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The Evolution of Siphonophore Tentilla for Specialized Prey Capture in the Open Ocean

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The Evolution of Siphonophore Tentilla for Specialized Prey Capture in the Open Ocean The evolution of siphonophore tentilla for specialized prey capture in the open ocean Alejandro Damian-Serranoa,1, Steven H. D. Haddockb,c, and Casey W. Dunna aDepartment of Ecology and Evolutionary Biology, Yale University, New Haven, CT 06520; bResearch Division, Monterey Bay Aquarium Research Institute, Moss Landing, CA 95039; and cEcology and Evolutionary Biology, University of California, Santa Cruz, CA 95064 Edited by Jeremy B. C. Jackson, American Museum of Natural History, New York, NY, and approved December 11, 2020 (received for review April 7, 2020) Predator specialization has often been considered an evolutionary makes them an ideal system to study the relationships between “dead end” due to the constraints associated with the evolution of functional traits and prey specialization. Like a head of coral, a si- morphological and functional optimizations throughout the organ- phonophore is a colony bearing many feeding polyps (Fig. 1). Each ism. However, in some predators, these changes are localized in sep- feeding polyp has a single tentacle, which branches into a series of arate structures dedicated to prey capture. One of the most extreme tentilla. Like other cnidarians, siphonophores capture prey with cases of this modularity can be observed in siphonophores, a clade of nematocysts, harpoon-like stinging capsules borne within special- pelagic colonial cnidarians that use tentilla (tentacle side branches ized cells known as cnidocytes. Unlike the prey-capture apparatus of armed with nematocysts) exclusively for prey capture. Here we study most other cnidarians, siphonophore tentacles carry their cnidocytes how siphonophore specialists and generalists evolve, and what mor- in extremely complex and organized batteries (3), which are located phological changes are associated with these transitions. To answer in their tentilla. While nematocyst batteries and clusters in other these questions, we: a) Measured 29 morphological characters of cnidarians are simple static scaffolds for cnidocytes, siphonophore tentacles from 45 siphonophore species, b) mapped these data to a tentilla have their own reaction mechanism, triggered upon en- phylogenetic tree, and c) analyzed the evolutionary associations be- counter with prey. When it fires, a tentillum undergoes an ex- tween morphological characters and prey-type data from the litera- tremely fast conformational change that wraps it around the prey, ture. Instead of a dead end, we found that siphonophore specialists maximizing the surface area of contact for nematocysts to fire on can evolve into generalists, and that specialists on one prey type the prey (4). In addition, some species have elaborate fluorescent have directly evolved into specialists on other prey types. Our results or bioluminescent lures on their tentilla to attract prey with EVOLUTION show that siphonophore tentillum morphology has strong evolution- aggressive mimicry (5–7). ary associations with prey type, and suggest that shifts between Siphonophores bear four major nematocyst types in their ten- prey types are linked to shifts in the morphology, mode of evolution, tacles and tentilla (Fig. 1F). The largest type, heteronemes, have and evolutionary correlations of tentilla and their nematocysts. The open-tip tubules characterized by bearing a distinctly wider spiny evolutionary history of siphonophore specialization helps build a shaft at the proximal end of the everted tubule. These are typically broader perspective on predatory niche diversification via morpho- found flanking the proximal end of the cnidoband (nematocyst logical innovation and evolution. These findings contribute to under- standing how specialization and morphological evolution have shaped present-day food webs. Significance siphonophores | nematocysts | predation | specialization | Predatory specialization is often associated with the evolution character evolution of modifications in the morphology of the prey-capture appa- ratus. Specialization has been considered an evolutionary “ ” ost animal predators use specific structures to capture and dead end due to the constraints associated with these mor- Msubdue prey. Raptors have claws and beaks, snakes have phological changes. However, in predators like siphonophores, fangs, wasps have stingers, and cnidarians have nematocyst-laden armed with modular structures used exclusively for prey cap- tentacles. The functional morphology of these structures is crit- ture, this assumption is challenged. Our results show that si- ical to their ability to successfully capture prey (1). Long-term phonophores can evolve generalism and new prey-type adaptive evolution in response to the defense mechanisms of the specializations by modifying the morphological states, modes of evolution, and evolutionary correlations between the parts prey (e.g., avoidance, escape, protective barriers) leads to mod- of their prey-capture apparatus. These findings demonstrate ifications that can counter those defenses. The more specialized how studying open-ocean nonbilaterian predators can reveal the diet of a predator is, the more specialized its structures need to novel patterns and mechanisms in the evolution of specializa- be to efficiently overcome the challenges posed by the prey. tion. Understanding these evolutionary processes is funda- Characterizing the relationships between morphology and preda- mental to the study of food web structure and complexity. tory specialization is necessary to understand how the phenotypic diversity of predators determines food web structure. However, for Author contributions: A.D.-S., S.H.D.H, and C.W.D. designed research; A.D.-S. performed many clades of predators, there is scarce knowledge on how these research; A.D.-S. analyzed data; S.H.D.H. contributed by facilitating the access to the field specializations evolved. The primary questions we set out to an- and collection tools, and directing the remotely operated vehicles and blue-water diving swer are: How do predator specialists and generalists evolve, and operations in the field; S.H.D.H. edited the paper, collected specimens, and contributed extensive knowledge of the biology and ecology of the organisms; C.W.D. contributed by how does predatory specialization shape morphological evolution? collecting specimens, editing the paper, and providing mentoring; and A.D.-S. wrote Siphonophores (Cnidaria: Hydrozoa) are a clade of gelatinous, the paper. colonial organisms that swim in the open ocean, feeding on a wide The authors declare no competing interest. diversity of prey (often fish, crustaceans, and jellyfish). Siphono- This article is a PNAS Direct Submission. phorecolonieshaveamodularbodyplanwithdifferentzooids This open access article is distributed under Creative Commons Attribution-NonCommercial- specialized for different tasks. This modularity extends also within NoDerivatives License 4.0 (CC BY-NC-ND). the feeding gastrozooids, which carry modular structures on the 1To whom correspondence may be addressed. Email: [email protected]. tentacle that are exclusively used for prey capture: The tentilla This article contains supporting information online at https://www.pnas.org/lookup/suppl/ (Fig. 1). The tentilla have great morphological variation across doi:10.1073/pnas.2005063118/-/DCSupplemental. species (2). Together with their well-understood function, this Published February 15, 2021. PNAS 2021 Vol. 118 No. 8 e2005063118 https://doi.org/10.1073/pnas.2005063118 | 1of9 Downloaded by guest on September 26, 2021 A B C D E Float Tentilla (budding) Peduncle Swimming bells Gastrozooid Mouth Gastrozooid and tentacle Tentacle Pedicle Involucrum Tentilla Cnidoband (mature) 1.0 cm Elastic strands F Terminal filament Cnidoband nematocysts Terminal filament nematocysts Heteronemes Haplonemes Spironemes Rhopalonemes Mastigophores Stenoteles Euryteles Birhopaloids Isorhizas Anisorhizas Desmonemes Anacrophores Acrophores Tubule Tubule Shaft + spines 50µm 20µm 20µm 20µm 20µm 50µm 20µm 50µm 20µm 20µm Fig. 1. Siphonophore anatomy. (A) Nanomia sp. siphonophore colony (photo by Catriona Munro). (B and C) Illustration of a Nanomia colony, gastrozooid, and tentacle close-up (by Freya Goetz). (D) Nanomia sp. Tentillum illustration and main parts. (E) Differential interference contrast micrograph of the ten- tillum illustrated in D.(F) Nematocyst types [illustration reproduced with permission from Mapstone (2)], hypothesized homologies, and locations in the tentillum. Undischarged to the left, discharged to the right. battery). The most abundant type, haplonemes, have no distinct specialization can be considered a dead end if lineages that are shaft, but similarly to heteronemes, their tubules have open tips feeding specialists do not give rise to feeding generalists or spe- and can be found in the cnidoband. Both heteronemes and hap- cialists on other prey. However, recent studies have found that lonemes bear short spines along the tubule. Both can be toxic and ecological mechanisms, such as interspecific competition, can fa- penetrate the surface of some prey types. In the terminal filament, vor the evolution of generalists from specialists (17–19) and spe- siphonophores bear two other types of nematocysts, characterized cialist resource switching (20, 21). In addition to studying by their adhesive function, closed tip tubules and lack of spines on relationships with morphology, we seek to identify what evolutionary the tubule. These are the desmonemes (a type of adhesive coiled- transitions in trophic niche breadth
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