Phylogenetic relationships and the evolution of host preferences in the largest clade of brood parasitic bees (Apidae: Nomadinae).

Brood parasites (also known as cleptoparasites) represent a substantial fraction of global bee diversity. Rather than constructing their own nests, these species instead invade those of host bees to lay their eggs. Larvae then hatch and consume the food provisions intended for the host's offspring. While this life history strategy has evolved numerous times across the phylogeny of bees, the oldest and most speciose parasitic clade is the subfamily Nomadinae (Apidae). However, the phylogenetic relationships among brood parasitic apids both within and outside the Nomadinae have not been fully resolved. Here, we present new findings on the phylogeny of this diverse group of brood parasites based on ultraconserved element (UCE) sequence data and extensive taxon sampling with 114 nomadine species representing all tribes. We suggest a broader definition of the subfamily Nomadinae to describe a clade that includes almost all parasitic members of the family Apidae. The tribe Melectini forms the sister group to all other Nomadinae, while the remainder of the subfamily is composed of two sister clades: a "nomadine line" representing the former Nomadinae sensu stricto, and an "ericrocidine line" that unites several mostly Neotropical lineages. We find the tribe Osirini Handlirsch to be polyphyletic, and divide it into three lineages, including the newly described Parepeolini trib. nov. In addition to our taxonomic findings, we use our phylogeny to explore the evolution of different modes of parasitism, detecting two independent transitions from closed-cell to open-cell parasitism. Finally, we examine how nomadine host-parasite associations have evolved over time. In support of Emery's rule, which suggests close relationships between hosts and parasites, we confirm that the earliest nomadines were parasites of their close free-living relatives within the family Apidae, but that over time their host range broadened to include more distantly related hosts spanning the diversity of bees. This expanded breadth of host taxa may also be associated with the transition to open-cell parasitism.

Biogeography and early diversification of Tapinotaspidini oil-bees support presence of Paleocene savannas in South America.

Worldwide distributed tropical savannas were established only in the Miocene, with climatic cooling and rise of C4 grasses. However, there is evidence for an earlier presence of savanna-like vegetation in southern parts of South America. Here we investigated the biogeographic history of a clade of solitary bees which have endemic groups in areas covered by savannas and other types of open vegetation as well as forested areas. We hypothesized that these bees originated in savanna-like biomes and that shifts to forested areas and floral host shifts increased species diversification along their evolutionary history. We reconstructed a comprehensive phylogeny for Tapinotaspidini bees based majorly on original DNA sequences. We then used macroevolutionary tools to estimate ancestral range area and reconstructed ancestral habitat (open versus forested) and host plant association to analyze the effects of shifts in vegetation type and flower hosts on their diversification. Tapinotaspidini bees originated in the Paleocene and in a savanna-type, Cerrado-like, which is reinforced by reconstruction of open vegetation as the most probable ancestral area, thus bringing additional evidence to a much earlier origin of this vegetation type in South America. Shifts to forested areas occurred at least three times in a period of 30 Ma and were responsible for slight increases in diversification rates. Malpighiaceae is the ancestral floral host; host broadening occurred only in the Miocene and at least in three occasions. Host shifts, i.e. from Malpighiaceae to other oil families, occurred in the Eocene and Miocene. Both host broadening and host shifts did not significantly alter diversification rates, however exploitation of other oil sources were important in occupying new habitats. The link between biomes and host plant shifts and changes in diversification rate brings us additional insights into the evolution of bees and associated flora in South America.

Gain and loss of specialization in two oil-bee lineages, Centris and Epicharis (Apidae).

It is plausible that specialized ecological interactions constrain geographic ranges. We address this question in neotropical bees, Centris and Epicharis, that collect oils from flowers of Calceolariaceae, Iridaceae, Krameriaceae, Malpighiaceae, Plantaginaceae, or Solanaceae, with different species exploiting between one and five of these families, which either have epithelial oil glands or hair fields. We plotted the level of oil-host specialization on a clock-dated phylogeny for 22 of the 35 species of Epicharis and 72 of the 230 species of Centris (genera that are not sister genera) and calculated geographic ranges (km(2) ) for 23 bee species based on collection data from museum specimens. Of the oil-offering plants, the Malpighiaceae date to the Upper Cretaceous, whereas the other five families are progressively younger. The stem and crown groups of the two bee genera date to the Cretaceous, Eocene, and Oligocene. Shifts between oil hosts from different families are common in Centris, but absent in Epicharis, and the direction is from flowers with epithelial oil glands to flowers with oil hairs, canalized by bees' oil-collecting apparatuses, suitable for piercing epithelia or mopping oil from hair fields. With the current data, a link between host specialization and geographic range size could not be detected.

Several origins of floral oil in the Angelonieae, a southern hemisphere disjunct clade of Plantaginaceae.

UNLABELLED: • PREMISE OF THE STUDY: Over the past 75 Myr, successive groups of plants have entered the "oil bee pollination niche," meaning that they depend on oil-collecting bees for their pollination. The highly dissimilar numbers of plant species and bee species involved in these mutualisms imply evolutionary host switching, asymmetric mutual dependencies, and uncoupled diversification. Among the clades with the best field data on oil bee behavior is the Angelonieae, which we here investigate to better understand the evolutionary time frame of this pollination syndrome.• METHODS: We generated nuclear and plastid data matrices for 56% of the Angelonieae species (plus outgroups) and used Bayesian methods of molecular clock dating, ancestral state reconstruction, and biogeographic inference.• KEY RESULTS: We found that Angelonieae have two major clades, Angelonia (including Monopera) and Basistemon, and Monttea, Melosperma, and Ourisia.• CONCLUSIONS: Angelonieae date back to the Uppermost Eocene, ca. 35 (26-47) Myr ago (Ma) and diversified in dry areas of southern South America; they switched from nectar to oil as a reward four or five times over the past 25 Ma. As predicted in a previous non-clock-dated study, dispersal to Australasia dates to the Miocene/Pliocene.

The corbiculate bees arose from New World oil-collecting bees: implications for the origin of pollen baskets.

The economically most important group of bees is the "corbiculates", or pollen basket bees, some 890 species of honeybees (Apis), bumblebees (Bombus), stingless bees (Meliponini), and orchid bees (Euglossini). Molecular studies have indicated that the corbiculates are closest to the New World genera Centris, with 230 species, and Epicharis, with 35, albeit without resolving the precise relationships. Instead of concave baskets, these bees have hairy hind legs on which they transport pollen mixed with floral oil, collected with setae on the anterior and middle legs. We sampled two-thirds of all Epicharis, a third of all Centris, and representatives of the four lineages of corbiculates for four nuclear gene regions, obtaining a well-supported phylogeny that has the corbiculate bees nested inside the Centris/Epicharis clade. Fossil-calibrated molecular clocks, combined with a biogeographic reconstruction incorporating insights from the fossil record, indicate that the corbiculate clade arose in the New World and diverged from Centris 84 (72-95)mya. The ancestral state preceding corbiculae thus was a hairy hind leg, perhaps adapted for oil transport as in Epicharis and Centris bees. Its replacement by glabrous, concave baskets represents a key innovation, allowing efficient transport of plant resins and large pollen/nectar loads and freeing the corbiculate clade from dependence on oil-offering flowers. The transformation could have involved a novel function of Ubx, the gene known to change hairy into smooth pollen baskets in Apis and Bombus.