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.

Why Did the Bee Eat the Chicken? Symbiont Gain, Loss, and Retention in the Vulture Bee Microbiome.

Diet and gut microbiomes are intricately linked on both short and long timescales. Changes in diet can alter the microbiome, while microbes in turn allow hosts to access novel diets. Bees are wasps that switched to a vegetarian lifestyle, and the vast majority of bees feed on pollen and nectar. Some stingless bee species, however, also collect carrion, and a few have fully reverted to a necrophagous lifestyle, relying on carrion for protein and forgoing flower visitation altogether. These "vulture" bees belong to the corbiculate apid clade, which is known for its ancient association with a small group of core microbiome phylotypes. Here, we investigate the vulture bee microbiome, along with closely related facultatively necrophagous and obligately pollinivorous species, to understand how these diets interact with microbiome structure. Via deep sequencing of the 16S rRNA gene and subsequent community analyses, we find that vulture bees have lost some core microbes, retained others, and entered into novel associations with acidophilic microbes found in the environment and on carrion. The abundance of acidophilic bacteria suggests that an acidic gut is important for vulture bee nutrition and health, as has been found in other carrion-feeding animals. Facultatively necrophagous bees have more variable microbiomes than strictly pollinivorous bees, suggesting that bee diet may interact with microbiomes on both short and long timescales. Further study of vulture bees promises to provide rich insights into the role of the microbiome in extreme diet switches. IMPORTANCE When asked where to find bees, people often picture fields of wildflowers. While true for almost all species, there is a group of specialized bees, also known as the vulture bees, that instead can be found slicing chunks of meat from carcasses in tropical rainforests. In this study, researchers compared the microbiomes of closely related bees that live in the same region but vary in their dietary lifestyles: some exclusively consume pollen and nectar, others exclusively depend on carrion for their protein, and some consume all of the above. Researchers found that vulture bees lost some ancestral "core" microbes, retained others, and entered into novel associations with acidophilic microbes, which have similarly been found in other carrion-feeding animals such as vultures, these bees' namesake. This research expands our understanding of how diet interacts with microbiomes on both short and long timescales in one of the world's biodiversity hot spots.

Landscape Composition and Fungicide Exposure Influence Host-Pathogen Dynamics in a Solitary Bee.

Both ecosystem function and agricultural productivity depend on services provided by bees; these services are at risk from bee declines which have been linked to land use change, pesticide exposure, and pathogens. Although these stressors often co-occur in agroecosystems, a majority of pollinator health studies have focused on these factors in isolation, therefore limiting our ability to make informed policy and management decisions. Here, we investigate the combined impact of altered landscape composition and fungicide exposure on the prevalence of chalkbrood disease, caused by fungi in the genus Ascosphaera Olive and Spiltoir 1955 (Ascosphaeraceae: Onygenales), in the introduced solitary bee, Osmia cornifrons (Radoszkowski 1887) (Megachilidae: Hymenoptera). We used both field studies and laboratory assays to evaluate the potential for interactions between altered landscape composition, fungicide exposure, and Ascosphaera on O. cornifrons mortality. Chalkbrood incidence in larval O. cornifrons decreased with high open natural habitat cover, whereas Ascosphaera prevalence in adults decreased with high urban habitat cover. Conversely, high fungicide concentration and high forest cover increased chalkbrood incidence in larval O. cornifrons and decreased Ascosphaera incidence in adults. Our laboratory assay revealed an additive effect of fungicides and fungal pathogen exposure on the mortality of a common solitary bee. Additionally, we utilized phylogenetic methods and identified four species of Ascosphaera with O. cornifrons, both confirming previous reports and shedding light on new associates. Our findings highlight the impact of fungicides on bee health and underscore the importance of studying interactions among factors associated with bee decline.