Abstract

Given the importance that the evolution of cooperation bears in evolutionary biology and the social sciences, extensive theoretical work has focused on identifying conditions that promote cooperation among individuals. In insects, cooperative or altruistic interactions typically occur amongst social insects and are thus explained by kin selection. Here we provide evidence that in Lutzomia longipalpis, a small biting fly and an important vector of leishmaniasis in the New World, cooperative blood-feeding in groups of non-kin individuals results in a strong decrease in saliva expenditure. Feeding in groups also strongly affected the time taken to initiate a bloodmeal and its duration and ultimately resulted in greater fecundity. The benefits of feeding aggregations were particularly strong when flies fed on older hosts pre-exposed to sand fly bites, suggesting that flies feeding in groups may be better able to overcome their stronger immune response. These results demonstrate that, in L. longipalpis, feeding cooperatively maximizes the effects of salivary components injected into hosts to facilitate blood intake and to counteract the host immune defences. As a result, cooperating sand flies enjoy enormous fitness gains. This constitutes, to our knowledge, the first functional explanation for feeding aggregations in this species and potentially in other hematophagous insects and a rare example of cooperation amongst individuals of a non-social insects species. The evolution of cooperative group feeding in sand flies may have important implications for the epidemiology of leishmaniasis.

Highlights

  • Phlebotomine sand flies (Diptera: Psychodidae) are important vectors of leishmaniasis, a parasitic disease affecting an estimated 1–1.5 millions people and causing over 50’000 deaths worldwide each year [1]

  • Feeding aggregations have been observed in the laboratory, including in the New World sand fly Lutzomyia longipalpis which is commonly reared for research on drugs, vaccines and chemical attractants (Fig. 1), The functional explanation of this ‘invitational effect’ [3], which in L. longipalpis has been shown to be mediated by a pheromone produced on the female maxillary palps [4] so far has eluded scientists

  • Cooperative or altruistic interactions are usually observed amongst genetically related social insects

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Summary

Introduction

Phlebotomine sand flies (Diptera: Psychodidae) are important vectors of leishmaniasis, a parasitic disease affecting an estimated 1–1.5 millions people and causing over 50’000 deaths worldwide each year [1]. The ‘cooperative feeding hypothesis’ would provide a simple explanation for the invitational effect observed in group-feeding sand fly species and, possibly, in a number of other group-feeding hematophagous dipteran species [4,7,8,9]. This hypothesis is intriguing from an evolutionary point of view because cooperative interactions in insects are usually seen in social insects where it occurs among related individuals and can be explained through kin selection [10,11]. As most Diptera, do not provide parental care to their offspring [12] and are known to disperse over substantial distances in search of hosts [13,14], cooperative feeding occurs amongst unrelated flies and would constitute a rare example of non-kin cooperation in insects

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