Is parasite pressure a driver of chemical cue diversity in ants?

Abstract

Parasites and pathogens are possibly key evolutionary forces driving recognition systems. However, empirical evidence remains sparse. The ubiquitous pioneering ant Formica fusca is exploited by numerous socially parasitic ant species. We compared the chemical cue diversity, egg and nest mate recognition abilities in two Finnish and two UK populations where parasite pressure is high or absent, respectively. Finnish populations had excellent egg and nest mate discrimination abilities, which were lost in the UK populations. The loss of discrimination behaviour correlates with a loss in key recognition compounds (C 25 -dimethylalkanes). This was not owing to genetic drift or different ecotypes since neutral gene diversity was the same in both countries. Furthermore, it is known that the cuticular hydrocarbon profiles of non-host ant species remain stable between Finland and the UK. The most parsimonious explanation for the striking difference in the cue diversity (number of C 25 -dimethylalkanes isomers) between the UK and Finland populations is the large differences in parasite pressure experienced by F. fusca in the two countries. These results have strong parallels with bird (cuckoo) studies and support the hypothesis that parasites are driving recognition cue diversity.

A social insect fertility signal is dependent on chemical context

“…If a single compound were sufficient for mimicking a queen, social parasites would not need to replicate or obtain more complete profiles and an individual with a profile lacking nestmate signals but displaying the correct fertility signals would be an omnipotent parasite of the host species. However, resistance to parasitism in ants and wasps is thought to evolve by increasing the diversity and complexity of the nestmate recognition signals coded in the cuticular profiles, supporting the notion that a complex chemical background is advantageous because it inhibits mimicry [22].…”

The influence of slavemaking lifestyle, caste and sex on chemical profiles in Temnothorax ants: insights into the evolution of cuticular hydrocarbons

“…In non-parasitic species, workers possessed more dimethyl-alkanes than virgin queens and males, and males exhibited higher abundances than virgin queens (figure 2d). Slavemaker castes did not vary in the relative abundance of putative recognition substances [27], but within the non-parasitic species, workers carried relatively more recognition substances than virgin queens and males, whereas males and virgin queens did not differ (figure 2e). Absolute CHC quantities were generally highest in workers and were unaffected by lifestyle (figure 2f).…”

“…Hosts may be forced to integrate such parasites, because discriminating against individuals deficient of recognition cues would lead to rejection of young ants that have just developed their hydrocarbon profile [32]. In turn, the higher relative abundance of methyl-alkanes in hosts might be a counter-adaptation to enhance their discriminative ability against slavemakers [26] next to more diverse chemical profiles [26,27]. Slavemakers possessed similar total CHC quantities as their hosts, and thus were not chemically insignificant sensu [32].…”

“…Queens communicate their fertility through their CHC profile and/or glandular secretions [2]. Besides these functions, CHCs experience selection from social parasites [26,27], which are thought to be a major driver of recognition cue diversity [28,29].…”

How do cuticular hydrocarbons evolve? Physiological constraints and climatic and biotic selection pressures act on a complex functional trait

“…Chemical profiles within Drosophila also change across latitudinal gradients [16], suggesting that environmental factors can affect CHC evolution. Moreover, ant colonies from populations with social parasites show more diverse CHC profiles, suggesting that parasites select for higher cue diversity [17,18]. Besides, there are non-heritable CHC differences owing to environmental factors like food [19,20], host species [21], nest site material [22], short-term acclimation to climatic conditions [23,24] or changes in social status [25].…”