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

Abstract

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...

The evolution of siphonophore tentilla for specialized prey capture in the open ocean

“…( Right ) Grid showing the prey items consumed from which the feeding guild categories were derived. Diet data were obtained from the literature review, available in the Dryad repository ( 42 ).…”

“…The morphological work was carried out on siphonophore specimens fixed in 4% formalin from the Yale Peabody Museum Invertebrate Zoology (YPM-IZ) collection [accession numbers in Dryad repository ( 42 )]. These specimens were collected intact across many years of fieldwork expeditions, using blue-water diving ( 43 ), ROVs, plankton net trawls, and human-operated submersibles.…”

“…We did not measure the lengths of contractile structures (terminal filaments, pedicles, gastrozooids, and tentacles) since they are too variable to quantify. We measured at least one specimen for 96 different species [raw data available in Dryad repository ( 42 )]. Of these, we selected 38 focal species across clades based on specimen availability and phylogenetic representation.…”

“…The phylogenetic analysis included 55 siphonophore species and 6 outgroup cnidarian species ( Clytia hemisphaerica , Hydra circumcincta , Ectopleura dumortieri , Porpita porpita , Velella velella , Staurocladia wellingtoni ). The gene sequences we used in this study are available online [accession numbers in Dryad repository ( 42 )]. Some of the sequences we used were accessioned in Dunn et al ( 27 ), and others we extracted from the transcriptomes in Munro et al ( 24 ).…”

Characterising Functional Venom Profiles of Anthozoans and Medusozoans within Their Ecological Context

“…This transition is accompanied by an increase in mastigophores (large-volume nematocysts) and an increased diversity of toxin peptides, which together produce a potent venom specialised for targeting fish [58,59]. Similarly, the number and volume of heteroneme nematocysts, including mastigophores, were found to increase in siphonophore tentilla with a diet of fish compared to those with a diet of copepods [60]. The venom from cubozoan species that consistently prey upon shrimp is also capable of eliciting death in fish, but the amount of venom required exceeds the surface area of both nematocyst-laden tentacles and their prey, making it impractical for them to subdue fish [58].…”