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Keefover-Ring, K.

Publications and source records attributed to Keefover-Ring, K..

7 recordsLinked to original sources

Self-medicating behavior in bumble bees has cascading consequences for pollination and plant reproduction

The sublethal effects of parasites can profoundly influence host traits and propagate to other trophic levels via indirect effects. To date, research on such trait-mediated indirect effects of parasites has focused on non-adaptive changes to host behavior, but adaptive sickness behaviors, such as self-medication, could also indirectly affect community composition and even the evolution of medicinal traits in lower trophic levels. Here, we used interactions among the parasite Crithidia bombi, the bumble bee host Bombus impatiens, and Monarda fistulosa, a bee-pollinated plant with multiple chemotypes (genetically determined chemical phenotypes), to experimentally test whether parasite infection influences pollinator foraging, pollination success, and female plant reproduction differentially for medicinal vs. non-medicinal chemotypes. Compounds from three Monarda chemotypes reduced Crithidia infection intensity in bees (thymol, carvacrol, and 1,8-cineole; hereafter medicinal chemotypes), while two others did not ((R)-(-)-linalool and geraniol; hereafter non-medicinal chemotypes), compared to control sucrose solutions. We found evidence for self-medication in tent foraging choice assays: infected bees preferred medicinal chemotypes while uninfected bees foraged indiscriminately, leading to differences in pollen receipt. Crithidia infection had weak but compounding chemotype-specific effects on seed production, germination rate, and offspring chemotype, such that pollination by infected bees resulted in a 57% increase in the proportion of medicinal plants in the F1 generation compared to pollination by uninfected bees. Self-medicating behavior can have differential effects on the reproduction of medicinal vs. non-medicinal plants, suggesting that pollinator parasites may act as agents of selection on the phytochemistry of floral rewards. SIGNIFICANCE STATEMENTParasite infection can alter host behavior in multiple ways, including by inducing self-medication. Self-medication has been documented in diverse animal taxa, yet we know very little about the broader ecological or evolutionary consequences of this response to infection. Here, we demonstrate that bumble bees infected with a common parasite show a preference for plant genotypes whose nectar contains antiparasitic compounds, and that this results in differential pollination and reproductive success for medicinal vs. non-medicinal individuals of a chemically polymorphic plant species. Our findings highlight self-medication as a previously understudied mechanism by which parasite infection could initiate cascading effects across trophic levels, and suggest that parasites may indirectly influence the evolution of plant traits via pollinator self-medication behaviors.

ecology↗

Phylogenomics reveals patterns of ancient hybridization and differential diversification contributing to phylogenetic conflict in Populus L. and Salix L.

Despite the economic, ecological, and scientific importance of the genera Populus L. (poplars, cottonwoods, and aspens) and Salix L. Salicaceae (willows), we know little about the sources of differences in species diversity between the genera and of the phylogenetic conflict that often confounds estimating phylogenetic trees. Salix subgenera and sections, in particular, have been difficult to classify, with one recent attempt termed a spectacular failure due to a speculated radiation of the subgenera Vetrix and Chamaetia. Here we use targeted sequence capture to understand the evolutionary history of this portion of the Salicaceae plant family. Our phylogenetic hypothesis was based on 787 gene regions and identified extensive phylogenetic conflict among genes. Our analysis supported some previously described subgeneric relationships and confirmed polyphyly of others. Using an fbranch analysis we identified several cases of hybridization in deep branches of the phylogeny, which likely contributed to discordance among gene trees. In addition, we identified a rapid increase in diversification rate near the origination of the Vetrix-Chamaetia clade in Salix. This region of the tree coincided with several nodes that lacked strong statistical support, indicating a possible increase in incomplete lineage sorting due to rapid diversification. The extraordinary level of both recent and ancient hybridization in both Populus and Salix have played important roles in the diversification and diversity in these two genera. Supplementary data files will be provided by request to matt.olson@ttu.edu

evolutionary biology↗

A general model to explain repeated turnovers of sex determination in the Salicaceae

Dioecy, the presence of separate sexes on distinct individuals, has evolved repeatedly in multiple plant lineages. However, the specific mechanisms through which sex systems evolve and their commonalities among plant species remain poorly understood. With both XY and ZW sex systems, the family Salicaceae provides a system to uncover the evolutionary forces driving sex chromosome turnovers. In this study, we performed a genome-wide association study to characterize sex determination in two Populus species, P. euphratica and P. alba. Our results reveal an XY system of sex determination on chromosome 14 of P. euphratica, and a ZW system on chromosome 19 of P. alba. We further assembled the corresponding sex determination regions, and found that their sex chromosome turnovers may be driven by the repeated translocations of a Helitron-like transposon. During the translocation, this factor may have captured partial or intact sequences that are orthologous to a type-A cytokinin response regulator gene. Based on results from this and other recently published studies, we hypothesize that this gene may act as a master regulator of sex determination for the entire family. We propose a general model to explain how the XY and ZW sex systems in this family can be determined by the same RR gene. Our study provides new insights into the diversification of incipient sex chromosome in flowering plants by showing how transposition and rearrangement of a single gene can control sex in both XY and ZW systems.

genomics↗

Sex determination through X-Y heterogamety in Salix nigra

The development of non-recombining sex chromosomes has radical effects on the evolution of discrete sexes and sexual dimorphism. Although dioecy is rare in plants, sex chromosomes have evolved repeatedly throughout the diversification of angiosperms, and many of these sex chromosomes are relatively young compared to those found in vertebrates. In this study, we designed and used a sequence capture array to identify a novel sex-linked region (SLR) in Salix nigra, a basal species in the willow clade, and demonstrated that this species has XY heterogamety. We did not detect any genetic overlap with the previously characterized ZW SLRs in willows, which map to a different chromosome. The S. nigra SLR is characterized by strong recombination suppression across a 2 MB region and an excess of low frequency alleles, resulting in a low Tajimas D compared to the remainder of the genome. We speculate that either a recent bottleneck in population size or factors related to positive or background selection generated this differential pattern of Tajimas D on the X and autosomes. This discovery provides insights into factors that may influence the evolution of sex chromosomes in plants and contributes to a large number of recent observations that underscore their dynamic nature.

genomics↗

Characterization of Salix nigra floral insect community and activity of three native Andrena bees

Salix nigra (black willow) is a widespread tree that hosts many species of polylectic hymenopterans and oligolectic bees of the genus Andrena. The early flowering time of S. nigra makes it an important nutritive resource for arthropods emerging from hibernation. However, since S. nigra is dioecious, not all insect visits will lead to successful pollination. Using both visual observation and pan-trapping we characterized the community of arthropods that visited S. nigra flowers and assessed the differences among male and female trees as well as the chemical and visual drivers that influenced community composition across three years. We found that male trees consistently supported higher diversity of insects than female trees and only three insect species, all Andrena spp., consistently visited both sexes. Additionally, A. nigrae, which was the only insect that occurred more on female than male flowers, correlated strongly to volatile cues. This suggests that cross-pollinators cue into specific aspects of floral scent, but diversity of floral visitors is driven strongly by visual cues. Through time the floral activity of two Andrena species remained stable, but A. nigrae visited less in 2017 when flowers bloomed earlier than other years. When native bee emergence does not synchronize with bloom, activity appears to be greatly diminished which could threaten species that only subsist on a single host. Despite the community diversity of S. nigra flowers, its productivity depends on a small fraction of species that are not threatened by competition, but rather rapidly changing conditions that lead to host-insect asynchrony.

ecology↗

Bacteria contribute to plant secondary compound degradation in a generalist herbivore system

Herbivores must overcome a variety of plant defenses, including coping with plant secondary compounds (PSCs). To help detoxify these defensive chemicals, several insect herbivores are known to harbor gut microbiota with the metabolic capacity to degrade PSCs. Leaf-cutter ants are generalist herbivores, obtaining sustenance from specialized fungus gardens that act as external digestive systems, degrading the diverse collection of plants foraged by the ants. There is in vitro evidence that certain PSCs harm Leucoagaricus gongylophorus, the fungal cultivar of leaf-cutter ants, suggesting a role for the Proteobacteria-dominant bacterial community present within fungus gardens. Here, we investigate the ability of symbiotic bacteria present within fungus gardens of leaf-cutter ants to degrade PSCs. We cultured fungus garden bacteria, sequenced the genomes of 42 isolates, and identified genes involved in PSC degradation, including genes encoding cytochrome p450s and genes in geraniol, cumate, cinnamate, and -pinene/limonene degradation pathways. Using metatranscriptomic analysis, we show that some of these degradation genes are expressed in situ. Most of the bacterial isolates grew unhindered in the presence of PSCs and, using GC-MS, we determined that isolates from the genera Bacillus, Burkholderia, Enterobacter, Klebsiella, and Pseudomonas degrade -pinene, {beta}-caryophyllene, or linalool. Using a headspace sampler, we show that sub-colonies of fungus gardens reduced -pinene and linalool over a 36-hour period, while L. gongylophorus strains alone only reduced linalool. Overall, our results reveal that the bacterial community in fungus gardens play a pivotal role in alleviating the effect of PSCs on the leaf-cutter ant system. ImportanceLeaf-cutter ants are dominant neotropical herbivores capable of deriving energy from a wide range of plant substrates. The success of leaf-cutter ants is largely due to their external gut composed of key microbial symbionts, specifically, the fungal mutualist L. gongylophorus and a consistent bacterial community. Both symbionts are known to have critical roles in extracting energy from plant material, yet comparatively little is known about their role in the detoxification of plant secondary compounds. Here, we assess if the bacterial community associated with leaf-cutter ant fungus gardens can degrade harmful plant chemicals. We identify plant secondary compound detoxification in leaf-cutter ant gardens as a process that depends on the degradative potential of both the bacterial community and L. gongylophorus. Our findings suggest the fungus garden and its associated microbial community influences the generalist foraging abilities of the ants, underscoring the importance of microbial symbionts in plant substrate suitability for herbivores.

ecology↗

Metagenomics reveals diet-specific specialization in fungus gardens of grass- and dicot-cutter ants

Leaf-cutter ants in the genus Atta are dominant herbivores in the Neotropics. While most species of Atta cut dicots to incorporate into their fungus gardens, some species specialize on grasses. Here we examine the bacterial community associated with the fungus gardens of grass- and dicot-cutter ants to examine how changes in substrate input affect the bacterial community. We sequenced the metagenomes of 12 Atta fungus gardens, across four species of ants, with a total of 5.316 Gbp of sequence data. We show significant differences in the fungus garden bacterial community composition between dicot- and grass-cutter ants, with grass-cutter ants having lower diversity. Reflecting this difference in community composition, the bacterial functional profiles between the fungus gardens are significantly different. Specifically, grass-cutter ant fungus garden metagenomes are particularly enriched for genes responsible for amino acid, siderophore, and terpenoid biosynthesis while dicot-cutter ant fungus gardens metagenomes are enriched in genes involved in membrane transport. These differences in bacterial community composition and functional capacity show that different substrate inputs matter for fungus garden bacteria, and sheds light on the potential role of bacteria in mediating the ants transition to the use of a novel substrate.

microbiology↗