N. Justin Marshall’s research while affiliated with The University of Queensland and other places

A variety of phylogenetically distant taxa, including flatworms, mollusks, amphibians, and fishes, use the deadly neurotoxin tetrodotoxin (TTX) for predation and defense. A well-known example is the blue-lined octopus, Hapalochlaena fasciata (Hoyle, 1886), which uses symbiotic bacteria to sequester TTX in its posterior salivary glands (PSG). When it bites, the TTX-laden saliva immobilizes large prey and has caused lethal envenomation in a few incidents involving humans. Female blue-lined octopuses are about twice the size of males, which bears the risk of males being cannibalized during reproduction. Surprisingly, we found that the PSG of males is roughly three times heavier than that of females. Using laboratory mating experiments, we show that males use a high-precision bite that targets the female’s aorta to inject TTX at the start of copulation. Envenomating the females renders them immobile, enabling the males to mate successfully.

Damselfishes (Pomacentridae) are widespread and highly abundant on tropical coral reefs. They exhibit diverse body colouration within and between the ~250 species and across ontogenetic stages. In addition to human‐visible colours (i.e., 400–700 nm), most adult damselfishes reflect ultraviolet (UV, 300–400 nm) colour patches. UV sensitivity and UV colour signals are essential for feeding and form the basis for a secret communication channel invisible to the many UV‐blind predatory fish on the reef; however, how these traits develop across ontogenetic stages and their distribution across the damselfish family is poorly characterised. Here, we used UV photography, phylogenetic reconstructions of opsin genes, and differential gene expression analysis (DGE) of retinal samples to investigate the development of UV vision and colour patterns in three ontogenetic stages (pre‐settlement larval, juvenile, and adult) of 11 damselfish species. Using DGE, we found similar gene expression between juveniles and adults, which strongly differed from larvae. All species and all stages expressed at least one UV‐sensitive sws1 opsin gene. However, UV body colour patterns only started to appear at the juvenile stage. Moreover, Pomacentrus species displayed highly complex UV body patterns that were correlated with the expression of two sws1 copies. This could mean that some damselfishes can discriminate colours that change only in their UV component. We demonstrate dramatic shifts in both UV sensitivity and UV colouration across the development stages of damselfish while highlighting the importance of considering ontogeny when studying the coevolution of visual systems and colour signals.

Octopus are well known for their rapidly changing and diverse body patterning achieved through combinations of chromatic, textural, postural and locomotory components. The function of octopus body patterns includes camouflage for prey ambush and predator avoidance, aposematic display to startle intruders and predators, and potentially intraspecific communication. However, as many octopus species are often solitary, body patterning during intraspecific social interactions is largely unexplored. Here we provide the first detailed description of body patterns and the associated components expressed during social interactions of the diurnal reef-dwelling species, Abdopus capricornicus. This is the first study aimed at disentangling the body patterns used for camouflage from those used for communication. This was achieved by staging interactions between octopus pairs under controlled conditions in a bare sand environment devoid of rocks or algae. While most studies on octopus interactions focused on mating behaviour, this study focused on the body patterns expressed during intrasexual (e.g. male-male, female-female) and intersexual interactions. Notably, A. capricornicus shows the richest body patterning repertoire among coastal octopuses studied so far, including 10 body patterns which comprise 27 chromatic, 8 postural and 10 locomotory components. In addition, 18 types of social encounters were identified. Numerous body patterns and components specifically expressed during their interactions were also identified, suggesting that the complexity of the visual stimuli experienced by A. capricornicus, including social cues from their frequent interactions, may contribute to its rich patterning.

Damselfishes (Pomacentridae) are widespread and highly abundant on tropical coral reefs. They exhibit diverse body colouration within and between the ∼250 species and across ontogenetic stages. In addition to human visible colours (i.e., 400-700 nm), most adult damselfishes reflect ultraviolet (UV, 300-400 nm) colour patches. UV sensitivity and UV colour signals are essential for feeding and form the basis for a secret communication channel invisible to the many UV-blind predatory fish on the reef; however, how these traits develop across ontogenetic stages, and their distribution across the damselfish family is poorly characterised. Here, we used UV photography, phylogenetic reconstructions of opsin genes, differential gene expression analysis (DGE) of retinal samples, to investigate the development of UV vision and colour patterns in three ontogenetic stages (pre-settlement larval, juvenile, and adult) of eleven damselfish species. Using DGE, we found similar gene expression between juveniles and adults, which strongly differed from larvae. All species and all stages expressed at least one UV-sensitive _sws1_ opsin gene. However, UV body colour patterns only started to appear at the juvenile stage. Moreover, _Pomacentrus_ species displayed highly complex UV body patterns that were correlated with the expression of two _sws1_ copies. This could mean that some damselfishes can discriminate colours that change only in their UV component. We demonstrate dramatic shifts in both UV sensitivity and UV colouration across the development stages of damselfish, while highlighting the importance of considering ontogeny when studying the coevolution of visual systems and colour signals.

[This corrects the article DOI: 10.1371/journal.pone.0261331.].

Damselfishes (Pomacentridae) are one of the most behaviourally diverse, colourful and species-rich reef fish families. One remarkable characteristic of damselfishes is their communication in ultraviolet (UV) light. Not only are they sensitive to UV, they are also prone to have UV-reflective colours and patterns enabling social signalling. Using more than 50 species, we aimed to uncover the evolutionary history of UV colour and UV vision in damselfishes. All damselfishes had UV-transmitting lenses, expressed the UV-sensitive SWS1 opsin gene, and most displayed UV-reflective patterns and colours. We find evidence for several tuning events across the radiation, and while SWS1 gene duplications are generally very rare among teleosts, our phylogenetic reconstructions uncovered two independent duplication events: one close to the base of the most species-rich clade in the subfamily Pomacentrinae, and one in a single Chromis species. Using amino acid comparisons, we found that known spectral tuning sites were altered several times in parallel across the damselfish radiation (through sequence change and duplication followed by sequence change), causing repeated shifts in peak spectral absorbance of around 10 nm. Pomacentrinae damselfishes expressed either one or both copies of SWS1, likely to further finetune UV-signal detection and differentiation. This highly advanced and modified UV vision among damselfishes, in particular the duplication of SWS1 among Pomacentrinae, might be seen as a key evolutionary innovation that facilitated the evolution of the exuberant variety of UV-reflectance traits and the diversification of this coral reef fish lineage.

In many animals, ultraviolet (UV) vision guides navigation, foraging, and communication, but few studies have addressed the contribution of UV signals to colour vision, or measured UV discrimination thresholds using behavioural experiments. Here, we tested UV colour vision in an anemonefish (Amphiprion ocellaris) using a five-channel (RGB-V-UV) LED display. We first determined that the maximal sensitivity of the A. ocellaris UV cone was ∼386 nm using microspectrophotometry. Three additional cone spectral sensitivities had maxima at ∼497, 515 and ∼535 nm. We then behaviourally measured colour discrimination thresholds by training anemonefish to distinguish a coloured target pixel from grey distractor pixels of varying intensity. Thresholds were calculated for nine sets of colours with and without UV signals. Using a tetrachromatic vision model, we found that anemonefish were better (i.e. discrimination thresholds were lower) at discriminating colours when target pixels had higher UV chromatic contrast. These colours caused a greater stimulation of the UV cone relative to other cone types. These findings imply that a UV component of colour signals and cues improves their detectability, which likely increases the prominence of anemonefish body patterns for communication and the silhouette of zooplankton prey.

Octopus are well known for their rapidly changing and diverse body patterning achieved through combinations of chromatic, textural and postural components. The function of octopus body patterns includes camouflage for prey ambush and predator avoidance, aposematic display to startle intruders and predators and potentially intraspecific communication. However, as many octopus species are often solitary animals, body patterning during intraspecific social interactions are largely unexplored. Here we start addressing this gap in one diurnal reef-dwelling species, Abdopus capricornicus, by providing the first detailed description of the body patterns and associated components expressed during social interactions in captivity. Importantly, this is the first study aimed at disentangling the body patterns used for camouflage from those used for communication. This was achieved by staging dyadic interactions between octopus pairs under controlled conditions in a bare sand environment devoid of rocks or algae. Furthermore, while most studies on octopus interactions focus on reproductive behaviour, here we recorded the body patterns expressed during both intrasexual (e.g. male-male, female-female) and intersexual interactions. We revealed that some body patterns and components are specifically expressed when octopuses are interacting. Furthermore, A. capricornicus shows the richest body patterning repertoire among coastal octopuses studied so far, including 10 body patterns which comprise 27 chromatic, 8 postural and 10 locomotory components. In addition, 19 types of social encounters were identified. We suggest that the complexity of the reef habitat and of the visual stimuli experienced by A. capricornicus, including social cues deriving from frequent interactions, may contribute to its patterning richness.