Comprehensive phylogeny of apid bees reveals the evolutionary origins and antiquity of cleptoparasitism

Abstract

Apidae is the most speciose and behaviorally diverse family of bees. It includes solitary, eusocial, socially parasitic, and an exceptionally high proportion of cleptoparasitic species. Cleptoparasitic bees, which are brood parasites in the nests of other bees, have long caused problems in resolving the phylogenetic relationships within Apidae based on morphological data because of the tendency for parasites to converge on a suite of traits, making it difficult to differentiate similarity caused by common ancestry from convergence. Here, we resolve the evolutionary history of apid cleptoparasitism by conducting a detailed, comprehensive molecular phylogenetic analysis of all 33 apid tribes (based on 190 species), including representatives from every hypothesized origin of cleptoparasitism. Based on Bayesian ancestral state reconstruction, we show that cleptoparasitism has arisen just four times in Apidae, which is fewer times than previously estimated. Our results indicate that 99% of cleptoparasitic apid bees form a monophyletic group. Divergence time estimates reveal that cleptoparasitism is an ancient behavior in bees that first evolved in the late Cretaceous 95 Mya [95% highest posterior density (HPD) = 87-103]. Our phylogenetic analysis of the Apidae sheds light on the macroevolution of a bee family that is of evolutionary, ecological, and economic importance.ancestral state reconstruction | apidae | divergence dating | kleptoparasitism | molecular phylogeny A pidae is the largest family of bees, with over 5,600 described species. The family includes the most important managed pollinator (Apis mellifera, the honey bee) and the only bees domesticated by humans for honey production (1). The honey bee is one of the more important model organisms, especially for all aspects of eusociality (2-5). Apid species represent a rich diversity of solitary, social, and parasitic lifestyles, and they pollinate a wide variety of agricultural and native plants. Despite the importance of this group, a robust comparative framework for evolutionary studies on the ecological and behavioral diversity of apid bees is lacking, primarily because of problems caused by the high proportion of cleptoparasitic species (28%) and tribes (50%).Cleptoparasitism (or kleptoparasitism), which involves the stealing of food or nesting material by one animal from another, is a widespread phenomenon found in many animal groups, including birds (6), bees (7), wasps (8), spiders (9), fish (10), and mammals (11). In bees, cleptoparasitic species do not build or provision their own nests; instead, they enter the nests of other bees and lay their eggs in either closed or open, partially provisioned brood cells (12). In a few cases, the adult female parasite destroys the host egg (13), but more commonly, a specialized larval instar kills the host larva (14). The parasitic larva then consumes the pollen and nectar provisions gathered by the host adult and completes its development before emerging from the host nest. This form of parasitism differs from t...

Long-term morphological stasis maintained by a plant–pollinator mutualism

“…Together, these results firmly support the hypothesis by Anderson (12) suggest that this association likely arose much earlier, at least 75 Myr (17,22,42,43). These results argue against a primary role for intrinsic factors, such as genetic or developmental constraints, in shaping floral evolution in Malpighiaceae.…”

Genes involved in convergent evolution of eusociality in bees

“…Bee species and evolutionary models used to identify genes evolving rapidly in eusocial lineages. (A) Phylogeny of species in study based on previously published trees (9)(10)(11) and EST data (SI Text). Some analyses of EST data yielded an alternative topology; molecular evolutionary analyses performed with each topology gave highly similar results (SI Text and Table S2).…”

“…There is a wide diversity of social lifestyles within this group, from solitary to intermediately social to elaborate eusociality (8). Additionally, eusociality has been gained independently at least six times (9)(10)(11)(12) in the bees, more than in any other group. These features make it possible to compare multiple, independent origins of different social lifestyles among relatively closely related species.…”

Floral-oil-producing Plantaginaceae species: geographical distribution, pollinator rewards and interactions with oil-collecting bees

“…In Apinae the oil-collecting behavior is polyphyletic according to morphological (Roig-Alsina & Michener 1993) and molecular phylogenies (Cardinal et al 2010), and this behavior is present in four tribes: Centridini, Ctenoplectrini, Tapinotaspidini and Tetrapediini.…”