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.

Siphonophores are a diverse group of hydrozoans (Cnidaria) that are found at most depths of the ocean - from the surface, like the familiar Portuguese man of war, to the deep sea. They play important roles in ocean ecosystems, and are among the most abundant gelatinous predators. A previous phylogenetic study based on two ribosomal RNA genes provided insight into the internal relationships between major siphonophore groups. There was, however, little support for many deep relationships within the clade Codonophora. Here, we present a new siphonophore phylogeny based on new transcriptome data from 29 siphonophore species analyzed in combination with 14 publicly available genomic and transcriptomic datasets. We use this new phylogeny to reconstruct several traits that are central to siphonophore biology, including sexual system (monoecy vs. dioecy), gain and loss of zooid types, life history traits, and habitat. The phylogenetic relationships in this study are largely consistent with the previous phylogeny, but we find strong support for new clades within Codonophora that were previously unresolved. These results have important implications for trait evolution within Siphonophora, including favoring the hypothesis that monoecy arose at least twice.

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.

Recent work challenges the paradigm that gelatinous animals are trophic dead ends and demonstrates their central roles as predators and prey in marine food webs. However, that research is primarily focused on scyphozoan "true jellies." We review the ecological niches of siphonophores, gelatinous cnidarians that are understudied but abundant across the water column. We discuss methodological advances that facilitate studying the diets of gelatinous animals and consider avenues for future research. Our results illustrate that siphonophores occupy numerous trophic niches. There are diet differences between siphonophore suborders and species, and our results suggest that specialization may be more predominant within deep, compared to shallow habitats. Synthesizing siphonophore predator-prey interactions highlights the diverse energy flow pathways through gelatinous components of marine food webs.

Acorn barnacle adults experience environmental heterogeneity at various spatial scales of their circumboreal habitat, raising the question of how adaptation to high environmental variability is maintained in the face of strong juvenile dispersal and mortality. Here we show that 4% of genes in the barnacle genome experience balancing selection across the entire range of the species. Many of these genes harbor mutations maintained across 2 million years of evolution between the Pacific and Atlantic oceans. These genes are involved in ion regulation, pain reception, and heat tolerance, functions which are essential in highly variable ecosystems. The data also reveal complex population structure within and between basins, driven by the trans-Arctic interchange and the last glaciation. Divergence between Atlantic and Pacific populations is high, foreshadowing the onset of allopatric speciation, and suggesting that balancing selection is strong enough to maintain functional variation for millions of years in the face of complex demography.

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The northern acorn barnacle (Semibalanus balanoides) is a robust system to study the genetic basis of adaptations to highly heterogeneous environments. Adult barnacles may be exposed to highly dissimilar levels of thermal stress depending on where they settle in the intertidal (i.e., closer to the upper or lower tidal boundary). For instance, barnacles near the upper tidal limit experience episodic summer temperatures above recorded heat coma levels. This differential stress at the microhabitat level is also dependent on the aspect of sun exposure. In the present study, we used pool-seq approaches to conduct a genome wide screen for loci responding to intertidal zonation across the North Atlantic basin (Maine, Rhode Island, and Norway). Our analysis discovered 382 genomic regions containing SNPs which are consistently zonated (i.e., SNPs whose frequencies vary depending on their position in the rocky intertidal) across all surveyed habitats. Notably, most zonated SNPs are young and private to the North Atlantic. These regions show high levels of genetic differentiation across ecologically extreme microhabitats concomitant with elevated levels of genetic variation and Tajima's D, suggesting the action of non-neutral processes. Overall, these findings support the hypothesis that spatially heterogeneous selection is a general and repeatable feature for this species, and that natural selection can maintain functional genetic variation in heterogeneous environments.

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...