title: The Evolution of Fangs, Venom, and Mimicry Systems in Blenny Fishes.
abstract: Venom systems have evolved on multiple occasions across the animal kingdom, and they can act as key adaptations to protect animals from predators [1]. Consequently, venomous animals serve as models for a rich source of mimicry types, as non-venomous species benefit from reductions in predation risk by mimicking the coloration, body shape, and/or movement of toxic counterparts [2-5]. The frequent evolution of such deceitful imitations provides notable examples of phenotypic convergence and are often invoked as classic exemplars of evolution by natural selection. Here, we investigate the evolution of fangs, venom, and mimetic relationships in reef fishes from the tribe Nemophini (fangblennies). Comparative morphological analyses reveal that enlarged canine teeth (fangs) originated at the base of the Nemophini radiation and have enabled a micropredatory feeding strategy in non-venomous Plagiotremus spp. Subsequently, the evolution of deep anterior grooves and their coupling to venom secretory tissue provide Meiacanthus spp. with toxic venom that they effectively employ for defense. We find that fangblenny venom contains a number of toxic components that have been independently recruited into other animal venoms, some of which cause toxicity via interactions with opioid receptors, and result in a multifunctional biochemical phenotype that exerts potent hypotensive effects. The evolution of fangblenny venom has seemingly led to phenotypic convergence via the formation of a diverse array of mimetic relationships that provide protective (Batesian mimicry) and predatory (aggressive mimicry) benefits to other fishes [2, 6]. Our results further our understanding of how novel morphological and biochemical adaptations stimulate ecological interactions in the natural world.
authors.affiliation: Alistair Reid Venom Research Unit, Parasitology Department, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, UK. Electronic address: nicholas.casewell@lstmed.ac.uk.
authors.forename: Nicholas R
authors.initials: NR
authors.lastname: Casewell
authors.affiliation: Institute of Biology Leiden (IBL), Leiden University, Sylviusweg 72, 2333 BE, Leiden, the Netherlands.
authors.forename: Jeroen C
authors.initials: JC
authors.lastname: Visser
authors.affiliation: Venom Evolution Lab, School of Biological Sciences, The University of Queensland, St Lucia, QLD 4072, Australia.
authors.forename: Kate
authors.initials: K
authors.lastname: Baumann
authors.affiliation: Venom Evolution Lab, School of Biological Sciences, The University of Queensland, St Lucia, QLD 4072, Australia.
authors.forename: James
authors.initials: J
authors.lastname: Dobson
authors.affiliation: Monash Venom Group, Department of Pharmacology, Biomedicine Discovery Institute, Monash University, VIC 3800, Australia.
authors.forename: Han
authors.initials: H
authors.lastname: Han
authors.affiliation: Monash Venom Group, Department of Pharmacology, Biomedicine Discovery Institute, Monash University, VIC 3800, Australia; Department of Biochemistry & Molecular Biology, Biomedicine Discovery Institute, Monash University, VIC 3800, Australia.
authors.forename: Sanjaya
authors.initials: S
authors.lastname: Kuruppu
authors.affiliation: Centre for Pain Research, Institute for Molecular Bioscience, The University of Queensland, St Lucia, QLD 4072, Australia.
authors.forename: Michael
authors.initials: M
authors.lastname: Morgan
authors.affiliation: Vertebrate Palaeontology and Biomechanics Laboratory, School of Biological Sciences, The University of Queensland, St Lucia, QLD 4072, Australia.
authors.forename: Anthony
authors.initials: A
authors.lastname: Romilio
authors.affiliation: Morphological Evo-Devo Laboratory, School of Biological Sciences, The University of Queensland, St Lucia, QLD 4072, Australia.
authors.forename: Vera
authors.initials: V
authors.lastname: Weisbecker
authors.affiliation: Centre for Advanced Imaging, The University of Queensland, St Lucia, QLD 4072, Australia.
authors.forename: Karine
authors.initials: K
authors.lastname: Mardon
authors.affiliation: Venom Evolution Lab, School of Biological Sciences, The University of Queensland, St Lucia, QLD 4072, Australia; HEJ Research Institute of Chemistry, International Centre for Chemical and Biological Sciences (ICCBS), University of Karachi, Karachi 75270, Pakistan.
authors.forename: Syed A
authors.initials: SA
authors.lastname: Ali
authors.affiliation: Venom Evolution Lab, School of Biological Sciences, The University of Queensland, St Lucia, QLD 4072, Australia.
authors.forename: Jordan
authors.initials: J
authors.lastname: Debono
authors.affiliation: Venom Evolution Lab, School of Biological Sciences, The University of Queensland, St Lucia, QLD 4072, Australia.
authors.forename: Ivan
authors.initials: I
authors.lastname: Koludarov
authors.affiliation: Department of Radiology, Leiden University Medical Center, Leiden, 2300 RC, the Netherlands.
authors.forename: Ivo
authors.initials: I
authors.lastname: Que
authors.affiliation: Molecular Ecology and Evolution Group, School of Biological Sciences, Bangor University, Deiniol Road, Bangor LL57 2UW, UK.
authors.forename: Gregory C
authors.initials: GC
authors.lastname: Bird
authors.affiliation: Molecular Ecology and Evolution Group, School of Biological Sciences, Bangor University, Deiniol Road, Bangor LL57 2UW, UK; Department of Life Sciences, Anglia Ruskin University, Cambridge CB1 1PT, UK.
authors.forename: Gavan M
authors.initials: GM
authors.lastname: Cooke
authors.affiliation: School of Chemistry and Molecular Biosciences, The University of Queensland, St Lucia, QLD 4072, Australia.
authors.forename: Amanda
authors.initials: A
authors.lastname: Nouwens
authors.affiliation: Monash Venom Group, Department of Pharmacology, Biomedicine Discovery Institute, Monash University, VIC 3800, Australia.
authors.forename: Wayne C
authors.initials: WC
authors.lastname: Hodgson
authors.affiliation: Bioinformatics Unit, Parasitology Department, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, UK.
authors.forename: Simon C
authors.initials: SC
authors.lastname: Wagstaff
authors.affiliation: Visual Ecology Laboratory, School of Biological Sciences, The University of Queensland, St Lucia, QLD 4072, Australia.
authors.forename: Karen L
authors.initials: KL
authors.lastname: Cheney
authors.affiliation: Centre for Pain Research, Institute for Molecular Bioscience, The University of Queensland, St Lucia, QLD 4072, Australia.
authors.forename: Irina
authors.initials: I
authors.lastname: Vetter
authors.affiliation: Department of Radiology, Leiden University Medical Center, Leiden, 2300 RC, the Netherlands; Department of Human Genetics, Leiden University Medical Center, Leiden, 2300 RC, the Netherlands.
authors.forename: Louise
authors.initials: L
authors.lastname: van der Weerd
authors.affiliation: Institute of Biology Leiden (IBL), Leiden University, Sylviusweg 72, 2333 BE, Leiden, the Netherlands.
authors.forename: Michael K
authors.initials: MK
authors.lastname: Richardson
authors.affiliation: Venom Evolution Lab, School of Biological Sciences, The University of Queensland, St Lucia, QLD 4072, Australia. Electronic address: bgfry@uq.edu.au.
authors.forename: Bryan G
authors.initials: BG
authors.lastname: Fry
mesh_terms: D000222:Adaptation, Physiological; D000818:Animals; D005075:Biological Evolution; D005399:Fishes / Q000502:physiology*; D010641:Phenotype; D010858:Pigmentation; D011235:Predatory Behavior; D020543:Proteome / Q000032:analysis; D012641:Selection, Genetic; D014688:Venoms
chemical_list: D020543:Proteome; D014688:Venoms
keywords: Meiacanthus; adaptation; convergence; defense; evolution; hypotension; mimicry; opioid; toxin; venom