Characterizing the Bioluminescence of the Humboldt Squid, <i>Dosidicus gigas</i> (d'Orbigny, 1835): One of the Largest Luminescent Animals in the World

Galeazzo, Gabriela A.; Mirza, Jeremy; Pinto, Ernani; Stevani, Cassius V.; Lohrmann, Karin B.; Oliveira, Adriana Gonçalves

doi:10.1111/php.13106

Cited by 8 publications

(7 citation statements)

References 27 publications

(44 reference statements)

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“…Secreted bioluminescence, which is used for mating and defence, is discharged from light organs such as modified mouths, photophores, and appendages (Angel, 1968; Nicol, 1969; Barnes & Case, 1972; Abe et al ., 2000; Robison et al ., 2003; Wong et al ., 2015). Alternatively, internal extracellular and intracellular bioluminescence, which is used for counterillumination, prey capture, mating, and communication, is produced in light spots associated with the epithelium, light organs connected to the digestive tract, luminous lanterns, or structurally complex photophores (Peterson & Buck, 1968; Arnold & Young, 1974; Baguet, 1975; Haddock & Case, 1999; Thacker & Roje, 2009; Galeazzo et al ., 2019).…”

Section: Bioluminescence: An Excellent System For Studying Convergencmentioning

confidence: 99%

“…Photoproteins using coelenterazine as a substrate can also vary in terms of the cofactors required to produce bioluminescence. For example, cnidarians, ctenophores, and radiolarians use the divalent cation Ca 2+ as a photoprotein cofactor, but the squids Dosidicus gigas and Sthenoteuthis oualaniensis use a monovalent cation cofactor such as Na + or K + (Shimomura, 1985; Takahashi & Isobe, 1994; Tsuji et al ., 1995; Galeazzo et al ., 2019). This biochemical variability in bioluminescence reveals that there are numerous biological approaches to harnessing coelenterazine‐based bioluminescence.…”

Section: Reviewing the Multi‐level Convergent Evolution Of Bioluminesmentioning

confidence: 99%

“…Alternatively, internal extracellular and intracellular bioluminescence, which is used for counterillumination, prey capture, mating, and communication, is produced in light spots associated with the epithelium, light organs connected to the digestive tract, luminous lanterns, or structurally complex photophores (Peterson & Buck, 1968;Arnold & Young, 1974;Baguet, 1975;Haddock & Case, 1999;Thacker & Roje, 2009;Galeazzo et al, 2019).…”

Section: Bioluminescence: An Excellent System For Studying Convermentioning

confidence: 99%

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Multi‐level convergence of complex traits and the evolution of bioluminescence

Lau

Oakley

2020

Biological Reviews

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Evolutionary convergence provides natural opportunities to investigate how, when, and why novel traits evolve. Many convergent traits are complex, highlighting the importance of explicitly considering convergence at different levels of biological organization, or ‘multi‐level convergent evolution’. To investigate multi‐level convergent evolution, we propose a holistic and hierarchical framework that emphasizes breaking down traits into several functional modules. We begin by identifying long‐standing questions on the origins of complexity and the diverse evolutionary processes underlying phenotypic convergence to discuss how they can be addressed by examining convergent systems. We argue that bioluminescence, a complex trait that evolved dozens of times through either novel mechanisms or conserved toolkits, is particularly well suited for these studies. We present an updated estimate of at least 94 independent origins of bioluminescence across the tree of life, which we calculated by reviewing and summarizing all estimates of independent origins. Then, we use our framework to review the biology, chemistry, and evolution of bioluminescence, and for each biological level identify questions that arise from our systematic review. We focus on luminous organisms that use the shared luciferin substrates coelenterazine or vargulin to produce light because these organisms convergently evolved bioluminescent proteins that use the same luciferins to produce bioluminescence. Evolutionary convergence does not necessarily extend across biological levels, as exemplified by cases of conservation and disparity in biological functions, organs, cells, and molecules associated with bioluminescence systems. Investigating differences across bioluminescent organisms will address fundamental questions on predictability and contingency in convergent evolution. Lastly, we highlight unexplored areas of bioluminescence research and advances in sequencing and chemical techniques useful for developing bioluminescence as a model system for studying multi‐level convergent evolution.

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Section: Bioluminescence: An Excellent System For Studying Convergencmentioning

confidence: 99%

Section: Reviewing the Multi‐level Convergent Evolution Of Bioluminesmentioning

confidence: 99%

Section: Bioluminescence: An Excellent System For Studying Convermentioning

confidence: 99%

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Multi‐level convergence of complex traits and the evolution of bioluminescence

Lau

Oakley

2020

Biological Reviews

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“…These authors suggested that symplectins may have multiple functions including hydrolase activity (Francis et al, 2017). Both dehydrocoelenterazine and symplectin-like photoprotein were recently demonstrated to be responsible for the light emission of the Humboldt squid, Dosidicus gigas, one of the largest cephalopods on Earth (Francis et al, 2017;Galeazzo et al, 2019).…”

Section: Sthenoteuthis-type Photoproteins or Symplectin (Group Vii)mentioning

confidence: 99%

Leaving the Dark Side? Insights Into the Evolution of Luciferases

et al. 2021

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Bioluminescence—i.e., the emission of visible light by living organisms—is defined as a biochemical reaction involving, at least, a luciferin substrate, an oxygen derivative, and a specialised luciferase enzyme. In some cases, the enzyme and the substrate are durably associated and form a photoprotein. While this terminology is educatively useful to explain bioluminescence, it gives a false idea that all luminous organisms are using identical or homologous molecular tools to achieve light emission. As usually observed in biology, reality is more complex. To date, at least 11 different luciferins have indeed been discovered, and several non-homologous luciferases lato sensu have been identified which, all together, confirms that bioluminescence emerged independently multiple times during the evolution of living organisms. While some phylogenetically related organisms may use non-homologous luciferases (e.g., at least four convergent luciferases are found in Pancrustacea), it has also been observed that phylogenetically distant organisms may use homologous luciferases (e.g., parallel evolution observed in some cnidarians, tunicates and echinoderms that are sharing a homologous luciferase-based system). The evolution of luciferases then appears puzzling. The present review takes stock of the diversity of known “bioluminescent proteins,” their evolution and potential evolutionary origins. A total of 134 luciferase and photoprotein sequences have been investigated (from 75 species and 11 phyla), and our analyses identified 12 distinct types—defined as a group of homologous bioluminescent proteins. The literature review indicated that genes coding for luciferases and photoproteins have potentially emerged as new genes or have been co-opted from ancestral non-luciferase/photoprotein genes. In this latter case, the homologous gene’s co-options may occur independently in phylogenetically distant organisms.

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“…Numerous (a single D. gigas may have hundreds) small subcutaneous (s.c.) photophores that consist of relatively rudimentary aggregations of photogenic tissue are embedded throughout the muscle tissue ( Fig. 3 A-C) and cause the entire animal to glow (45)(46)(47)(48)(49). Pigmentation patterns are generated by the overlying chromatophore layer, which is cutaneous.…”

Section: Bioluminescent Backlighting and The Illumination Of Chromaticmentioning

confidence: 99%

Bioluminescent backlighting illuminates the complex visual signals of a social squid in the deep sea

Burford

Robison

2020

Proc. Natl. Acad. Sci. U.S.A.

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Visual signals rapidly relay information, facilitating behaviors and ecological interactions that shape ecosystems. However, most known signaling systems can be restricted by low light levels—a pervasive condition in the deep ocean, the largest inhabitable space on the planet. Resident visually cued animals have therefore been hypothesized to have simple signals with limited information-carrying capacity. We used cameras mounted on remotely operated vehicles to study the behavior of the Humboldt squid, Dosidicus gigas, in its natural deep-sea habitat. We show that specific pigmentation patterns from its diverse repertoire are selectively displayed during foraging and in social scenarios, and we investigate how these behaviors may be used syntactically for communication. We additionally identify the probable mechanism by which D. gigas, and related squids, illuminate these patterns to create visual signals that can be readily perceived in the deep, dark ocean. Numerous small subcutaneous (s.c.) photophores (bioluminescent organs) embedded throughout the muscle tissue make the entire body glow, thereby backlighting the pigmentation patterns. Equipped with a mechanism by which complex information can be rapidly relayed through a visual pathway under low-light conditions, our data suggest that the visual signals displayed by D. gigas could share design features with advanced forms of animal communication. Visual signaling by deep-living cephalopods will likely be critical in understanding how, and how much, information can be shared in one of the planet’s most challenging environments for visual communication.

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Characterizing the Bioluminescence of the Humboldt Squid, Dosidicus gigas (d'Orbigny, 1835): One of the Largest Luminescent Animals in the World

Cited by 8 publications

References 27 publications

Multi‐level convergence of complex traits and the evolution of bioluminescence

Multi‐level convergence of complex traits and the evolution of bioluminescence

Leaving the Dark Side? Insights Into the Evolution of Luciferases

Bioluminescent backlighting illuminates the complex visual signals of a social squid in the deep sea

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