scholarly journals Dietary Breadth is Positively Correlated with Venom Complexity in Cone Snails

2015 ◽  
Author(s):  
Mark A Phuong ◽  
Gusti N Mahardika ◽  
Michael E Alfaro
Keyword(s):  
Evolutionary Dynamics ◽  
Gene Diversity ◽  
Expression Patterns ◽  
Snail Species ◽  
Ecological Data ◽  
Dietary Breadth ◽  
Venom Composition ◽  
Taxonomic Class ◽  
Venom Evolution ◽  
Cone Snails

Although diet is believed to be a major factor underlying the evolution of venom, few comparative studies examine both venom composition and diet across a radiation of venomous species. Cone snails within the family, Conidae, comprise more than 700 species of carnivorous marine snails that capture their prey by using a cocktail of venomous neurotoxins (conotoxins or conopeptides). Venom composition across species has been previously hypothesized to be shaped by (a) prey taxonomic class (i.e., worms, molluscs, or fish) and (b) dietary breadth. We tested these hypotheses under a comparative phylogenetic framework using ecological data in conjunction with venom duct transcriptomes sequenced from 12 phylogenetically disparate cone snail species, including 10 vermivores (worm-eating), one molluscivore, and one generalist. We discovered 2223 unique conotoxin precursor peptides that encoded 1864 unique mature toxins across all species, >90% of which are new to this study. In addition, we identified two novel gene superfamilies and 16 novel cysteine frameworks. Each species exhibited unique venom profiles, with venom composition and expression patterns among species dominated by a restricted set of gene superfamilies and mature toxins. In contrast with the dominant paradigm for interpreting Conidae venom evolution, prey taxonomic class did not predict venom composition patterns among species. Our results suggests that cone snails have either evolved species-specific expression patterns likely as a consequence of the rapid evolution of conotoxin genes, or that traditional means of categorizing prey type (i.e., worms, mollusc, or fish) and conotoxins (i.e., by gene superfamily) do not accurately encapsulate evolutionary dynamics between diet and venom composition. We also found a significant positive relationship between dietary breadth and measures of conotoxin complexity. These results indicate that species with more generalized diets tend to have more complex venoms and utilize a greater number of venom genes for prey capture. Whether this increased gene diversity confers an increased capacity for evolutionary change remains to be tested. Overall, our results corroborate the key role of diet in influencing patterns of venom evolution in cone snails and other venomous radiations.

scholarly journals Targeted sequencing of venom genes from cone snail genomes reveals coupling between dietary breadth and conotoxin diversity

2017 ◽  
Author(s):  
Mark A Phuong ◽  
Gusti N Mahardika
Keyword(s):  
Gene Diversity ◽  
Gene Families ◽  
Targeted Sequencing ◽  
Toxin Gene ◽  
Cone Snail ◽  
Genetic Changes ◽  
Marine Gastropods ◽  
Dietary Breadth ◽  
Cone Snails ◽  
The Impact

AbstractAlthough venomous taxa provide an attractive system to study the genetic basis of adaptation and speciation, the slow pace of toxin gene discovery through traditional laboratory techniques (e.g., cDNA cloning) have limited their utility in the study of ecology and evolution. Here, we applied targeted sequencing techniques to selectively recover venom gene superfamilies and non-toxin loci from the genomes of 32 species of cone snails (family, Conidae), a hyper diverse group of carnivorous marine gastropods that capture their prey using a cocktail of neurotoxic proteins (conotoxins). We were able to successfully recover conotoxin gene superfamilies across all species sequenced in this study with high confidence (> 100X coverage). We found that conotoxin gene superfamilies are composed of 1-6 exons and adjacent noncoding regions are not enriched for simple repetitive elements. Additionally, we provided further evidence for several genetic factors shaping venom composition in cone snails, including positive selection, extensive gene turnover, expression regulation, and potentially, presence-absence variation. Using comparative phylogenetic methods, we found that while diet specificity did not predict patterns of conotoxin gene superfamily size evolution, dietary breadth was positively correlated with total conotoxin gene diversity. These results continue to emphasize the importance of dietary breadth in shaping venom evolution, an underappreciated ecological correlate in venom biology. Finally, the targeted sequencing technique demonstrated here has the potential to radically increase the pace at which venom gene families are sequenced and studied, reshaping our ability to understand the impact of genetic changes on ecologically relevant phenotypes and subsequent diversification.

scholarly journals Effects of Predator-Prey Interactions on Predator Traits: Differentiation of Diets and Venoms of a Marine Snail

Toxins ◽  
2019 ◽  
Vol 11 (5) ◽  
pp. 299 ◽  
Author(s):  
David A. Weese ◽  
Thomas F. Duda
Keyword(s):  
Resource Utilization ◽  
Species Interactions ◽  
Expression Patterns ◽  
Easter Island ◽  
Island Population ◽  
Predator Prey ◽  
Dietary Breadth ◽  
Venom Composition ◽  
Marine Snails ◽  
Prey Utilization

Species interactions are fundamental ecological forces that can have significant impacts on the evolutionary trajectories of species. Nonetheless, the contribution of predator-prey interactions to genetic and phenotypic divergence remains largely unknown. Predatory marine snails of the family Conidae exhibit specializations for different prey items and intraspecific variation in prey utilization patterns at geographic scales. Because cone snails utilize venom to capture prey and venom peptides are direct gene products, it is feasible to examine the evolution of genes associated with changes in resource utilization. Here, we compared feeding ecologies and venom duct transcriptomes of individuals from three populations of Conus miliaris, a species that exhibits geographic variation in prey utilization and dietary breadth, in order to determine the extent to which dietary differences are correlated with differences in venom composition, and if expanded niche breadth is associated with increased variation in venom composition. While populations showed little to no overlap in resource utilization, taxonomic richness of prey was greatest at Easter Island. Changes in dietary breadth were associated with differences in expression patterns and increased genetic differentiation of toxin-related genes. The Easter Island population also exhibited greater diversity of toxin-related transcripts, but did not show increased variance in expression of these transcripts. These results imply that differences in dietary breadth contribute more to the structural and regulatory differentiation of venoms than differences in diet.

scholarly journals Diet Diversity in Carnivorous Terebrid Snails Is Tied to the Presence and Absence of a Venom Gland

Toxins ◽  
2021 ◽  
Vol 13 (2) ◽  
pp. 108
Author(s):  
Juliette Gorson ◽  
Giulia Fassio ◽  
Emily S. Lau ◽  
Mandë Holford
Keyword(s):  
Venom Gland ◽  
Molecular Study ◽  
Strongly Correlated ◽  
Animal Evolution ◽  
Diet Diversity ◽  
Dietary Breadth ◽  
Venom Composition ◽  
Marine Snails ◽  
Predatory Strategy ◽  
Definition Of

Predator-prey interactions are thought to play a driving role in animal evolution, especially for groups that have developed venom as their predatory strategy. However, how the diet of venomous animals influences the composition of venom arsenals remains uncertain. Two prevailing hypotheses to explain the relationship between diet and venom composition focus on prey preference and the types of compounds in venom, and a positive correlation between dietary breadth and the number of compounds in venom. Here, we examined venom complexity, phylogenetic relationship, collection depth, and biogeography of the Terebridae (auger snails) to determine if repeated innovations in terebrid foregut anatomy and venom composition correspond to diet variation. We performed the first molecular study of the diet of terebrid marine snails by metabarcoding the gut content of 71 terebrid specimens from 17 species. Our results suggest that the presence or absence of a venom gland is strongly correlated with dietary breadth. Specifically, terebrid species without a venom gland displayed greater diversity in their diet. Additionally, we propose a revision of the definition of venom complexity in conoidean snails to more accurately capture the breadth of ecological influences. These findings suggest that prey diet is an important factor in terebrid venom evolution and diversification and further investigations of other understudied organisms, like terebrids, are needed to develop robust hypotheses in this area.

scholarly journals The wild strawberry kinome: identification, classification and transcript profiling of protein kinases during development and in response to gray mold infection

BMC Genomics ◽  
2020 ◽  
Vol 21 (1) ◽  
Author(s):  
Hui Liu ◽  
Wei Qu ◽  
Kaikai Zhu ◽  
Zong-Ming Cheng
Keyword(s):  
Protein Kinases ◽  
Evolutionary Dynamics ◽  
Expression Patterns ◽  
Gene Families ◽  
Gray Mold ◽  
Fragaria Vesca ◽  
Woodland Strawberry ◽  
Go Enrichment ◽  
Potential Link ◽  
Wild Strawberry

Abstract Background Protein kinases (PKs) play an important role in signaling cascades and are one of the largest and most conserved protein super families in plants. Despite their importance, the woodland strawberry (Fragaria vesca) kinome and expression patterns of PK genes remain to be characterized. Results Here, we report on the identification and classification of 954 Fragaria vesca PK genes, which were classified into nine groups and 124 gene families. These genes were distributed unevenly among the seven chromosomes, and the number of introns per gene varied from 0 to 47. Almost half of the putative PKs were predicted to localize to the nucleus and 24.6% were predicted to localize to the cell membrane. The expansion of the woodland strawberry PK gene family occurred via different duplication mechanisms and tandem duplicates occurred relatively late as compared to other duplication types. Moreover, we found that tandem and transposed duplicated PK gene pairs had undergone stronger diversifying selection and evolved relatively faster than WGD genes. The GO enrichment and transcriptome analysis implicates the involvement of strawberry PK genes in multiple biological processes and molecular functions in differential tissues, especially in pollens. Finally, 109 PKs, mostly the receptor-like kinases (RLKs), were found transcriptionally responsive to Botrytis cinerea infection. Conclusions The findings of this research expand the understanding of the evolutionary dynamics of PK genes in plant species and provide a potential link between cell signaling pathways and pathogen attack.

scholarly journals Lack of signal for the impact of venom gene diversity on speciation rates in cone snails

2018 ◽  
Author(s):  
Mark A Phuong ◽  
Michael E Alfaro ◽  
Gusti N Mahardika ◽  
Ristiyanti M Marwoto ◽  
Romanus Edy Prabowo ◽  
...  
Keyword(s):  
Gene Diversity ◽  
Rapid Evolution ◽  
Limiting Factor ◽  
Exon Capture ◽  
Speciation Rates ◽  
Intrinsic Capacity ◽  
Cone Snails ◽  
Species Specific ◽  
Capture Techniques ◽  
The Impact

AbstractUnderstanding why some groups of organisms are more diverse than others is a central goal in macroevolution. Evolvability, or lineages’ intrinsic capacity for evolutionary change, is thought to influence disparities in species diversity across taxa. Over macroevolutionary time scales, clades that exhibit high evolvability are expected to have higher speciation rates. Cone snails (family: Conidae, >900 spp.) provide a unique opportunity to test this prediction because their venom genes can be used to characterize differences in evolvability between clades. Cone snails are carnivorous, use prey-specific venom (conotoxins) to capture prey, and the genes that encode venom are known and diversify through gene duplication. Theory predicts that higher gene diversity confers a greater potential to generate novel phenotypes for specialization and adaptation. Therefore, if conotoxin gene diversity gives rise to varying levels of evolvability, conotoxin gene diversity should be coupled with macroevolutionary speciation rates. We applied exon capture techniques to recover phylogenetic markers and conotoxin loci across 314 species, the largest venom discovery effort in a single study. We paired a reconstructed timetree using 12 fossil calibrations with species-specific estimates of conotoxin gene diversity and used trait-dependent diversification methods to test the impact of evolvability on diversification patterns. Surprisingly, did not detect any signal for the relationship between conotoxin gene diversity and speciation rates, suggesting that venom evolution may not be the rate-limiting factor controlling diversification dynamics in Conidae. Comparative analyses showed some signal for the impact of diet and larval dispersal strategy on diversification patterns, though whether or not we detected a signal depended on the dataset and the method. If our results remain true with increased sampling in future studies, they suggest that the rapid evolution of Conidae venom may cause other factors to become more critical to diversification, such as ecological opportunity or traits that promote isolation among lineages.

scholarly journals Vexitoxins: a novel class of conotoxin-like venom peptides from predatory gastropods of the genus Vexillum

2022 ◽  
Author(s):  
Ksenia G Kuznetsova ◽  
Sofia S Zvonareva ◽  
Rustam Ziganshin ◽  
Elena S Mekhova ◽  
Polina Yu Dgebuadze ◽  
...  
Keyword(s):  
Sequence Similarity ◽  
Venom Gland ◽  
Data Sets ◽  
Rna Seq ◽  
Proteomic Profiling ◽  
Post Translational Modifications ◽  
Origin And Evolution ◽  
The Family ◽  
Venom Evolution ◽  
Cone Snails

Venoms of predatory marine cone snails (the family Conidae, order Neogastropoda) are intensely studied because of the broad range of biomedical applications of the neuropeptides that they contain, conotoxins. Meanwhile anatomy in some other neogastropod lineages strongly suggests that they have evolved similar venoms independently of cone snails, nevertheless their venom composition remains unstudied. Here we focus on the most diversified of these lineages, the genus Vexillum (the family Costellariidae). We have generated comprehensive multi-specimen, multi-tissue RNA-Seq data sets for three Vexillum species, and supported our findings in two species by proteomic profiling. We show that venoms of Vexillum are dominated by highly diversified short cysteine-rich peptides that in many aspects are very similar to conotoxins. Vexitoxins possess the same precursor organization, display overlapping cysteine frameworks and share several common post-translational modifications with conotoxins. Some vexitoxins show detectable sequence similarity to conotoxins, and are predicted to adopt similar domain conformations, including a pharmacologically relevant inhibitory cysteine-know motif (ICK). The tubular gL of Vexillum is a notably more recent evolutionary novelty than the conoidean venom gland. Thus, we hypothesize lower divergence between the toxin genes, and their somatic counterparts compared to that in conotoxins, and we find support for this hypothesis in the molecular evolution of the vexitoxin cluster V027. We use this example to discuss how future studies on vexitoxins can inform origin and evolution of conotoxins, and how they may help addressing standing questions in venom evolution.

scholarly journals Genome analyses of four Wolbachia strains and associated mitochondria of Rhagoletis cerasi expose cumulative modularity of cytoplasmic incompatibility factors and cytoplasmic hitchhiking across host populations

BMC Genomics ◽  
2021 ◽  
Vol 22 (1) ◽  
Author(s):  
Jennifer L. Morrow ◽  
Markus Riegler
Keyword(s):  
Evolutionary Dynamics ◽  
Cytoplasmic Incompatibility ◽  
Gene Diversity ◽  
Management Strategies ◽  
Fruit Fly ◽  
Type I ◽  
Nucleotide Polymorphisms ◽  
Type Iv ◽  
Type V ◽  
Rhagoletis Cerasi

Abstract Background The endosymbiont Wolbachia can manipulate arthropod reproduction and invade host populations by inducing cytoplasmic incompatibility (CI). Some host species are coinfected with multiple Wolbachia strains which may have sequentially invaded host populations by expressing different types of modular CI factor (cif) genes. The tephritid fruit fly Rhagoletis cerasi is a model for CI and Wolbachia population dynamics. It is associated with at least four Wolbachia strains in various combinations, with demonstrated (wCer2, wCer4), predicted (wCer1) or unknown (wCer5) CI phenotypes. Results We sequenced and assembled the draft genomes of the Wolbachia strains wCer1, wCer4 and wCer5, and compared these with the previously sequenced genome of wCer2 which currently invades R. cerasi populations. We found complete cif gene pairs in all strains: four pairs in wCer2 (three Type I; one Type V), two pairs in wCer1 (both Type I) and wCer4 (one Type I; one Type V), and one pair in wCer5 (Type IV). Wolbachia genome variant analyses across geographically and genetically distant host populations revealed the largest diversity of single nucleotide polymorphisms (SNPs) in wCer5, followed by wCer1 and then wCer2, indicative of their different lengths of host associations. Furthermore, mitogenome analyses of the Wolbachia genome-sequenced individuals in combination with SNP data from six European countries revealed polymorphic mitogenome sites that displayed reduced diversity in individuals infected with wCer2 compared to those without. Conclusions Coinfections with Wolbachia are common in arthropods and affect options for Wolbachia-based management strategies of pest and vector species already infected by Wolbachia. Our analyses of Wolbachia genomes of a host naturally coinfected by several strains unravelled signatures of the evolutionary dynamics in both Wolbachia and host mitochondrial genomes as a consequence of repeated invasions. Invasion of already infected populations by new Wolbachia strains requires new sets of functionally different cif genes and thereby may select for a cumulative modularity of cif gene diversity in invading strains. Furthermore, we demonstrated at the mitogenomic scale that repeated CI-driven Wolbachia invasions of hosts result in reduced mitochondrial diversity and hitchhiking effects. Already resident Wolbachia strains may experience similar cytoplasmic hitchhiking effects caused by the invading Wolbachia strain.

Distribution of the T2-MITE Family Transposons in the Xenopus (Silurana) tropicalis Genome

2015 ◽  
Vol 145 (3-4) ◽  
pp. 230-242 ◽  
Author(s):  
Akira Hikosaka ◽  
Yoshinobu Uno ◽  
Yoichi Matsuda
Keyword(s):  
Evolutionary Dynamics ◽  
Expression Patterns ◽  
Mutual Relationship ◽  
Chromosomal Distribution ◽  
Transposition Activity ◽  
Tropicalis Genome ◽  
Unique Distribution ◽  
Distribution Uniformity ◽  
Silurana Tropicalis ◽  
Mite Family

The T2 family of miniature inverted-repeat transposable elements (T2-MITE) is a prevalent MITE family found in both Xenopus(Silurana) tropicalis and X. laevis. Some subfamilies, particularly T2-A1 and T2-C, may have originated prior to the diversification of the 2 Xenopus lineages and currently include active members in X. tropicalis, whereas another subfamily, T2-E, may have lost its transposition activity even earlier. The distribution of each T2-MITE subfamily in X. tropicalis was investigated and compared to evaluate the evolutionary dynamics of the T2-MITE subfamilies. The subfamilies showed differences in chromosomal distribution, uniformity of insertion density on scaffolds, ratios of upstream to downstream insertions with respect to genes, and their distance from genes. Among these, the T2-C subfamily was interesting because it was frequently inserted upstream and close to genes and because genes with close insertions of this subfamily showed high correlations in spatial expression patterns. This unique distribution and long-lived transposition activity may reflect a mutual relationship evolved between this subfamily and the host.

scholarly journals “Beyond Primary Sequence”—Proteomic Data Reveal Complex Toxins in Cnidarian Venoms

2019 ◽  
Vol 59 (4) ◽  
pp. 777-785 ◽  
Author(s):  
Adrian Jaimes-Becerra ◽  
Ranko Gacesa ◽  
Liam B Doonan ◽  
Ashlie Hartigan ◽  
Antonio C Marques ◽  
...  
Keyword(s):  
Adaptive Significance ◽  
Proteomic Data ◽  
Body Regions ◽  
Venomous Animals ◽  
Venom Composition ◽  
Toxin Protein ◽  
Clustering Approach ◽  
Venom Evolution ◽  
Present Understanding ◽  
Dual Functions

Abstract Venomous animals can deploy toxins for both predation and defense. These dual functions of toxins might be expected to promote the evolution of new venoms and alteration of their composition. Cnidarians are the most ancient venomous animals but our present understanding of their venom diversity is compromised by poor taxon sampling. New proteomic data were therefore generated to characterize toxins in venoms of a staurozoan, a hydrozoan, and an anthozoan. We then used a novel clustering approach to compare venom diversity in cnidarians to other venomous animals. Comparison of the presence or absence of 32 toxin protein families indicated venom composition did not vary widely among the 11 cnidarian species studied. Unsupervised clustering of toxin peptide sequences suggested that toxin composition of cnidarian venoms is just as complex as that in many venomous bilaterians, including marine snakes. The adaptive significance of maintaining a complex and relatively invariant venom remains unclear. Future study of cnidarian venom diversity, venom variation with nematocyst types and in different body regions are required to better understand venom evolution.

scholarly journals Lack of Signal for the Impact of Conotoxin Gene Diversity on Speciation Rates in Cone Snails

2019 ◽  
Vol 68 (5) ◽  
pp. 781-796 ◽  
Author(s):  
Mark A Phuong ◽  
Michael E Alfaro ◽  
Gusti N Mahardika ◽  
Ristiyanti M Marwoto ◽  
Romanus Edy Prabowo ◽  
...  
Keyword(s):  
Gene Diversity ◽  
Rapid Evolution ◽  
Limiting Factor ◽  
Exon Capture ◽  
Speciation Rates ◽  
Intrinsic Capacity ◽  
Cone Snails ◽  
Species Specific ◽  
Capture Techniques ◽  
The Impact

Abstract Understanding why some groups of organisms are more diverse than others is a central goal in macroevolution. Evolvability, or the intrinsic capacity of lineages for evolutionary change, is thought to influence disparities in species diversity across taxa. Over macroevolutionary time scales, clades that exhibit high evolvability are expected to have higher speciation rates. Cone snails (family: Conidae, $>$900 spp.) provide a unique opportunity to test this prediction because their toxin genes can be used to characterize differences in evolvability between clades. Cone snails are carnivorous, use prey-specific venom (conotoxins) to capture prey, and the genes that encode venom are known and diversify through gene duplication. Theory predicts that higher gene diversity confers a greater potential to generate novel phenotypes for specialization and adaptation. Therefore, if conotoxin gene diversity gives rise to varying levels of evolvability, conotoxin gene diversity should be coupled with macroevolutionary speciation rates. We applied exon capture techniques to recover phylogenetic markers and conotoxin loci across 314 species, the largest venom discovery effort in a single study. We paired a reconstructed timetree using 12 fossil calibrations with species-specific estimates of conotoxin gene diversity and used trait-dependent diversification methods to test the impact of evolvability on diversification patterns. Surprisingly, we did not detect any signal for the relationship between conotoxin gene diversity and speciation rates, suggesting that venom evolution may not be the rate-limiting factor controlling diversification dynamics in Conidae. Comparative analyses showed some signal for the impact of diet and larval dispersal strategy on diversification patterns, though detection of a signal depended on the dataset and the method. If our results remain true with increased taxonomic sampling in future studies, they suggest that the rapid evolution of conid venom may cause other factors to become more critical to diversification, such as ecological opportunity or traits that promote isolation among lineages.

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