Evolutionary Ecology of Fish Venom: Adaptations and Consequences of Evolving a Venom System

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: aposematism; coevolution; ecological niche; ecology; evolution; evolutionary ecology; fish; mimicry; natural enemy interactions; venom.

Figure 1

A phylogenetic tree of fish families (excluding cyclostomes) highlighting all known venomous families in orange. The exact number of venomous fish families lies between 58 and 63 [12]. The phylogenies of Chondrichthyes and Actinopterygii were obtained from the Time Tree web project (www.timetree.org) and merged using R package phytools [16].

Figure 2

Examples of the different morphological structures used by fish to deliver venom. This figure is reproduced from Ziegman and Alewood [11], 2015, MDPI. The venom apparatuses are highlighted in red: (A) Serrated dorsal spine of chimera; (B) serrated caudal spine of stingray; (C) serrated pectoral spine of catfish; (D) canine tooth of fangblenny; (E) dorsal and opercular spines of toadfish; (F) dorsal and opercular spines of weeverfish; (G) dorsal, pectoral, and pelvic spines of gurnard perch; and (H) dorsal and anal spines with venom gland in stonefish.

Figure 3

Examples of aposematic colouration adopted by venomous fish species: (A) Lesser weever fish (Echiichthys vipera); (B) Lionfish (Pterois volitans); (C) Bluespotted ribbontail ray (Taeniura lymma); (D) Striped eel catfish (Plotosus lineatus); (E) Striped fang blenny (Meiacanthus grammistes); and (F) Devil scorpionfish (Inimicus didactylus). Image copyrights ©: Rachel Scott, Niels Sloth via www.biopix.dk, Jens Petersen via https://www.en.wikipedia.org CC BY 2.5, Elias Levy via https://www.flickr.com CC BY 2.0, Neil Hepworth—Bauer Media via https://practicalfishkeeping.co.uk, David Harasti via https://www.daveharasti.com.

Figure 4

Examples of Müllerian mimetic patterns in venomous Corydoras catfish mimicry ring communities. (A) Corydoras multimaculatus, C. araguaiaensis and C. sp. (left to right) and (B) C. imitator (left) and C. sp. (right). Images courtesy of © Martin Taylor via https://www.flickr.com/photos/99775901@N03/.