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Vertebrate dentitions are extraordinarily diverse in both morphology and regenerative capacity. The teleost order Tetraodontiformes exhibits an exceptional array of novel dental morphologies, epitomized by constrained beak-like dentitions in several families, i.e., porcupinefishes, three-toothed pufferfishes, ocean sunfishes, and pufferfishes. Modification of tooth replacement within these groups leads to the progressive accumulation of tooth generations, underlying the structure of their beaks. We focus on the dentition of the pufferfish (Tetraodontidae) because of its distinct dental morphology. This complex dentition develops as a result of (i) a reduction in the number of tooth positions from seven to one per quadrant during the transition from first to second tooth generations and (ii) a dramatic shift in tooth morphogenesis following the development of the first-generation teeth, leading to the elongation of dental units along the jaw. Gene expression and 1,1′-Dioctadecyl-3,3,3′,3′-tetramethylindocarbocyanine perchlorate (DiI) lineage tracing reveal a putative dental epithelial progenitor niche, suggesting a highly conserved mechanism for tooth regeneration despite the development of a unique dentition. MicroCT analysis reveals restricted labial openings in the beak, through which the dental epithelium (lamina) invades the cavity of the highly mineralized beak. Reduction in the number of replacement tooth positions coincides with the development of only four labial openings in the pufferfish beak, restricting connection of the oral epithelium to the dental cavity. Our data suggest the spatial restriction of dental regeneration, coupled with the unique extension of the replacement dental units throughout the jaw, are primary contributors to the evolution and development of this unique beak-like dentition.

1. Ocean sunfish (Mola mola) were believed to be inactive jellyfish feeders because they are often observed lying motionless at the sea surface. Recent tracking studies revealed that they are actually deep divers, but there has been no evidence of foraging in deep water. Furthermore, the surfacing behaviour of ocean sunfish was thought to be related to behavioural thermoregulation, but there was no record of sunfish body temperature. 2. Evidence of ocean sunfish feeding in deep water was obtained using a combination of an animal-borne accelerometer and camera with a light source. Siphonophores were the most abundant prey items captured by ocean sunfish and were typically located at a depth of 50–200 m where the water temperature was <12 °C. Ocean sunfish were diurnally active, made frequently deep excursions and foraged mainly at 100–200 m depths during the day. 3. Ocean sunfish body temperatures were measured under natural conditions. The body temperatures decreased during deep excursions and recovered during subsequent surfacing periods. Heat-budget models indicated that the whole-body heat-transfer coefficient between sunfish and the surrounding water during warming was 3–7 times greater than that during cooling. These results suggest that the main function of surfacing is the recovery of body temperature, and the fish might be able to increase heat gain from the warm surface water by physiological regulation. 4. The thermal environment of ocean sunfish foraging depths was lower than their thermal preference (c. 16–17 °C). The behavioural and physiological thermoregulation enables the fish to increase foraging time in deep, cold water. 5. Feeding rate during deep excursions was not related to duration or depth of the deep excursions. Cycles of deep foraging and surface warming were explained by a foraging strategy, to maximize foraging time with maintaining body temperature by vertical temperature environment.

Innovations in locomotor morphology have been invoked as important drivers of vertebrate diversification, although the influence of novel locomotion strategies on marine fish diversification remains largely unexplored. Using triggerfish as a case study, we determine whether the evolution of the distinctive synchronization of enlarged dorsal and anal fins that triggerfish use to swim may have catalyzed the ecological diversification of the group. By adopting a comparative phylogenetic approach to quantify median fin and body shape integration and to assess the tempo of functional and morphological evolution in locomotor traits, we find that: (1) functional and morphological components of the locomotive system exhibit a strong signal of correlated evolution; (2) triggerfish partitioned locomotor morphological and functional spaces early in their history; and (3) there is no strong evidence that a pulse of lineage diversification accompanied the major episode of phenotypic diversification. Together these findings suggest that the acquisition of a distinctive mode of locomotion drove an early radiation of shape and function in triggerfish, but not an early radiation of species.

Satellite-tracking of adult bumphead sunfish, Mola alexandrini , revealed long-distance latitudinal migration patterns covering thousands of kilometers. Horizontal and vertical movements of four bumphead sunfish off Taiwan were recorded with pop-up satellite archival tags in 2019–2020. Two individuals moved northward and traveled to Okinawa Island and Kyushu, Japan and two moved southwards; crossing the equator, to Papua New Guinea and New Caledonia. During daytime, bumphead sunfish descended below the thermocline and ascended to mixed layer depths (MLD) during nighttime. The N–S migrants, however, demonstrated different habitat utilization patterns. Instead of using prevailing currents, the northward movements of sunfish cohorts exhibited extensive use of mesoscale eddies. Fish in anticyclonic eddies usually occupied deeper habitats whereas those in cyclonic eddies used near-surface habitats. On northward excursions, fish spent most of their time in regions with high dissolved oxygen concentrations. Southward movement patterns were associated with major currents and thermal stratification of the water column. In highly stratified regions, fish stayed below the thermocline and frequently ascended to MLD during daytime either to warm muscles or repay oxygen debts. These results for bumphead sunfish present important insights into different habitat use patterns and the ability to undergo long-distance migrations over varying spatial-temporal scales and features.

Mimicry of warning signals is common, and can be mutualistic when mimetic species harbour equal levels of defence (Müllerian), or parasitic when mimics are undefended but still gain protection from their resemblance to the model (Batesian). However, whether chemically defended mimics should be similar in terms of toxicity (i.e. causing damage to the consumer) and/or unpalatability (i.e. distasteful to consumer) is unclear and in many studies remains undifferentiated. In this study, we investigated the evolution of visual signals and chemical defences in a putative mimicry ring of nudibranch molluscs. First, we demonstrated that the appearance of a group of red spotted nudibranchs molluscs was similar from the perspective of potential fish predators using visual modelling and pattern analysis. Second, using phylogenetic reconstruction, we demonstrated that this colour pattern has evolved multiple times in distantly related individuals. Third, we showed that these nudibranchs contained different chemical profiles used for defensive purposes. Finally, we demonstrated that although levels of distastefulness towards Palaemon shrimp remained relatively constant between species, toxicity levels towards brine shrimp varied significantly. We highlight the need to disentangle toxicity and taste when considering chemical defences in aposematic and mimetic species, and discuss the implications for aposematic and mimicry signal evolution.

Pufferfishes of the Family Tetraodontidae are the most speciose group in the Order Tetraodontiformes and mainly inhabit coastal waters along continents. Although no members of other tetraodontiform families have fully discarded their marine lives, approximately 30 tetraodontid species spend their entire lives in freshwaters in disjunct tropical regions of South America, Central Africa, and Southeast Asia. To investigate the interrelationships of tetraodontid pufferfishes and thereby elucidate the evolutionary origins of their freshwater habitats, we performed phylogenetic analysis based on whole mitochondrial genome sequences from 50 tetraodontid species and closely related species (including 31 newly determined sequences). The resulting phylogenies reveal that the family is composed of four major lineages and that freshwater species from the different continents are independently nested in two of the four lineages. A monophyletic origin of the use of freshwater habitats was statistically rejected, and ancestral habitat reconstruction on the resulting tree demonstrates that tetraodontids independently entered freshwater habitats in different continents at least three times. Relaxed molecular-clock Bayesian divergence time estimation suggests that the timing of these invasions differs between continents, occurring at 0-10 million years ago (MA) in South America, 17-38 MA in Central Africa, and 48-78 MA in Southeast Asia. These timings are congruent with geological events that could facilitate adaptation to freshwater habitats in each continent.

Approximately 75% of vertebrate proteins belong to protein families encoded by multiple evolutionarily related genes, a pattern that emerged as a result of gene and genome duplications over the course of vertebrate evolution. In families of genes with similar or related functions, adaptation to a strong selective agent should involve multiple adaptive changes across the entire gene family. However, we know of no evolutionary studies that have explicitly addressed this point. Here, we show how 4 taxonomically diverse species of pufferfishes (Tetraodontidae) each evolved resistance to the guanidinium toxins tetrodotoxin (TTX) and saxitoxin (STX) via parallel amino acid replacements across all 8 sodium channels present in teleost fish genomes. This resulted in diverse suites of coexisting sodium channel types that all confer varying degrees of toxin resistance, yet show remarkable convergence among genes and phylogenetically diverse species. Using site-directed mutagenesis and expression of a vertebrate sodium channel, we also demonstrate that resistance to TTX/STX is enhanced up to 15-fold by single, frequently observed replacements at 2 sites that have not previously been implicated in toxin binding but show similar or identical replacements in pufferfishes and in distantly related vertebrate and nonvertebrate animals. This study presents an example of natural selection acting upon a complete gene family, repeatedly arriving at a diverse but limited number of adaptive changes within the same genome. To be maximally informative, we suggest that future studies of molecular adaptation should consider all functionally similar paralogs of the affected gene family. [PUBLICATION ABSTRACT]

We report that male pufferfishes ( Torquigener sp., Tetraodontidae) constructed large geometric circular structures on the seabed that played an important role in female mate choice. Males dug valleys at various angles in a radial direction, constructing nests surrounded by radially aligned peaks and valleys. Furthermore, they created irregular patterns in the nest comprising fine sand particles. The circular structure not only influences female mate choice but also functions to gather fine sand particles in nests, which are important in female mate choice. Strangely enough, the males never reuse the nest, always constructing a new circular structure at the huge cost of construction. This is because the valleys may not contain sufficient fine sand particles for multiple reproductive cycles.

Animal‐borne cameras, accelerometers and depth loggers have revealed the secret life on the world's largest bony fish the ocean sunfish (Mola mola). Photograph credit: Mike Johnson Nakamura, I., Goto, Y. & Sato, K. (2015) Ocean sunfish rewarm at the surface after deep excursions to forage for siphonophores. Journal of Animal Ecology, 84, 590–603. Logging cameras and accelerometers have opened our eyes to the secret lives of many enigmatic species. Here some of the new opportunities provided by this technology are reviewed. Recent discoveries are highlighted including the observation of selective feeding on energy‐rich parts of prey. As such, biologging cameras provide new opportunities for consideration of selective feeding within the same sort of theoretical framework (marginal value theory/optimal foraging) that exploitation of prey patches has been examined. A recent study with the world's largest bony fish, the ocean sunfish (Mola mola), is highlighted where animal‐borne cameras allowed the ground‐truthing of data sets collected with depth recorders and accelerometers. This synergistic use of a range of biologging approaches will help drive an holistic understanding of the free‐living behaviour of a range of species. Small logging cameras attached to animals can reveal amazing insights into their behaviour including patterns of movements and diet. The new opportunities provided by this technology are highlighted in a recent study in which cameras were attached to the world's largest fish, the ocean sunfish. Footage revealed the mysteries of sunfish feeding on jellyfish in the ocean depths.