Specialization makes resource use more efficient and should therefore be a common process in animal evolution. However, this process is not as universal in nature as one might expect. Our study shows that Sphecodes (Halictidae) cuckoo bees frequently change their host over the course of their evolution. To test the evolutionary scenario of host specialization in cuckoo bees, we constructed well-supported phylogenetic trees based on partial sequences of five genes for subtribe Sphecodina (Halictini). We detected up to 17 host switches during Sphecodes evolution based on 37 ingroup species subject to mapping analysis of the hosts associated with the cuckoo bee species. We also examine the direction of evolution of host specialization in Sphecodes using the likelihood ratio test and obtain results to support the bidirectional evolutionary scenario in which specialists can arise from generalists, and vice versa. We explain the existence of generalist species in Sphecodes based on their specialization at the individual level, which is recently known in two species. Our findings suggest flexible host choice and frequent host switches in the evolution of Sphecodes cuckoo bees. This scenario leads us to propose an individual choice constancy hypothesis based on the individual specialization strategy in cuckoo bees. Choice constancy has a close relationship to flower constancy in bees and might be an extension of the latter. Our analysis also shows relationships among the genera Microsphecodes, Eupetersia, Sphecodes and Austrosphecodes, a formerly proposed Sphecodes subgenus. Austrosphecodes species form a basal lineage of the subtribe, and Microsphecodes makes it paraphyletic.

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