Title: Diversity in olfactory receptor repertoires is associated with dietary specialization in a genus of frugivorous bat
Abstract Mammalian olfactory receptor genes (ORs) are a diverse family of genes encoding proteins that directly interact with environmental chemical cues. ORs evolve via gene duplication in a birth-death fashion, neofunctionalizing and pseudogenizing over time. Olfaction is a primary sense used for food detection in plant-visiting bats, but the relationship between dietary specialization and OR repertoire diversity is unclear. Within neotropical Leaf-nosed bats (Phyllostomidae), many lineages are plant specialists, and some have a distinct OR repertoire compared to insectivorous species. Yet, whether specialization on particular plant genera is associated with the evolution of specialized, less diverse OR repertoires has never been tested. Using targeted sequence capture, we sequenced the OR repertoires of three sympatric species of short-tailed fruit bats (Carollia), which vary in their degree of specialization on the fruits of Piper plants. We characterized orthologous vs duplicated receptors among Carollia species, and explored the diversity and redundancy of the receptor gene repertoire. At the species level, the most dedicated Piper specialist, Carollia castanea, had lower OR diversity compared to the two generalists (C. sowelli and C. perspicillata), but we discovered a few unique sets of ORs within C. castanea with high redundancy of similar gene duplicates. These unique receptors potentially enable C. castanea to detect Piper fruit odorants better than its two congeners. Carollia perspicillata, the species with the most generalist diet, had a higher diversity of intact receptors, suggesting the ability to detect a wider range of odorant molecules. Variation among ORs may be a factor in the coexistence of these sympatric species, facilitating the exploitation of different plant resources. Our study sheds light on how gene duplication and changes in OR diversity may play a role in dietary adaptations and underlie ecological interactions between bats and plants. more »« less
Santana, Sharlene E.; Kaliszewska, Zofia A.; Leiser-Miller, Leith B.; Lauterbur, M. Elise; Arbour, Jessica H.; Dávalos, Liliana M.; Riffell, Jeffrey A.
(, 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.
Under an adaptive hypothesis, the reciprocal influence between mutualistic plants and frugivores is expected to result in suites of matching frugivore and plant traits that structure fruit consumption. Recent work has suggested fruit traits can represent adaptations to broad groups of functionally similar frugivores, but the role of frugivore traits and within-species variation in structuring fruit consumption is less understood. To address these knowledge gaps, we assess the presence of reciprocal trait matching for the mutualistic ecological network comprising of Carollia bats that feed on and disperse Piper seeds. We used generalized joint attribute modeling (GJAM), a Bayesian modeling approach that simultaneously accounts for multiple sources of variance across trait types. In support of frugivore adaptation to their dietary composition and suggesting niche partitioning among Carollia bats, we find differential consumption of a suite of Piper species influenced by bat traits such as body size; however, the Piper morphological traits considered had no effect on bat consumption. Slow evolutionary rates, dispersal by other vertebrates, and unexamined fruit traits, such as Piper chemical bouquets, may explain the lack of association between bat Piper consumption and fruit morphological traits. We have identified a potential asymmetric influence of frugivore traits on plant–frugivore interactions, providing a template for future trait analyses of plant–animal networks. As intraspecific trait variation is rarely included in studies on trait matching, this paper contributes to closing that important knowledge gap. # Data from: Frugivore traits predict plant-frugivore interactions using generalized joint attribute modeling [https://doi.org/10.5061/dryad.2v6wwpzwg](https://doi.org/10.5061/dryad.2v6wwpzwg) Bayesian models relating: 1\. head.R: relates *Carollia* traits to bite force (performance) via hierarchical ML models 2\. carollia3_0.R: relates *Carollia* traits to bite force (performance) via hierarchical Bayesian models 3\. gjam generated model of consumption relationship to traits for *Carollia* bats 4\. gjam processed model outputs 5\. piper.R: relates *Piper* traits and GJAM coefficients obtained from 3 and 4 ## Description of the data and file structure All cells marked as NA lacked data and correspond to missing data. ## Code/Software 1\. head.R: relates *Carollia* traits to bite force (performance) via hierarchical ML models. Requires data file bat_l_biteBody.csv and R library lme4. Prints results to .txt file. 2\. carollia3_0.R: relates *Carollia* traits to bite force (performance) via hierarchical Bayesian models. Requires data file bat_l_biteBody.csv, R library R2Jags, and 3 Jags files. The three Jags files are: * carollia_bf_size.txt * carollia_bf_mass.txt * carollia_bf_head.txt carollia3_0.R prints out the results of hierarchical Bayesian regressions in txt and saves an Rdata file. 3\. niche_Carollia.R: generates gjam model of consumption relationship t traits for *Carollia* bats Requires data files: * carollia_niche_xdata.csv: x or explanatory variables, bat traits * carollia_niche_ydata_trim.csv: y or response variables, bat consumption of *Piper* fruit from different species * carollia_type.csv: individual bat assignment to one of 3 species * and R libraries gjam, reshape2 and plyr plus function * bayesReg.R (which codes a function to run a Tobit and Bayesian regression from the NEON example here: [https://rstudio-pubs-static.s3.amazonaws.com/710083_480b1b43b4f0470691e95302483fdc08.html](https://rstudio-pubs-static.s3.amazonaws.com/710083_480b1b43b4f0470691e95302483fdc08.html)). This script generates the bayesian gjam model and saves an Rdata file. 4\. plot_Carollia_v2.r processes gjam model outputs. Requires data files: * models_Carollia.Rdata * and R libraries gjam, reshape2, plyr, ggplot2, MCMCvis and wesanderson This script generates the standardized summary and prints out a file called piper_medians.csv 5\. piper.R relates *Piper* traits and gjam coefficients obtained from steps 3 and 4.. Requires data files: * piper.nex: phylogeny of *Piper* plants * piper_k_traits.csv: correspondence between *Piper* traits and *Piper* species * output.csv: this is processed from piper_medians.csv to separate relate Piper species to bat trait values resulting from gjam * Requires R libraries MCMCglmm and geiger This script prints out the results of phylogenetic Bayesian regressions of gjam outputs as a function of *Piper* traits in txt and saves a Rdata file.
ABSTRACT Under an adaptive hypothesis, the reciprocal influence between mutualistic plants and frugivores is expected to result in suites of matching frugivore and plant traits that structure fruit consumption. Recent work has suggested fruit traits can represent adaptations to broad groups of functionally similar frugivores, but the role of frugivore traits and within‐species variation in structuring fruit consumption is less understood. To address these knowledge gaps, we assess the presence of reciprocal trait matching for the mutualistic ecological network comprising ofCarolliabats that feed on and dispersePiperseeds. We used generalized joint attribute modeling (GJAM), a Bayesian modeling approach that simultaneously accounts for multiple sources of variance across trait types. In support of frugivore adaptation to their dietary composition and suggesting niche partitioning amongCarolliabats, we find differential consumption of a suite ofPiperspecies influenced by bat traits such as body size; however, thePipermorphological traits considered had no effect on bat consumption. Slow evolutionary rates, dispersal by other vertebrates, and unexamined fruit traits, such asPiperchemical bouquets, may explain the lack of association between batPiperconsumption and fruit morphological traits. We have identified a potential asymmetric influence of frugivore traits on plant–frugivore interactions, providing a template for future trait analyses of plant–animal networks. As intraspecific trait variation is rarely included in studies on trait matching, this paper contributes to closing that important knowledge gap.
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
(, 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.
This repository contains scripts, information, and figures related to the statistical analyses conducted for the research paper “Testing the effectiveness of synthetic chemical lures to increase fruit bat-mediated seed dispersal in a tropical forest.” Our research explores the effectiveness of synthetic chemical lures as a novel strategy to attract fruit bats and enhance seed rain in a lowland rainforest in northeastern Costa Rica (La Selva Biological Station). We investigated the impact of chemical lures on increasing bat activity and seed rain. All the analyses were performed in R v. 4.2.1. Scripts 1. Objective 1: Assess the effectiveness of the chemical lure to increase bat activity in open and semi-open areas (script1.R and script2.R) These scripts details the process of analyzing the impact of chemical lures on bat activity. script1.R compares bat communities across different sites and treatments. Non-metric multidimensional scaling (NMDS) was employed for visualization. Homogeneity of variances was checked using the ‘betadisper()’ function, followed by permutational multivariate analysis of variance (PERMANOVA) using the ‘adonis2()’ function with 999 permutations. In script2.R GLMMs were employed using the glmmTMB package. The models included the bat abundance as fixed effect, and site and capture date as random effects. The analysis was performed using various count data distributions from the glmmTMB package Overdispersion and zero inflation were assessed using the ‘check_overdispersion()’ and ‘check_zeroinflation()’ functions from the performance package. Effect sizes were computed based on estimated marginal means using the ‘emmeans()’ function from the emmeans package. We performed an autocorrelation analysis on the residuals of each model fitted. First, we performed a Durbin-Watson (DW) using the function ‘dwtest()’ from the lmtest package to test to assess temporal autocorrelation in these residuals. Then, we generated a visual representation of the autocorrelation function (ACF). Our results indicate that there is no temporal autocorrelation present in our bat data. 1. Objective 2: Assess the effectiveness of the chemical lure to increase seed rain of open and semi-open areas (script3.R) This script outlines the analysis of the impact of chemical lures on seed rain NMDS was used for visualization, and homogeneity of variances was checked with ‘betadisper()’. PERMANOVA was conducted using the ‘adonis2()’ function with 999 permutations to test for statistical significance. Data Files Folder Objective 1: data.csv and data_nodates.csv Contains the data used for analyzing bat activity. The columns in the dataset are as follows: date: The date of bat capture. site: The site where the capture took place. bats: Total number of bats captured. fruit_bats: Total number of captured fruit bats. cperspicillata: Number of captured Carollia perspicillata bats. csowelli: Number of captured Carollia sowelli bats. ccastanea: Number of captured Carollia castanea bats. carollia_spp: Total number of captured bats from the Carollia genus. uroderma_spp: Number of captured bats from the Uroderma genus. sturnira_spp: Number of captured bats from the Sturnira genus. ectophylla_alba: Number of captured Ectophylla alba bats. artibeus_spp: Number of captured bats from the Artibeus genus. desmodus_rotundus: Number of captured Desmodus rotundus bats. nectarivorous_bats: Number of captured nectarivorous bats. insectivorous_bats: Number of captured insectivorous bats. treatment: The treatment applied (“control” or “lures”). hours: Total hours of mist nesting. nets: Total number of nets used for bat capture. Folder Objective 2: seed_data.csv Contains the data used for analyzing seed rain. The columns in the dataset are as follows: week: The week of the seed collection. Seeds were collected every 15 days. site_name: The name of the site where the observation took place at La Selva (“Zompopa”, “Lab”, “STR - Sendero Tres Rios”, “PS - Parcelas de Sucesion”). site_letter: The site’s letter designation (“A”, “B”, “C”, “D”) collection_date: The date of seed collection. treatment: The treatment applied (“baseline”, “control”, “treatment”). Columns for various plant species/plant families, indicating the count of seeds for each species. total: The total count of seeds for all plant species per collection week. comments: Additional comments or notes about the observation. Figures folder The ‘Figures’ folder contains various output files generated from the analyses conducted in the main scripts. These figures represent the results and insights obtained from the data exploration and statistical modeling.
Yohe, Laurel R, Leiser-Miller, Leith B, Kaliszewska, Zofia A, Donat, Paul, Santana, Sharlene E, and Dávalos, Liliana M. Diversity in olfactory receptor repertoires is associated with dietary specialization in a genus of frugivorous bat. Retrieved from https://par.nsf.gov/biblio/10299796. G3 Genes|Genomes|Genetics 11.10 Web. doi:10.1093/g3journal/jkab260.
Yohe, Laurel R, Leiser-Miller, Leith B, Kaliszewska, Zofia A, Donat, Paul, Santana, Sharlene E, & Dávalos, Liliana M. Diversity in olfactory receptor repertoires is associated with dietary specialization in a genus of frugivorous bat. G3 Genes|Genomes|Genetics, 11 (10). Retrieved from https://par.nsf.gov/biblio/10299796. https://doi.org/10.1093/g3journal/jkab260
Yohe, Laurel R, Leiser-Miller, Leith B, Kaliszewska, Zofia A, Donat, Paul, Santana, Sharlene E, and Dávalos, Liliana M.
"Diversity in olfactory receptor repertoires is associated with dietary specialization in a genus of frugivorous bat". G3 Genes|Genomes|Genetics 11 (10). Country unknown/Code not available. https://doi.org/10.1093/g3journal/jkab260.https://par.nsf.gov/biblio/10299796.
@article{osti_10299796,
place = {Country unknown/Code not available},
title = {Diversity in olfactory receptor repertoires is associated with dietary specialization in a genus of frugivorous bat},
url = {https://par.nsf.gov/biblio/10299796},
DOI = {10.1093/g3journal/jkab260},
abstractNote = {Abstract Mammalian olfactory receptor genes (ORs) are a diverse family of genes encoding proteins that directly interact with environmental chemical cues. ORs evolve via gene duplication in a birth-death fashion, neofunctionalizing and pseudogenizing over time. Olfaction is a primary sense used for food detection in plant-visiting bats, but the relationship between dietary specialization and OR repertoire diversity is unclear. Within neotropical Leaf-nosed bats (Phyllostomidae), many lineages are plant specialists, and some have a distinct OR repertoire compared to insectivorous species. Yet, whether specialization on particular plant genera is associated with the evolution of specialized, less diverse OR repertoires has never been tested. Using targeted sequence capture, we sequenced the OR repertoires of three sympatric species of short-tailed fruit bats (Carollia), which vary in their degree of specialization on the fruits of Piper plants. We characterized orthologous vs duplicated receptors among Carollia species, and explored the diversity and redundancy of the receptor gene repertoire. At the species level, the most dedicated Piper specialist, Carollia castanea, had lower OR diversity compared to the two generalists (C. sowelli and C. perspicillata), but we discovered a few unique sets of ORs within C. castanea with high redundancy of similar gene duplicates. These unique receptors potentially enable C. castanea to detect Piper fruit odorants better than its two congeners. Carollia perspicillata, the species with the most generalist diet, had a higher diversity of intact receptors, suggesting the ability to detect a wider range of odorant molecules. Variation among ORs may be a factor in the coexistence of these sympatric species, facilitating the exploitation of different plant resources. Our study sheds light on how gene duplication and changes in OR diversity may play a role in dietary adaptations and underlie ecological interactions between bats and plants.},
journal = {G3 Genes|Genomes|Genetics},
volume = {11},
number = {10},
author = {Yohe, Laurel R and Leiser-Miller, Leith B and Kaliszewska, Zofia A and Donat, Paul and Santana, Sharlene E and Dávalos, Liliana M},
editor = {null}
}
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