Abstract

A long-standing controversy in bee social evolution concerns whether highly eusocial behavior has evolved once or twice within the corbiculate Apidae. Corbiculate bees include the highly eusocial honey bees and stingless bees, the primitively eusocial bumble bees, and the predominantly solitary or communal orchid bees. Here we use a model-based approach to reconstruct the evolutionary history of eusociality and date the antiquity of eusocial behavior in apid bees, using a recent molecular phylogeny of the Apidae. We conclude that eusociality evolved once in the common ancestor of the corbiculate Apidae, advanced eusociality evolved independently in the honey and stingless bees, and that eusociality was lost in the orchid bees. Fossil-calibrated divergence time estimates reveal that eusociality first evolved at least 87 Mya (78 to 95 Mya) in the corbiculates, much earlier than in other groups of bees with less complex social behavior. These results provide a robust new evolutionary framework for studies of the organization and genetic basis of social behavior in honey bees and their relatives.

Highlights

  • Eusociality, characterized by reproductive division of labor, cooperative brood care, and overlap of generations, is considered one of the key innovations that has allowed ants, bees, and termites to become the dominant organisms in terrestrial ecosystems [1]

  • These results imply a single origin of eusocial behavior in the corbiculate bees with two independent origins of advanced eusocial behavior, and a reversal from primitively eusocial to solitary/communal nesting in some orchid bees

  • Evolution of eusociality According to our model-based ancestral state reconstructions, the ancestral state for corbiculate bees appears to be primitive eusociality (Fig. 1, Table S2)

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Summary

Introduction

Eusociality, characterized by reproductive division of labor, cooperative brood care, and overlap of generations, is considered one of the key innovations that has allowed ants, bees, and termites to become the dominant organisms in terrestrial ecosystems [1]. One of the primary controversies in the evolution of sociality in bees lies within the corbiculates (Hymenoptera: Apidae), where a single versus dual-origin hypothesis for highly eusocial behavior has been extensively debated. There are four extant monophyletic tribes: the highly eusocial Apini (honey bees) and Meliponini (stingless bees), the primitively eusocial Bombini (bumble bees), and the mostly solitary, communal, and weakly social Euglossini (orchid bees). The advanced eusocial Apini and Meliponini have morphologically distinct queens and workers with new nests founded by swarms [8], whereas the primitively eusocial Bombini have queens and workers that differ only in size, with new nests established by a single foundress. Non-parasitic orchid bees are usually referred to as being solitary or communal [9], but hints of more advanced forms of social behavior, including overlap of generations and cooperative brood care, have been reported in some taxa [10,11]

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