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1. Fruit odorants mediate co-specialization in a multispecies plant–animal mutualism

   https://doi.org/10.1098/rspb.2021.0312  

   Santana, Sharlene E.; Kaliszewska, Zofia A.; Leiser-Miller, Leith B.; Lauterbur, M. Elise; Arbour, Jessica H.; Dávalos, Liliana M.; Riffell, Jeffrey A. (August 2021, Proceedings of the Royal Society B: Biological Sciences)

   null (Ed.)

   Despite the widespread notion that animal-mediated seed dispersal led to the evolution of fruit traits that attract mutualistic frugivores, the dispersal syndrome hypothesis remains controversial, particularly for complex traits such as fruit scent. Here, we test this hypothesis in a community of mutualistic, ecologically important neotropical bats ( Carollia spp.) and plants ( Piper spp.) that communicate primarily via chemical signals. We found greater bat consumption is significantly associated with scent chemical diversity and presence of specific compounds, which fit multi-peak selective regime models in Piper . Through behavioural assays, we found Carollia prefer certain compounds, particularly 2-heptanol, which evolved as a unique feature of two Piper species highly consumed by these bats. Thus, we demonstrate that volatile compounds emitted by neotropical Piper fruits evolved in tandem with seed dispersal by scent-oriented Carollia bats. Specifically, fruit scent chemistry in some Piper species fits adaptive evolutionary scenarios consistent with a dispersal syndrome hypothesis. While other abiotic and biotic processes likely shaped the chemical composition of ripe fruit scent in Piper , our results provide some of the first evidence of the effect of bat frugivory on plant chemical diversity. 

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2. Ecological constraints on highly evolvable olfactory receptor genes and morphology in neotropical bats

   https://doi.org/10.1111/evo.14591  

   Yohe, Laurel R.; Fabbri; Lee, Daniela; Davies, Kalina T.J.; Yohe, Thomas P.; Sánchez, Miluska K.R.; Rengifo, Edgardo M.; Hall, Ronald; Mutumi, Gregory; Hedrick, Brandon P.; et al (January 2022, Evolution)

   While evolvability of genes and traits may promote specialization during species diversification, how ecology subsequently restricts such variation remains unclear. Chemosensation requires animals to decipher a complex chemical background to locate fitness-related resources, and thus the underlying genomic architecture and morphology must cope with constant exposure to a changing odorant landscape; detecting adaptation amidst extensive chemosensory diversity is an open challenge. In phyllostomid bats, an ecologically diverse clade that evolved plant-visiting from an insectivorous ancestor, the evolution of novel food detection mechanisms is suggested to be a key innovation, as plant-visiting species rely strongly on olfaction, supplementarily using echolocation. If this is true, exceptional variation in underlying olfactory genes and phenotypes may have preceded dietary diversification. We compared olfactory receptor (OR) genes sequenced from olfactory epithelium transcriptomes and olfactory epithelium surface area of bats with differing diets. Surprisingly, although OR evolution rates were quite variable and generally high, they are largely independent of diet. Olfactory epithelial surface area, however, is relatively larger in plant-visiting bats and there is an inverse relationship between OR evolution rates and surface area. Relatively larger surface areas suggest greater reliance on olfactory detection and stronger constraint on maintaining an already diverse OR repertoire. Instead of the typical case in which specialization and elaboration are coupled with rapid diversification of associated genes, here the relevant genes are already evolving so quickly that increased reliance on smell has led to stabilizing selection, presumably to maintain the ability to consistently discriminate among specific odorants — a potential ecological constraint on sensory evolution. 

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3. Multiple dimensions of dietary diversity in large mammalian herbivores

   https://doi.org/10.1111/1365-2656.13206  

   Kartzinel, Tyler R.; Pringle, Robert M.; Eizaguirre, ed., Christophe (April 2020, Journal of Animal Ecology)

   Abstract Theory predicts that trophic specialization (i.e. low dietary diversity) should make consumer populations sensitive to environmental disturbances. Yet diagnosing specialization is complicated both by the difficulty of precisely quantifying diet composition and by definitional ambiguity: what makes a diet ‘diverse’?We sought to characterize the relationship between taxonomic dietary diversity (TDD) and phylogenetic dietary diversity (PDD) in a species‐rich community of large mammalian herbivores in a semi‐arid East African savanna. We hypothesized that TDD and PDD would be positively correlated within and among species, because taxonomically diverse diets are likely to include plants from many lineages.By using DNA metabarcoding to analyse 1,281 faecal samples collected across multiple seasons, we compiled high‐resolution diet profiles for 25 sympatric large‐herbivore species. For each of these populations, we calculated TDD and PDD with reference to a DNA reference library for local plants.Contrary to our hypothesis, measures of TDD and PDD were either uncorrelated or negatively correlated with each other. Thus, these metrics reflect distinct dimensions of dietary specialization both within and among species. In general, grazers and ruminants exhibited greater TDD, but lower PDD, than did browsers and non‐ruminants. We found significant seasonal variation in TDD and/or PDD for all but four species (Grevy's zebra, buffalo, elephant, Grant's gazelle); however, the relationship between TDD and PDD was consistent across seasons for all but one of the 12 best‐sampled species (plains zebra).Our results show that taxonomic generalists can be phylogenetic specialists, and vice versa. These two dimensions of dietary diversity suggest contrasting implications for efforts to predict how consumers will respond to climate change and other environmental perturbations. For example, populations with low TDD may be sensitive to phylogenetically ‘random’ losses of food species, whereas populations with low PDD may be comparatively more sensitive to environmental changes that disadvantage entire plant lineages—and populations with low dietary diversity in both taxonomic and phylogenetic dimensions may be most vulnerable of all. 

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4. Molecular adaptation and convergent evolution of frugivory in Old World and neotropical fruit bats

   https://doi.org/10.1111/mec.15542  

   Wang, Kai; Tian, Shilin; Galindo‐González, Jorge; Dávalos, Liliana_M; Zhang, Yuzhi; Zhao, Huabin (July 2020, Molecular Ecology)

   Abstract Although cases of independent adaptation to the same dietary niche have been documented in mammalian ecology, the molecular correlates of such shifts are seldom known. Here, we used genomewide analyses of molecular evolution to examine two lineages of bats that, from an insectivorous ancestor, have both independently evolved obligate frugivory: the Old World family Pteropodidae and the neotropical subfamily Stenodermatinae. New genome assemblies from two neotropical fruit bats (Artibeus jamaicensisandSturnira hondurensis) provide a framework for comparisons with Old World fruit bats. Comparative genomics of 10 bat species encompassing dietary diversity across the phylogeny revealed convergent molecular signatures of frugivory in both multigene family evolution and single‐copy genes. Evidence for convergent molecular adaptations associated with frugivorous diets includes the composition of three subfamilies of olfactory receptor genes, losses of three bitter taste receptor genes, losses of two digestive enzyme genes and convergent amino acid substitutions in several metabolic genes. By identifying suites of adaptations associated with the convergent evolution of frugivory, our analyses both reveal the extent of molecular mechanisms under selection in dietary shifts and will facilitate future studies of molecular ecology in mammals. 

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5. Functional and evolutionary insights into chemosensation and specialized herbivory from the genome of the red milkweed beetle, Tetraopes tetrophthalmus (Cerambycidae: Lamiinae)

   https://doi.org/10.1093/jhered/esae049  

   Adams, Richard; Sylvester, Terrence; Mitchell, Robert_F; Price, Mathew_A; Shen, Rongrong; McKenna, Duane_D; Garrick, ed., Ryan (August 2024, Journal of Heredity)

   Abstract Tetraopes are aposematic longhorn beetles (Cerambycidae) that feed primarily on toxic plants in the genus Asclepias (milkweeds). Studies of Tetraopes and their host plants have revealed compelling evidence for insect–plant coevolution and cospeciation. We sequenced, assembled, and annotated the genome of the common red milkweed beetle, Tetraopes tetrophthalmus, and explored gene content and evolution, focusing on annotated genes putatively involved in chemosensation, allelochemical detoxification, and phytophagy. Comparisons were made to the Asian longhorned beetle (Anoplophora glabripennis) genome. The genome assembly comprised 779 Mb distributed across 1,057 contigs, with an N50 of 2.21 Mb and 13,089 putative genes, including 97.3% of expected single-copy orthologs. Manual curation identified 122 putative odorant receptors (OR) and 162 gustatory receptors (GR), the former number similar to A. glabripennis but the latter only 69% of the A. glabripennis suite. We also documented a greater percentage of pseudogenic GRs and ORs compared to A. glabripennis, suggesting an ongoing reduction in chemosensory function, perhaps related to host specialization. We found lower diversity within certain well-studied gene families predicted to encode putative plant cell wall degrading enzymes in the T. tetrophthalmus genome, perhaps also due to host specialization. Exploring genes relevant to stress and allelochemical detoxification revealed evidence of an abundance of ABC-family genes in the T. tetrophthalmus genome, which may be related to sequestering toxic cardiac glycosides. Our studies further illuminate the genomic basis and evolution of chemosensation in longhorn beetles and provide a new vantage point from which to explore the ecology and evolution of specialized plant-feeding in Tetraopes and other phytophagous beetles. 

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