toxins Review Evolutionary Ecology of Fish Venom: Adaptations and Consequences of Evolving a Venom System Richard J. Harris 1,* and Ronald A. Jenner 2,* 1 Venom Evolution Lab, School of Biological Sciences, The University of Queensland, St Lucia, Brisbane, Queensland 4072, Australia 2 Department of Life Sciences, the Natural History Museum, Cromwell Road, London SW7 5BD, UK * Correspondence: [email protected] (R.J.H.); [email protected] (R.A.J.) Received: 14 December 2018; Accepted: 18 January 2019; Published: 22 January 2019 Abstract: Research on venomous animals has mainly focused on the molecular, biochemical, and pharmacological aspects of venom toxins. However, it is the relatively neglected broader study of evolutionary ecology that is crucial for understanding the biological relevance of venom systems. As fish have convergently evolved venom systems multiple times, it makes them ideal organisms to investigate the evolutionary ecology of venom on a broader scale. This review outlines what is known about how fish venom systems evolved as a result of natural enemy interactions and about the ecological consequences of evolving a venom system. This review will show how research on the evolutionary ecology of venom in fish can aid in understanding the evolutionary ecology of animal venoms more generally. Further, understanding these broad ecological questions can shed more light on the other areas of toxinology, with applications across multiple disciplinary fields. Keywords: evolution; ecology; fish; venom; evolutionary ecology; coevolution; natural enemy interactions; ecological niche; aposematism; mimicry Key Contribution: This is a comprehensive review of the evolutionary ecology of venomous fish. It discusses the consequences and adaptations associated with the evolution of venom systems in fish. 1. Introduction Animal venoms have been the subject of much research, particularly in reptiles, arachnids, insects, and cone snails [1–6]. The biological activity of venom components and their characterisation have been at the forefront of toxinology for many years. This has led to some ground-breaking biochemical, genetic, evolutionary, and pharmacological discoveries [7–10]. In contrast, the evolutionary aspects of venom, particularly their evolutionary ecology, remain poorly studied. Investigating the evolution of venomous traits in the context of their ecology can answer many questions about how and why venom systems have evolved and shed light on the adaptive value and ecological implications of evolving a venom system. Venom systems play a vital role as key fitness components that facilitate survival and reproductive success. Yet, traits relevant to understanding the evolutionary ecology of venom systems, including their morphology, the behaviour of venomous organisms, the presence and nature of aposematic, and mimetic traits, as well as the niche spaces and life histories of venomous species all deserve more detailed investigations across a broader range of venomous species. Venomous fish have been relatively poorly studied, both with respect to the composition and evolution of their venoms [11–13]. The focus of this review is to summarize what is known about the evolution of fish venoms considered from an ecological perspective and, where possible, to place it in the context of the evolutionary ecology of other venomous/toxic taxa. Toxins 2019, 11, 60; doi:10.3390/toxins11020060 www.mdpi.com/journal/toxins ToxinsToxins 20192019, 11, 11, 60, 60 2 of2 of21 21 A Brief Introduction to Venomous Fish: Morphology and Biochemistry A Brief Introduction to Venomous Fish: Morphology and Biochemistry Fish venom systems are thought to have convergently evolved 19 times (we include the toxic buccal Fishsecretions venom of systems lamprey are as thoughtvenom) (Figure to have 1), convergently with more than evolved 2900 19species times utilising (we include venom the as toxic a formbuccal of defence, secretions while of lamprey a few species as venom) use venom (Figure for1), predation/competition with more than 2900 species [12–15]. utilising Venom venomevolution as a hasform had of a defence,particularly while large a few impact species in usethe lineage venoms for Scorpaeniformes predation/competition (scorpionfish [12–15 and]. Venom relatives) evolution and Siluriformeshas had a particularly (catfish), which large together impact incomprise the lineages the majority Scorpaeniformes of venomous (scorpionfish fish species and [12] relatives) (Figure 1). and SiluriformesFish deliver (catfish), venom which through together a range comprise of structures, the majority such as of spines, venomous barbs, fish and species teeth/fangs [12] (Figure [12,13]1). (FigureFish 2). Venom deliver spines venom can through be part a rangeof dorsal, of structures, pectoral, pelvic, such as and spines, anal barbs,fins, as and well teeth/fangs associated [with12,13 ] or(Figure positioned2). Venom close to spines the operculum, can be part whilst of dorsal, stingray pectoral, barbs pelvic, are found and analon the fins, tail. as Morphological well associated analyseswith or of positioned fish venom close systems to the indicate operculum, that whilstspines stingrayare usually barbs associated are found with on thesome tail. form Morphological of venom gland/secretoryanalyses of fish cells venom located systems near indicateor surrounding that spines the arespines. usually Spines associated usually withcontain some an formanterolateral of venom groovegland/secretory that allows cells venom located to move near orfrom surrounding the base of the the spines. spine Spines to the usuallytip in a contain hypodermic an anterolateral fashion [12,13],groove allowing that allows the venom toxins toentry move into from the the enveno base ofmated the spine target to thevia tip a wound. in a hypodermic Although fashion this is [12 the,13 ], generalallowing morphology the toxins of entry venom into spines, the envenomated there are diffe targetrences via between a wound. species Although (Figure this 2) as is thewould general be expectedmorphology for convergently of venom spines, evolved there systems are differences (see Smith between et al. [12] species for a more (Figure in-depth2) as would review). be expected for convergently evolved systems (see Smith et al. [12] for a more in-depth review). Figure 1. A phylogenetic tree of fish families (excluding cyclostomes) highlighting all known venomous Figurefamilies 1. A in orange.phylogenetic The exacttree numberof fish families of venomous (exclu fishding families cyclostomes) lies between highlighting 58 and all 63 [known12]. The venomousphylogenies families of Chondrichthyes in orange. The andexact Actinopterygii number of venomous were obtained fish families from the lies Time between Tree 58 web and project 63 [12].(www.timetree.org The phylogenies) andof Chondric mergedhthyes using Rand package Actinopterygii phytools [were16]. obtained from the Time Tree web project (www.timetree.org) and merged using R package phytools [16]. Toxins 2019, 11, 60 3 of 21 Toxins 2019, 11, 60 3 of 21 FigureFigure 2. Examples ofof the the different different morphological morphological structures structures used used by fishby tofish deliver to deliver venom. venom. This figure This figureis reproduced is reproduced from Ziegman from Ziegman and Alewood and Alewood [11], 2015, [11], MDPI. 2015, The MDPI. venom The apparatuses venom apparatuses are highlighted are highlightedin red: (A) Serrated in red: dorsal(A) Serrated spine ofdorsal chimera; spine (B )of serrated chimera; caudal (B) serrated spine of caudal stingray; spine (C) serratedof stingray; pectoral (C) serratedspine of catfish;pectoral ( Dspine) canine of catfish; tooth of (D fangblenny;) canine tooth (E) of dorsal fangblenny; and opercular (E) dorsal spines and of opercular toadfish; (spinesF) dorsal of toadfish;and opercular (F) dorsal spines and of weeverfish;opercular spines (G) dorsal, of weeverfish; pectoral, and(G) pelvicdorsal, spines pectoral, of gurnard and pelvic perch; spines and (Hof) gurnarddorsal and perch; anal and spines (H)with dorsal venom and anal gland spines in stonefish. with venom gland in stonefish. FishFish venoms venoms contain contain a a plethora plethora of of compounds, compounds, the the majority majority of of which which are are defensive defensive in in nature, nature, with the the sole sole purpose purpose of of causing causing discomfort discomfort and and pain pain to to any any potential potential predator. predator. Bioactive Bioactive toxins toxins from from fishfish venoms venoms cause cause a a range range of of neuromuscular, neuromuscular, cardiovascular, cardiovascular, cytotoxic, cytotoxic, and and nociceptive nociceptive effects effects [11]. [11]. TheThe biochemistry biochemistry of of toxins toxins also also differs differs between between and and within within lineages. lineages. Large Large pore-forming pore-forming toxins, toxins, such assuch stonustoxin as stonustoxin and verrucotoxin and verrucotoxin can be can found be foundin many in scorpaenid many scorpaenid fish (e.g., fish Synanceia (e.g., Synanceia horrida horridaand S. verrucosaand S. verrucosa). Whilst). there Whilst are there many are other many protein/peptide other protein/peptide toxins (dracotoxin, toxins (dracotoxin, trachinine, trachinine, and nattectin, and etc.)nattectin, that have etc.) thatbeen have isolated been isolatedfrom different from different species species(e.g., Echiichthys (e.g., Echiichthys vipera, vipera,Trachinus Trachinus draco,draco, and