Social trematode parasites increase standing army size in areas of greater invasion threat

Abstract

Organisms or societies are resource limited, causing important trade-offs between reproduction and defence. Given such trade-offs, optimal allocation theory predicts that, for animal societies with a soldier caste, allocation to soldiers should reflect local external threats. Although both threat intensity and soldier allocation can vary widely in nature, we currently lack strong evidence that spatial variation in threat can drive the corresponding variation in soldier allocation. The diverse guild of trematode parasites of the California horn snail provides a useful system to address this problem. Several of these species form colonies in their hosts with a reproductive division of labour including a soldier caste. Soldiers are non-reproductive and specialized in defence, attacking and killing invading parasites. We quantified invasion threat and soldier allocation for 168 trematode colonies belonging to six species at 26 sites spread among 10 estuaries in temperate and tropical regions. Spatial variation in invasion threat was matched as predicted by the relative number of soldiers for multiple parasite species. Soldier allocation correlated with invasion threat at fine spatial scales, suggesting that allocation is at least partly inducible. These results may represent the first clear documentation of a spatial correlation between allocation to any type of caste and a biotic selective agent.

Factors that influence the caste ratio in a bacterial division of labour

“…Classic experiments with ants [7] and polyembryonic wasps [8] found that more soldiers were produced when colonies were exposed to higher levels of interspecific competition, and moreover that these shifts were adaptive. Similar results were recently reported in parasitic trematode worms that colonize snails as part of their complex life cycle [9,10]. As with ants and wasps, worms that developed in the presence of competition from other parasite species invested more heavily in defensive castes.…”

Variation between species, populations, groups and individuals in the fitness consequences of out-group conflict

“…For instance, in the Ngorongoro Crater, Tanzania, which has a high population density of African lions, females are more likely to respond to experimentally simulated territory intrusions than do lionesses in the Serengeti, Tanzania, which has a lower population density [ 115 ]. Similarly, trematode colonies within snails may invest in a bigger ‘standing army’ in areas with higher prevalence of competitors [ 116 ]. Diana monkey, Cercopithecus diana , groups in a forest with high population density (where intergroup competition is high) exhibit greater aggression towards neighbours cf.…”

“…turtle ants, Cephalotes rohweri [ 167 ]; trematode spp. [ 116 ]); these individuals overwhelmingly deal with conspecific competition and thus bear the costs. In vertebrates, sex and dominance most commonly affect participation levels.…”

The weird eusociality of polyembryonic parasites

“…In aphids and thrips, soldiers are associated with host plants that prolong gall formation [ 21 , 79 ], but comparable metrics are not yet supported in polyembryonic wasps or trematodes. In theory, when parasite niches overlap, the fitness benefits of aggressive interference (and thus soldier morphs) should positively correlate with host characteristics that increase susceptibility (or exposure [ 13 ]) to parasite co-infections. We will learn more about the selective conditions favouring soldier castes with further understanding of parasite competitive ecology, which, serendipitously, is also a potentially useful avenue of research for medically relevant parasitology [ 80 , 81 ].…”

“…Recently, however, larval colonies of trematodes (i.e. flatworms, blood flukes) are argued to be eusocial, following the discovery of morphologically distinct soldier castes [7], and this claim has received growing support [8][9][10][11][12][13]. This discovery is unexpected and exciting, extending our social evolutionary theories into a phylum (Platyhelminthes) that seemingly had no relevance to social evolution research.…”