Multi-jet propulsion organized by clonal development in a colonial siphonophore

Costello, John H.; Colin, Sean P.; Gemmell, Brad J.; Dabiri, John O.; Sutherland, Kelly R.

doi:10.1038/ncomms9158

Cited by 40 publications

(51 citation statements)

References 22 publications

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“…Directionality and propulsion can also result from the coordination of multiple individuals, as seen for instance in colonial siphonophores. In Nanomia bijuga , clonal medusoid individuals, termed nectophores, propel the colony, and developmental differences between them generate a division of labor that ultimately modulates locomotion (Costello et al, 2015). …”

Section: Cnidarian Muscle Functionsmentioning

confidence: 99%

Diversity of Cnidarian Muscles: Function, Anatomy, Development and Regeneration

Leclère

Röttinger

2017

Front. Cell Dev. Biol.

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The ability to perform muscle contractions is one of the most important and distinctive features of eumetazoans. As the sister group to bilaterians, cnidarians (sea anemones, corals, jellyfish, and hydroids) hold an informative phylogenetic position for understanding muscle evolution. Here, we review current knowledge on muscle function, diversity, development, regeneration and evolution in cnidarians. Cnidarian muscles are involved in various activities, such as feeding, escape, locomotion and defense, in close association with the nervous system. This variety is reflected in the large diversity of muscle organizations found in Cnidaria. Smooth epithelial muscle is thought to be the most common type, and is inferred to be the ancestral muscle type for Cnidaria, while striated muscle fibers and non-epithelial myocytes would have been convergently acquired within Cnidaria. Current knowledge of cnidarian muscle development and its regeneration is limited. While orthologs of myogenic regulatory factors such as MyoD have yet to be found in cnidarian genomes, striated muscle formation potentially involves well-conserved myogenic genes, such as twist and mef2. Although satellite cells have yet to be identified in cnidarians, muscle plasticity (e.g., de- and re-differentiation, fiber repolarization) in a regenerative context and its potential role during regeneration has started to be addressed in a few cnidarian systems. The development of novel tools to study those organisms has created new opportunities to investigate in depth the development and regeneration of cnidarian muscle cells and how they contribute to the regenerative process.

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Section: Cnidarian Muscle Functionsmentioning

confidence: 99%

Diversity of Cnidarian Muscles: Function, Anatomy, Development and Regeneration

Leclère

Röttinger

2017

Front. Cell Dev. Biol.

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“…Thus, the morphological diversity of tentilla has only been characterized for a few taxa, and their evolutionary history remains largely unexplored. Contemporary underwater sampling technology provides an unprecedented opportunity to explore the trophic ecology (Choy et al 2017) and functional morphology (Costello et al 2015) of siphonophores. In addition, well-supported phylogenies based on molecular data are now available for these organisms (Munro et al 2018).…”

Section: Figurementioning

confidence: 99%

Shaped to kill: The evolution of siphonophore tentilla for specialized prey capture in the open ocean

Damian‐Serrano

Haddock

Dunn

2019

Preprint

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15Predator specialization has often been considered an evolutionary 'dead-end' due to the 16 constraints associated with the evolution of morphological and functional optimizations 17 throughout the organism. However, in some predators, these changes are localized in separate 18 structures dedicated to prey capture. One of the most extreme cases of this modularity can 19 be observed in siphonophores, a clade of pelagic colonial cnidarians that use tentilla (tentacle 20 side branches armed with nematocysts) exclusively for prey capture. Here we study how 21 siphonophore specialists and generalists evolve, and what morphological changes are associated 22 with these transitions. To answer these questions, we: (1) measured 29 morphological 23 characters of tentacles from 45 siphonophore species, (2) mapped these data to a phylogenetic 24 tree, and (3) analyzed the evolutionary associations between morphological characters and prey 25 type data from the literature. Instead of a dead-end, we found that siphonophore specialists 26 can evolve into generalists, and that specialists on one prey type have directly evolved into 27 specialists on other prey types. Our results show that siphonophore tentillum morphology has 28 strong evolutionary associations with prey type, and suggest that shifts between prey types 29 are linked to shifts in the morphology, mode of evolution, and genetic correlations of tentilla 30 and their nematocysts. The evolutionary history of siphonophore specialization helps build 31 a broader perspective on predatory niche diversification via morphological innovation and 32 evolution. These findings contribute to understanding how specialization and morphological 33 evolution have shaped present-day food webs. 34 Significance Statement 35Predatory specialization is often associated with the evolution of modifications in the mor-36 phology of the prey capture apparatus. Specialization has been considered an evolutionary 37 'dead-end' due to the constraints associated with these morphological changes. However, 38 in predators like siphonophores, armed with modular structures used exclusively for prey 39 capture, this assumption is challenged. Our results show that siphonophores can evolve 40 2 generalism and new prey-type specializations by modifying the morphological states, modes of 41 evolution, and genetic correlations between the parts of their prey capture apparatus. These 42 findings demonstrate how studying open-ocean non-bilaterian predators can reveal novel 43 patterns and mechanisms in the evolution of specialization. Understanding these evolutionary 44 processes is fundamental to the study of food-web structure and complexity. 45 Introduction 46Most animal predators use specific structures to capture and subdue prey. Raptors have 47 claws and beaks, snakes have fangs, wasps have stingers, and cnidarians have nematocyst-48 laden tentacles. The functional morphology of these structures is critical to their ability 49 to successfully capture prey (1). Long-term adaptive evolution in response t...

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“…The physonect siphonophore Nanomia bijuga is a colonial cnidarian capable of long distance migrations (Robison et al, 1998) as well as short sprints and maneuvering (Costello et al, 2015). As in other physonect siphonophores, multiple swimming units, called nectophores, are organized linearly along a central nectosome (Fig.…”

Section: Introductionmentioning

confidence: 99%

“…1). The nectophores produce pulsed, high speed jets and in N. bijuga the nectophores are coordinated to produce forward swimming, reverse swimming and turning (Mackie, 1964; Costello et al, 2015). The coordination of multiple jets makes N. bijuga a highly effective swimmer that performs extensive diel vertical migrations, travelling 100s of m to the surface each night and then returning to depth during the day (Robison et al, 1998).…”

Section: Introductionmentioning

confidence: 99%

“…Up to this point, studies of swimming in N. bijuga have primarily focused on colony-level coordination between the nectophores, which play different roles during turning and straight swimming depending on their development and position along the nectosome (Costello et al, 2015). Newly budded nectophores toward the colony apex (Dunn and Wagner, 2006) are used for turning the colony.…”

Section: Introductionmentioning

confidence: 99%

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Propulsive design principles in a multi-jet siphonophore

Sutherland

Colin

Costello

et al. 2018

Preprint

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14Coordination of multiple propulsors can provide performance benefits in swimming organisms. 15 Siphonophores are marine colonial organisms that orchestrate the motion of multiple swimming 16 zooids for effective swimming. However, the kinematics at the level of individual swimming 17 zooids (nectophores) have not been examined in detail. We used high speed, high resolution 18 microvideography and particle image velocimetry (PIV) of the physonect siphonophore, 19 Nanomia bijuga, to study the motion of the nectophores and the associated fluid motion during 20 jetting and refilling. The integration of nectophore and velum kinematics allow for a high-speed 21 (maximum ~1 m s -1 ), narrow (1-2 mm) jet and rapid refill as well as a 1:1 ratio of jetting to refill 22 time. Overall swimming performance is enhanced by velocity gradients produced in the 23 nectophore during refill, which lead to a high pressure region that produces forward thrust. 24 Generating thrust during both the jet and refill phases augments the distance travelled by 17% 25 over theoretical animals, which generate thrust only during the jet phase. The details of velum 26 kinematics and associated fluid mechanics elucidate how siphonophores effectively navigate 27 three-dimensional space and could be applied to exit flow parameters in multijet underwater 28 vehicles. 29 30 Summary statement: Colonial siphonophores produce high speed jets and generate forward 31 thrust during refill using a flexible velum to achieve effective propulsion.32 33 34 35The physonect siphonophore Nanomia bijuga is a colonial cnidarian capable of long distance 36 migrations (Robison et al., 1998) as well as short sprints and maneuvering (Costello et al., 2015). 37 As in other physonect siphonophores, multiple swimming units, called nectophores, are 38 organized linearly along a central nectosome (Fig. 1). The nectophores produce pulsed, high 39 speed jets and in N. bijuga the nectophores are coordinated to produce forward swimming, 40 reverse swimming and turning (Mackie, 1964; Costello et al., 2015). The coordination of 41 multiple jets makes N. bijuga a highly effective swimmer that performs extensive diel vertical 42 migrations, travelling 100s of m to the surface each night and then returning to depth during the 43 day (Robison et al., 1998). Due to this pronounced migration behavior, its cosmopolitan 44 distribution (Totton 1965), and the acoustic scattering properties of the gas-filled pneumatophore 45 at the colony tip, N. bijuga is a prominent member of the sound scattering layer in much of the 46 world's oceans (Barham, 1963). 47 Up to this point, studies of swimming in N. bijuga have primarily focused on colony-level 48 coordination between the nectophores, which play different roles during turning and straight 49 swimming depending on their development and position along the nectosome (Costello et al., 50 2015). Newly budded nectophores toward the colony apex (Dunn and Wagner, 2006) are used 51for turning the colony. To achieve this, these nectopho...

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Multi-jet propulsion organized by clonal development in a colonial siphonophore

Cited by 40 publications

References 22 publications

Diversity of Cnidarian Muscles: Function, Anatomy, Development and Regeneration

Diversity of Cnidarian Muscles: Function, Anatomy, Development and Regeneration

Shaped to kill: The evolution of siphonophore tentilla for specialized prey capture in the open ocean

Propulsive design principles in a multi-jet siphonophore

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