scholarly journals Prey-Capture Strategies of Fish-Hunting Cone Snails: Behavior, Neurobiology and Evolution

2015 ◽  
Vol 86 (1) ◽  
pp. 58-74 ◽  
Author(s):  
Baldomero M. Olivera ◽  
Jon Seger ◽  
Martin P. Horvath ◽  
Alexander E. Fedosov

The venomous fish-hunting cone snails (Conus) comprise eight distinct lineages evolved from ancestors that preyed on worms. In this article, we attempt to reconstruct events resulting in this shift in food resource by closely examining patterns of behavior, biochemical agents (toxins) that facilitate prey capture and the combinations of toxins present in extant species. The first sections introduce three different hunting behaviors associated with piscivory: ‘taser-and-tether', ‘net-engulfment' and ‘strike-and-stalk'. The first two fish-hunting behaviors are clearly associated with distinct groups of venom components, called cabals, which act in concert to modify the behavior of prey in a specific manner. Derived fish-hunting behavior clearly also correlates with physical features of the radular tooth, the device that injects these biochemical components. Mapping behavior, biochemical components and radular tooth features onto phylogenetic trees shows that fish-hunting behavior emerged at least twice during evolution. The system presented here may be one of the best examples where diversity in structure, physiology and molecular features were initially driven by particular pathways selected through behavior.

2019 ◽  
Vol 9 (1) ◽  
Author(s):  
Mriga Dutt ◽  
Jean Giacomotto ◽  
Lotten Ragnarsson ◽  
Åsa Andersson ◽  
Andreas Brust ◽  
...  

AbstractCone snails use separately evolved venoms for prey capture and defence. While most use a harpoon for prey capture, the Gastridium clade that includes the well-studied Conus geographus and Conus tulipa, have developed a net hunting strategy to catch fish. This unique feeding behaviour requires secretion of “nirvana cabal” peptides to dampen the escape response of targeted fish allowing for their capture directly by mouth. However, the active components of the nirvana cabal remain poorly defined. In this study, we evaluated the behavioural effects of likely nirvana cabal peptides on the teleost model, Danio rerio (zebrafish). Surprisingly, the conantokins (NMDA receptor antagonists) and/or conopressins (vasopressin receptor agonists and antagonists) found in C. geographus and C. tulipa venom failed to produce a nirvana cabal-like effect in zebrafish. In contrast, low concentrations of the non-competitive adrenoceptor antagonist ρ-TIA found in C. tulipa venom (EC50 = 190 nM) dramatically reduced the escape response of zebrafish larvae when added directly to aquarium water. ρ-TIA inhibited the zebrafish α1-adrenoceptor, confirming ρ-TIA has the potential to reverse the known stimulating effects of norepinephrine on fish behaviour. ρ-TIA may act alone and not as part of a cabal, since it did not synergise with conopressins and/or conantokins. This study highlights the importance of using ecologically relevant animal behaviour models to decipher the complex neurobiology underlying the prey capture and defensive strategies of cone snails.


Author(s):  
W. Barthlott ◽  
M. Mail ◽  
C. Neinhuis

A comprehensive survey of the construction principles and occurrences of superhydrophobic surfaces in plants, animals and other organisms is provided and is based on our own scanning electron microscopic examinations of almost 20 000 different species and the existing literature. Properties such as self-cleaning (lotus effect), fluid drag reduction (Salvinia effect) and the introduction of new functions (air layers as sensory systems) are described and biomimetic applications are discussed: self-cleaning is established, drag reduction becomes increasingly important, and novel air-retaining grid technology is introduced. Surprisingly, no evidence for lasting superhydrophobicity in non-biological surfaces exists (except technical materials). Phylogenetic trees indicate that superhydrophobicity evolved as a consequence of the conquest of land about 450 million years ago and may be a key innovation in the evolution of terrestrial life. The approximate 10 million extant species exhibit a stunning diversity of materials and structures, many of which are formed by self-assembly, and are solely based on a limited number of molecules. A short historical survey shows that bionics (today often called biomimetics) dates back more than 100 years. Statistical data illustrate that the interest in biomimetic surfaces is much younger still. Superhydrophobicity caught the attention of scientists only after the extreme superhydrophobicity of lotus leaves was published in 1997. Regrettably, parabionic products play an increasing role in marketing. This article is part of the themed issue ‘Bioinspired hierarchically structured surfaces for green science’.


PeerJ ◽  
2016 ◽  
Vol 4 ◽  
pp. e1915 ◽  
Author(s):  
Eric R. Larson ◽  
Magalie Castelin ◽  
Bronwyn W. Williams ◽  
Julian D. Olden ◽  
Cathryn L. Abbott

Molecular genetic approaches are playing an increasing role in conservation science by identifying biodiversity that may not be evident by morphology-based taxonomy and systematics. So-called cryptic species are particularly prevalent in freshwater environments, where isolation of dispersal-limited species, such as crayfishes, within dendritic river networks often gives rise to high intra- and inter-specific genetic divergence. We apply here a multi-gene molecular approach to investigate relationships among extant species of the crayfish genusPacifastacus, representing the first comprehensive phylogenetic study of this taxonomic group. Importantly,Pacifastacusincludes both the widely invasive signal crayfishPacifastacus leniusculus,as well as several species of conservation concern like the Shasta crayfishPacifastacus fortis. Our analysis used 83 individuals sampled across the four extantPacifastacusspecies (omitting the extinctPacifastacus nigrescens), representing the known taxonomic diversity and geographic distributions within this genus as comprehensively as possible. We reconstructed phylogenetic trees from mitochondrial (16S, COI) and nuclear genes (GAPDH), both separately and using a combined or concatenated dataset, and performed several species delimitation analyses (PTP, ABGD, GMYC) on the COI phylogeny to propose Primary Species Hypotheses (PSHs) within the genus. All phylogenies recovered the genusPacifastacusas monophyletic, within which we identified a range of six to 21 PSHs; more abundant PSHs delimitations from GMYC and ABGD were always nested within PSHs delimited by the more conservative PTP method.Pacifastacus leniusculusincluded the majority of PSHs and was not monophyletic relative to the otherPacifastacusspecies considered. Several of these highly distinctP. leniusculusPSHs likely require urgent conservation attention. Our results identify research needs and conservation priorities forPacifastacuscrayfishes in western North America, and may inform better understanding and management ofP. leniusculusin regions where it is invasive, such as Europe and Japan.


2021 ◽  
Author(s):  
Graeme T Lloyd ◽  
Graham J Slater

Abstract Phylogenetic trees provide a powerful framework for testing macroevolutionary hypotheses, but it is becoming increasingly apparent that inferences derived from extant species alone can be highly misleading. Trees incorporating living and extinct taxa are are needed to address fundamental questions about the origins of diversity and disparity but it has proved challenging to generate robust, species-rich phylogenies that include large numbers of fossil taxa. As a result, most studies of diversification dynamics continue to rely on molecular phylogenies. Here, we extend and apply a recently developed meta-analytic approach for synthesizing previously published phylogenetic studies to infer a well-resolved set of species level, time-scaled phylogenetic hypotheses for extinct and extant cetaceans (whales, dolphins and allies). Our trees extend sampling from the ∼ 90 extant species to over 500 living and extinct species, and therefore allow for more robust inference of macroevolutionary dynamics. While the diversification scenarios we recover are broadly concordant with those inferred from molecular phylogenies they differ in critical ways, notably in the relative contributions of extinction and speciation rate shifts in driving rapid radiations. The metatree approach provides the most immediate route for generating higher level phylogenies of extinct taxa, and opens the door to re-evaluation of macroevolutionary hypotheses derived only from extant taxa.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
S. W. A. Himaya ◽  
Ai-Hua Jin ◽  
Brett Hamilton ◽  
Subash K. Rai ◽  
Paul Alewood ◽  
...  

AbstractThe venom duct origins of predatory and defensive venoms has not been studied for hook-and-line fish hunting cone snails despite the pharmacological importance of their venoms. To better understand the biochemistry and evolution of injected predatory and defensive venoms, we compared distal, central and proximal venom duct sections across three specimens of C. striatus (Pionoconus) using proteomic and transcriptomic approaches. A total of 370 conotoxin precursors were identified from the whole venom duct transcriptome. Milked defensive venom was enriched with a potent cocktail of proximally expressed inhibitory α-, ω- and μ-conotoxins compared to milked predatory venom. In contrast, excitatory κA-conotoxins dominated both the predatory and defensive venoms despite their distal expression, suggesting this class of conotoxin can be selectively expressed from the same duct segment in response to either a predatory or defensive stimuli. Given the high abundance of κA-conotoxins in the Pionoconus clade, we hypothesise that the κA-conotoxins have evolved through adaptive evolution following their repurposing from ancestral inhibitory A superfamily conotoxins to facilitate the dietary shift to fish hunting and species radiation in this clade.


2019 ◽  
Author(s):  
Donald Davesne ◽  
François J. Meunier ◽  
Armin D. Schmitt ◽  
Matt Friedman ◽  
Olga Otero ◽  
...  

Vertebrate bone is composed of three main cell types: osteoblasts, osteoclasts and osteocytes, the latter being by far the most numerous. Osteocytes are thought to play a fundamental role in bone physiology and homeostasis, however they are entirely absent in most extant species of teleosts, a group that comprises the vast majority of bony ‘fishes’, and approximately half of vertebrates. Understanding how this acellular (anosteocytic) bone appeared and was maintained in such an important vertebrate group has important implications for our understanding of the function and evolution of osteocytes. Nevertheless, although it is clear that cellular bone is ancestral for teleosts, it has not been clear in which specific subgroup the osteocytes were lost. This review aims at clarifying the phylogenetic distribution of cellular and acellular bone in teleosts, to identify its precise origin, reversals to cellularity, and their implications. We surveyed the bone type for more than 600 fossil and extant ray-finned fish species and optimised the results on recent large-scale molecular phylogenetic trees, estimating ancestral states. We find that acellular bone is a probable synapomorphy of Euteleostei, a group uniting approximately two-thirds of teleost species. We also confirm homoplasy in these traits: acellular bone occurs in some non-euteleosts (although rarely), and cellular bone was reacquired several times independently within euteleosts, in salmons and relatives, tunas and the opah (Lampris sp.). The occurrence of peculiar ecological (e.g. anadromous migration) and physiological (e.g. red-muscle endothermy) strategies in these lineages might explain the reacquisition of osteocytes. Our review supports that the main contribution of osteocytes in teleost bone is to mineral homeostasis (via osteocytic osteolysis) and not to strain detection or bone remodelling, helping to clarify their role in bone physiology.


PeerJ ◽  
2018 ◽  
Vol 6 ◽  
pp. e4331 ◽  
Author(s):  
Gustavo Sanchez ◽  
Davin H.E. Setiamarga ◽  
Surangkana Tuanapaya ◽  
Kittichai Tongtherm ◽  
Inger E. Winkelmann ◽  
...  

Comprising more than 800 extant species, the class Cephalopoda (octopuses, squid, cuttlefish, and nautiluses) is a fascinating group of marine conchiferan mollusks. Recently, the first cephalopod genome (of Octopus bimaculoides) was published, providing a genomic framework, which will enable more detailed investigations of cephalopod characteristics, including developmental, morphological, and behavioural traits. Meanwhile, a robust phylogeny of the members of the subclass Coleoidea (octopuses, squid, cuttlefishes) is crucial for comparative and evolutionary studies aiming to investigate the group’s traits and innovations, but such a phylogeny has proven very challenging to obtain. Here, we present the results of phylogenetic inference at the genus level using mitochondrial and nuclear marker sequences available from public databases. Topologies are presented which show support for (1) the monophyly of the two main superorders, Octobrachia and Decabrachia, and (2) some of the interrelationships at the family level. We have mapped morphological characters onto the tree and conducted molecular dating analyses, obtaining congruent results with previous estimates of divergence in major lineages. Our study also identifies unresolved phylogenetic relationships within the cephalopod phylogeny and insufficient taxonomic sampling among squids excluding the Loliginidae in the Decabrachia and within the Order Cirromorphida in the Octobrachia. Genomic and transcriptomic resources should enable resolution of these issues in the relatively near future. We provide our alignment as an open access resource, to allow other researchers to reconstruct phylogenetic trees upon this work in the future.


2015 ◽  
Vol 112 (6) ◽  
pp. 1743-1748 ◽  
Author(s):  
Helena Safavi-Hemami ◽  
Joanna Gajewiak ◽  
Santhosh Karanth ◽  
Samuel D. Robinson ◽  
Beatrix Ueberheide ◽  
...  

More than 100 species of venomous cone snails (genus Conus) are highly effective predators of fish. The vast majority of venom components identified and functionally characterized to date are neurotoxins specifically targeted to receptors, ion channels, and transporters in the nervous system of prey, predators, or competitors. Here we describe a venom component targeting energy metabolism, a radically different mechanism. Two fish-hunting cone snails, Conus geographus and Conus tulipa, have evolved specialized insulins that are expressed as major components of their venoms. These insulins are distinctive in having much greater similarity to fish insulins than to the molluscan hormone and are unique in that posttranslational modifications characteristic of conotoxins (hydroxyproline, γ-carboxyglutamate) are present. When injected into fish, the venom insulin elicits hypoglycemic shock, a condition characterized by dangerously low blood glucose. Our evidence suggests that insulin is specifically used as a weapon for prey capture by a subset of fish-hunting cone snails that use a net strategy to capture prey. Insulin appears to be a component of the nirvana cabal, a toxin combination in these venoms that is released into the water to disorient schools of small fish, making them easier to engulf with the snail’s distended false mouth, which functions as a net. If an entire school of fish simultaneously experiences hypoglycemic shock, this should directly facilitate capture by the predatory snail.


2019 ◽  
Vol 116 (34) ◽  
pp. 16921-16926 ◽  
Author(s):  
Venelin Mitov ◽  
Krzysztof Bartoszek ◽  
Tanja Stadler

Phylogenetic comparative methods are widely used to understand and quantify the evolution of phenotypic traits, based on phylogenetic trees and trait measurements of extant species. Such analyses depend crucially on the underlying model. Gaussian phylogenetic models like Brownian motion and Ornstein–Uhlenbeck processes are the workhorses of modeling continuous-trait evolution. However, these models fit poorly to big trees, because they neglect the heterogeneity of the evolutionary process in different lineages of the tree. Previous works have addressed this issue by introducing shifts in the evolutionary model occurring at inferred points in the tree. However, for computational reasons, in all current implementations, these shifts are “intramodel,” meaning that they allow jumps in 1 or 2 model parameters, keeping all other parameters “global” for the entire tree. There is no biological reason to restrict a shift to a single model parameter or, even, to a single type of model. Mixed Gaussian phylogenetic models (MGPMs) incorporate the idea of jointly inferring different types of Gaussian models associated with different parts of the tree. Here, we propose an approximate maximum-likelihood method for fitting MGPMs to comparative data comprising possibly incomplete measurements for several traits from extant and extinct phylogenetically linked species. We applied the method to the largest published tree of mammal species with body- and brain-mass measurements, showing strong statistical support for an MGPM with 12 distinct evolutionary regimes. Based on this result, we state a hypothesis for the evolution of the brain–body-mass allometry over the past 160 million y.


2020 ◽  
Vol 60 (5) ◽  
pp. 1251-1267 ◽  
Author(s):  
Karin H Olsson ◽  
Christopher H Martin ◽  
Roi Holzman

Abstract The complex interplay between form and function forms the basis for generating and maintaining organismal diversity. Fishes that rely on suction-feeding for prey capture exhibit remarkable phenotypic and trophic diversity. Yet the relationships between fish phenotypes and feeding performance on different prey types are unclear, partly because the morphological, biomechanical, and hydrodynamic mechanisms that underlie suction-feeding are complex. Here we demonstrate a general framework to investigate the mapping of multiple phenotypic traits to performance by mapping kinematic variables to suction-feeding capacity. Using a mechanistic model of suction-feeding that is based on core physical principles, we predict prey capture performance across a broad range of phenotypic trait values, for three general prey types: mollusk-like prey, copepod-like prey, and fish-like prey. Mollusk-like prey attach to surfaces, copepod-like prey attempt to escape upon detecting the hydrodynamic disturbance produced by the predator, and fish-like prey attempt to escape when the predator comes within a threshold distance. This approach allowed us to evaluate suction-feeding performance for any combination of six key kinematic traits, irrespective of whether these trait combinations were observed in an extant species, and to generate a multivariate mapping of phenotype to performance. We used gradient ascent methods to explore the complex topography of the performance landscape for each prey type, and found evidence for multiple peaks. Characterization of phenotypes associated with performance peaks indicates that the optimal kinematic parameter range for suction-feeding on different prey types are narrow and distinct from each other, suggesting different functional constraints for the three prey types. These performance landscapes can be used to generate hypotheses regarding the distribution of extant species in trait space and their evolutionary trajectories toward adaptive peaks on macroevolutionary fitness landscapes.


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