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. 2021 Feb 23;118(8):e2005063118.
doi: 10.1073/pnas.2005063118.

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

Alejandro Damian-Serrano  1 , Steven H D Haddock  2   3 , Casey W Dunn  4
Affiliations

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

Alejandro Damian-Serrano et al. Proc Natl Acad Sci U S A. .

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: a) Measured 29 morphological characters of tentacles from 45 siphonophore species, b) mapped these data to a phylogenetic tree, and c) 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 evolutionary 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.

Keywords: character evolution; nematocysts; predation; siphonophores; specialization.

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Conflict of interest statement

The authors declare no competing interest.

Figures

Fig. 1.
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 tentillum 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.
Fig. 2.
Fig. 2.
Bayesian time-tree inferred from 18S + 16S concatenated sequences and constrained to be congruent with a published transcriptome phylogeny. Branch lengths were estimated using a relaxed molecular clock. Species names in red indicate replicated representation in the morphology data. All data were publicly available, apart from new sequences produced for Thermopalia taraxaca and F. vityazi (bold). Nodes labeled with Bayesian posteriors (BP). Green circles indicate BP = 1. Blue circles indicate nodes constrained to be congruent with Munro et al. (24). Tips with black squares indicate the species with transcriptomes used in Munro et al. (24). Tips with purple squares indicate genus-level correspondence to taxa included in Munro et al. (24). The main clades are labeled with black bars for described taxonomic units, and gray bars for operational phylogenetic designations.
Fig. 3.
Fig. 3.
(Left) Subset phylogeny showing the mapped feeding guild regimes that were used to inform the OUwie analyses. (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).
See this image and copyright information in PMC

References

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