and larvae can discriminate against non-nestmate conspecific and heterospecific eggs (Helanterä and Sundström 2007;Helanterä and Ratnieks 2009a;Chernenko et al 2011Chernenko et al , 2013Martin et al 2011;Pulliainen et al 2019), most likely with the help of colony-specific egg odors (Helanterä and d'Ettorre 2014). Whether discrimination actually occurs depends on factors such as queen presence and exposure of young workers to foreign odors (Helanterä and Sundström 2007;Helanterä and Ratnieks 2009a;Chernenko et al 2013).…”

De novo transcriptome assembly and its annotation for the black ant Formica fusca at the larval stage

“…Perhaps due to high parasite pressure, F. fusca workers and larvae exhibit precise discrimination abilities against con- and heterospecific individuals 20–25 , making it an ideal species to study the molecular correlates of communication. In addition, F. fusca larvae have been shown to consume both con- and heterospecific eggs 25,26 , showing that even larvae are able to discriminate friend from foe. This provides the unique opportunity to study how nutritional stimulation in the form of egg consumption affects developmental gene expression.…”

Sex ratio and sexual conflict in a collective action problem

“…Although our study design made it difficult to disentangle whether female-biased groups cooperated more simply because they had more females (that each contribute more) or whether males too increase their effort in the presence of many sisters, our results raise the possibility that D. pini larvae have some means to recognize their kin as well as the sex of the other individuals in the group, adjusting their cooperative behaviour accordingly. Potential mechanisms include CHP-compounds, already known to be important in nest-mate recognition both in immature and mature life-stages in eusocial ant species (28, 29). In this context, it is interesting to note that individuals were divided into the experimental groups as smaller instars, and differences in their defensive behaviour were consistent until the last larval instar.…”