The Evolutionary History of Siphonophore Tentilla: Novelties, Convergence, and Integration

Abstract

Siphonophores are free-living predatory colonial hydrozoan cnidarians found in every region of the ocean. Siphonophore tentilla (tentacle side branches) are unique biological structures for prey capture, composed of a complex arrangement of cnidocytes (stinging cells) bearing different types of nematocysts (stinging capsules) and auxiliary structures. Tentilla present an extensive morphological and functional diversity across species. While associations between tentillum form and diet have been reported, the evolutionary history giving rise to this morphological diversity is largely unexplored. Here we examine the evolutionary gains and losses of novel tentillum substructures and nematocyst types on the most recent siphonophore phylogeny. Tentilla have a precisely coordinated high-speed strike mechanism of synchronous unwinding and nematocyst discharge. Here we characterize the kinematic diversity of this prey capture reaction using high-speed video and find relationships with morphological characters. Since tentillum discharge occurs in synchrony across a broad morphological diversity, we evaluate how phenotypic integration is maintaining character correlations across evolutionary time. We found that the tentillum morphospace has low dimensionality, identified instances of heterochrony and morphological convergence, and generated hypotheses on the diets of understudied siphonophore species. Our findings indicate that siphonophore tentilla are phenotypically integrated structures with a complex evolutionary history leading to a phylogenetically-structured diversity of forms which are predictive of kinematic performance and feeding habits.

Integrating siphonophores into marine food‐web ecology

“…These adaptations are used to attract different taxa and demonstrate the specialization for siphonophores feeding in midwater communities. Recent work (Damian-Serrano et al 2021a,2021b hypothesized that tentillum morphology may be a useful predictor for siphonophore diets, particularly to distinguish between generalist and specialist species. For example, siphonophores that specialize on copepods have convergently evolved smaller tentilla with fewer and smaller nematocysts (e.g., Hippopodius hippopus, Diphyes dispar, Chelophyes appendiculata, Sulculeolaria quadrivalis) compared to species that prey on other taxa.…”

“…Gastrozooids have a single, long tentacle with side branches (tentilla), which are used to capture and subdue prey (Mapstone 2014). Tentilla morphology is highly diverse across species (Damian-Serrano et al 2021b). Since tentilla are exclusively used for feeding, morphological variations may reflect niche partitioning and interspecific diet specialization (Damian-Serrano et al 2021a).…”

Characterizing the secret diets of siphonophores (Cnidaria: Hydrozoa) using DNA metabarcoding

“…Prey sources were annotated when plausible prey taxa were assigned. We know that siphonophores can only capture prey that actively swims to trigger tentilla discharge [9,27]. Therefore, we interpreted that DNA from non-pelagic and/or non-motile organisms cannot be sourced from dietary contributions from microorganisms, marine snow, eggs, or microscopic ciliated larvae.…”

“…Siphonophore tentillum and nematocyst morphologies are directly linked to feeding guild. Damian-Serrano et al [26,27] used these relationships to generate feeding guild predictions for 45 siphonophore species using their tentillum and nematocyst morphologies as predictors in a discriminant analysis of principal components (DAPC). These feeding guild categories comprise fish specialists (which feed primarily on teleost fish prey), large crustacean specialists (which feed primarily on krill, decapod shrimps, mysids, lophogastrids, amphipods, and other macro-planktonic crustaceans larger than 1cm), small crustacean specialists (which feed primarily on copepods, ostracods, cladocerans, larvae, and other meso-planktonic crustaceans smaller than 1cm), gelatinous specialists (which are able to feed on large gelatinous animals such as salps, ctenophores, or medusae in addition to other zooplankton), and generalists (which feed on a balanced variety of small and large, soft-and hard-bodied prey not including gelatinous animals).…”

“…These feeding guild categories comprise fish specialists (which feed primarily on teleost fish prey), large crustacean specialists (which feed primarily on krill, decapod shrimps, mysids, lophogastrids, amphipods, and other macro-planktonic crustaceans larger than 1cm), small crustacean specialists (which feed primarily on copepods, ostracods, cladocerans, larvae, and other meso-planktonic crustaceans smaller than 1cm), gelatinous specialists (which are able to feed on large gelatinous animals such as salps, ctenophores, or medusae in addition to other zooplankton), and generalists (which feed on a balanced variety of small and large, soft-and hard-bodied prey not including gelatinous animals). These predictions were cast on siphonophore species for which no dietary information was available [27], and thus remained to be tested with new data on siphonophore diets.…”