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

View ORCID ProfileAlejandro Damian-Serrano, View ORCID ProfileSteven H.D. Haddock, View ORCID ProfileCasey W. Dunn
doi: https://doi.org/10.1101/653345
Alejandro Damian-Serrano
1Yale University, Department of Ecology and Evolutionary Biology, 165 Prospect St., New Haven, CT 06520, USA
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  • For correspondence: alejandro.damianserrano@yale.edu
Steven H.D. Haddock
2Monterey Bay Aquarium Research Institute, 7700 Sandholdt Rd., Moss Landing, CA 95039, USA
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Casey W. Dunn
1Yale University, Department of Ecology and Evolutionary Biology, 165 Prospect St., New Haven, CT 06520, USA
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Abstract

Predator specialization has often been considered an evolutionary ‘dead-end’ due to the constraints associated with the evolution of morphological and functional optimizations throughout the organism. However, in some predators, these changes are localized in separate structures dedicated to prey capture. One of the most extreme cases of this modularity can be observed in siphonophores, a clade of pelagic colonial cnidarians that use tentilla (tentacle side branches armed with nematocysts) exclusively for prey capture. Here we study how siphonophore specialists and generalists evolve, and what morphological changes are associated with these transitions. To answer these questions, we: (1) measured 29 morphological characters of tentacles from 45 siphonophore species, (2) mapped these data to a phylogenetic tree, and (3) analyzed the evolutionary associations between morphological characters and prey type data from the literature. Instead of a dead-end, we found that siphonophore specialists can evolve into generalists, and that specialists on one prey type have directly evolved into specialists on other prey types. Our results show that siphonophore tentillum morphology has strong evolutionary associations with prey type, and suggest that shifts between prey types are linked to shifts in the morphology, mode of evolution, and genetic correlations of tentilla and their nematocysts. The evolutionary history of siphonophore specialization helps build a broader perspective on predatory niche diversification via morphological innovation and evolution. These findings contribute to understanding how specialization and morphological evolution have shaped present-day food webs.

Significance Statement Predatory specialization is often associated with the evolution of modifications in the morphology of the prey capture apparatus. Specialization has been considered an evolutionary ‘dead-end’ due to the constraints associated with these morphological changes. However, in predators like siphonophores, armed with modular structures used exclusively for prey capture, this assumption is challenged. Our results show that siphonophores can evolve generalism and new prey-type specializations by modifying the morphological states, modes of evolution, and genetic correlations between the parts of their prey capture apparatus. These findings demonstrate how studying open-ocean non-bilaterian predators can reveal novel patterns and mechanisms in the evolution of specialization. Understanding these evolutionary processes is fundamental to the study of food-web structure and complexity.

Footnotes

  • This manuscript has changed focus to a more focused approach on the evolution of predator specialists and generalists, and the different modes of morphological evolution associated with these transitions. A large amount of organismal-focused content and tangentially relevant results were removed. Supplements were consolidated.

  • https://github.com/dunnlab/tentilla_morph

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted April 02, 2020.
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Shaped to kill: The evolution of siphonophore tentilla for specialized prey capture in the open ocean
Alejandro Damian-Serrano, Steven H.D. Haddock, Casey W. Dunn
bioRxiv 653345; doi: https://doi.org/10.1101/653345
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Shaped to kill: The evolution of siphonophore tentilla for specialized prey capture in the open ocean
Alejandro Damian-Serrano, Steven H.D. Haddock, Casey W. Dunn
bioRxiv 653345; doi: https://doi.org/10.1101/653345

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