Ants use the odour of the colony to discriminate nestmates. In some species, this odour is learned during the first days following emergence, and thus early experience has a strong influence on nestmate discrimination. Slave-making ants are social parasites that capture brood of other ant species to increase the worker force of their colony. After emerging in the slave-maker nest, slave workers work as if they were in their own colony. We tested the hypothesis that early experience allows the deception of commonly enslaved species, while non-host species use a different mechanism, which does not involve learning.
Pupae of a host species, Temnothorax unifasciatus, and a non-host species, T. parvulus, were allowed to emerge in the presence of workers of one of two slave-maker species, Chalepoxenus muellerianus or Myrmoxenus ravouxi. When T. unifasciatus was exposed to slave-makers for 10 days following emergence, they were more aggressive towards their own sisters and groomed the slave-maker more. T. parvulus gave a less clear result: while workers behaved more aggressively towards their sisters when exposed early to C. muellerianus workers, this was not the case when exposed early to M. ravouxi workers. Moreover, T. parvulus workers allogroomed conspecific nestmates less than T. unifasciatus. Allogrooming activity might be very important for the slave-makers because they are tended by their slaves.
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Our findings show that early experience influences nestmate discrimination in the ant T. unifasciatus and can account for the successful enslavement of this species. However, the non-host species T. parvulus is less influenced by the early environment. This might help to explain why this species is never used by social parasites.
Myrmoxenus ravouxi and Chalepoxenus muellerianus are among the most common slave-makers in Western Europe. They use several related species as slaves but show a preference for Temnothorax unifasciatus [21]. In the Mediterranean area, M. ravouxi, C. muellerianus and T. unifasciatus can be found in sympatry with T. parvulus, though T. unifasciatus seems to prefer more arid environments. T. parvulus has never been found as a slave, but the reason for this is unknown. We postulated that slavery would be prevented if nestmate discrimination in T. parvulus was not achieved through early learning of colony odour, because slave workers emerging in the slave-maker colony would recognize the slave-maker brood and workers as aliens.
Our results suggest that the environment experienced by T. unifasciatus during the first 10 days after emergence influences nestmate discrimination, at least in our artificial laboratory conditions. Indeed, workers that were exposed early to M. ravouxi and C. muellerianus displayed a very aggressive behaviour towards their own sisters and spent much time grooming the slave-makers. This suggests that the influence of the early environment could potentially account for the fact that T. unifasciatus slaves care for and defend the slave-makers. However, as host workers never emerge only with slave-makers present the mechanisms allowing enslavement could be different in nature. The same result was obtained for T. parvulus workers that were exposed to C. muellerianus. However, when exposed to M. ravouxi, they were not more aggressive toward their sisters than toward the slave-maker. These results partly confirm our hypothesis that the effect of early experience on the discrimination capabilities is reduced in T. parvulus when compared with T. unifasciatus workers.
The use of tethered, but live ants to record the reaction of test workers could have influenced their behaviour through the performance of antennation, biting, stridulation, etc., and the emission of pheromones. Indeed, several species of social parasites are known to use repellent, appeasement, and/or propaganda substances to usurp host nests [22]. The occurrence of such substances in our focal slave-maker species is likely and could have reduced aggressiveness of test workers. Moreover, several pupae of the test species were allowed to emerge in the glass tubes containing slave-makers. The early experience of test workers could then have been influenced by the other emerging test workers. Another potential source of bias in our results is the unequal representation of collected populations of Temnothorax in the experimental groups. The observed differences between our T. parvulus and T. unifasciatus might be due to differences between populations rather than species, if early experience had a smaller influence on nestmate discrimination in the Italian population. However, this possibility seems unlikely because species differences for fundamental mechanisms (such as the determinant of nestmate discrimination) are expected to be unaffected by population differences. The observed differences between the two species cannot be due to a mere difference in aggressiveness, because their levels of aggression towards slave-makers in the control experiment were not significantly different. However the difference between their levels of allogrooming was highly significant. A low basic level of allogrooming activity for T. parvulus workers was probably responsible for the fact that they did not groom their sisters more than the slave-makers in the control experiment. This makes it difficult to test the influence of early experience on allogrooming behaviour of T. parvulus.
For some slave-making species, host colony take-over by slave-maker queens requires acceptance by adult host workers that have had no previous exposure to slave-makers. The founding queen of many slave-making species has to enter a host nest, be accepted by the host workers, then kill and replace the resident queen [19]. Once the slave-making queen manages to kill the resident queen, the workers care for the new queen and rear her brood. The acceptance of the new queen does not require previous exposure to slave-makers because specialised behavioural and chemical strategies are involved [22]. For example, in the genus Polyergus, the young slave-maker queen does not bear any odour, and thus prevents the host workers from detecting her. The slave-maker queen then acquires the cuticular hydrocarbons of the host queen by physical contact and the host workers accept her as though she were there natal queen [32, 33]. The founding queen of M. ravouxi enters the Temnothorax host nest, reaches the queen, and slowly throttles her to death [34]. The chemical mechanism responsible for the acceptation of the M. ravouxi queen by the host workers remains to be elucidated.
Queens of other slave-making species including C. muellerianus, Harpagoxenus and Protomognathus evict all adult ants from the host nest and keep only the host brood. They thus rely completely on the manipulation of early experience even during colony foundation. The life history of slave-making ants suggests that the use of adult slaves without previous exposure to the slave-maker is costly or involves a highly specialised strategy. Manipulation of early experience by the slave-maker appears as the most parsimonious strategy, which reinforces the suggestion that it facilitated the evolution of slavery.
Early behavioural plasticity is a widespread mechanism in animals and is involved in a number of host-parasite systems. However, in most cases, this mechanism is used by the parasite to find its host. The European cuckoo is known to rely on habitat, probably in addition to other cues, which is learned when reared by the host [35], but it does not seem to imprint directly on the host [36]. In parasitoid wasps, preimaginal imprinting is involved in host selection [5]. In slave-making ants, imprinting was also shown to influence host selection during raids and colony foundation [37, 38].
A striking result of this study was that manipulating the early experience of T. parvulus had different consequences depending on the slave-maker species to which it was exposed; nestmate discrimination seemed to be influenced by C. muellerianus, but not by M. ravouxi. If T. parvulus was insensitive to experience at emergence due to a strict genetic system of odour discrimination or an earlier sensitive period, we would expect the same outcome for both slave-maker species. A possible explanation is that there is a limited set of odours that T. parvulus can learn and/or perceive at emergence. M. ravouxi and C. muellerianus likely have different chemical profiles and T. parvulus might be chemically more similar to C. muellerianus than to M. ravouxi. Thus, the latter could be out of the range of potentially learned patterns. As we show in our experiments, phylogenetically closely related ant species can display various sensitivities to the early environment. Thus, perhaps the mechanisms of nestmate discrimination differ as well.
Nestmate discrimination has been shown to be less influenced by social environment at emergence in the ant genus Camponotus than in the genus Formica [7]. It is therefore interesting that no species of Camponotus is parasitized by slave-makers, while many Formica species are hosts to slave-makers. Similarly, our results on T. parvulus, the non-slave species, suggest that plasticity at emergence is not the only determinant of nestmate discrimination. A first alternative possibility is that nestmate discrimination is determined during an earlier sensitive period. Indeed, studies in Camponotus floridanus and Cataglyphis cursor demonstrated the importance of larval stages for nestmate discrimination [39, 40]. As most slave-makers capture pupae preferentially, a nestmate discrimination mechanism based on larval experience might prevent these species from being enslaved. A second possibility is that nestmate discrimination in T. parvulus has a genetic component or is based on self-referent phenotype matching. T. nylanderi, a species very closely related to T. parvulus, has nestmate discrimination cues based on colony environment, and especially nest site material [41]. Even if T. parvulus can be expected to rely in part on a similar mechanism in the field, it could not have influenced our results because colonies were reared in identical artificial nests. Whatever the determinant of nestmate discrimination in this species, it can be an obstacle to slavery because at least some elements of the template involved in discrimination are established before the slaves are captured. Moreover, T. parvulus workers do not groom their nestmates often, which could be problematic for the slave-makers because they are tended by the slaves. These characteristics might partly explain why T. parvulus has never been found as slave. However, other factors could explain why M. ravouxi and C. muellerianus does not enslave T. parvulus. Social parasites in the tribe Formicoxenini are phylogenetically closely-related to their hosts [42]. It might be impossible for the social parasites to exploit more distant species as hosts because they would not share the same ecological and microhabitat requirements, or the same communication system. Slave-maker species could also be under selection to match the colony odour of the host species. Coevolution occurs between slave-making ants and their hosts [43, 44] and it has been shown that in slave-maker colonies both species have similar cuticular hydrocarbon profiles [45, 46]. It might therefore be easier for the host species to learn the more similar profile of the parasite, than for the non-host species. 2ff7e9595c
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