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

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.

Ecological Load and Balancing Selection in Circumboreal Barnacles.

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 My 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.

From tides to nucleotides: Genomic signatures of adaptation to environmental heterogeneity in barnacles.

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.

Improved phylogenetic resolution within Siphonophora (Cnidaria) with implications for trait evolution.

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.

Spinning and corkscrewing of oceanic macroplankton revealed through in situ imaging.

Helical motion is prevalent in nature and has been shown to confer stability and efficiency in microorganisms. However, the mechanics of helical locomotion in larger organisms (>1 centimeter) remain unknown. In the open ocean, we observed the chain forming salp, Iasis cylindrica, swimming in helices. Three-dimensional imaging showed that helicity derives from torque production by zooids oriented at an oblique orientation relative to the chain axis. Colonies can spin both clockwise and counterclockwise and longer chains (>10 zooids) transition from spinning around a linear axis to a helical swimming path. Propulsive jets are non-interacting and directed at a small angle relative to the axis of motion, thus maximizing thrust while minimizing destructive interactions. Our integrated approach reveals the biomechanical advantages of distributed propulsion and macroscale helical movement.

A Developmental Ontology for the Colonial Architecture of Salps.

AbstractColonial animals are composed of clonal individuals that remain physically connected and physiologically integrated. Salps are tunicates with a dual life cycle, including an asexual solitary stage that buds sexual colonies composed of jet-propelling zooids that efficiently swim together as a single unit by multijet propulsion. Colonies from different species develop distinct architectures characterized by their zooid arrangement patterns, but this diversity has received little attention. Thus, these architectures have never been formally defined using a framework of variables and axes that would allow comparative analyses. We set out to define an ontology of the salp colony architecture morphospace and describe the developmental pathways that build the different architectures. To inform these definitions, we collected and photographed live specimens of adult and developing colonies through offshore scuba diving. Since all salp colonies begin their development as a transversal double chain, we characterized each adult colonial architecture as a series of developmental transitions, such as rotations and translations of zooids, relative to their orientation at this early shared stage. We hypothesize that all adult architectures are either final or intermediate stages within three developmental pathways toward bipinnate, cluster, or helical forms. This framework will enable comparative studies on the biomechanical implications, ecological functions, evolutionary history, and engineering applications of the diversity of salp colony architectures.

Metabolic similarity and the predictability of microbial community assembly.

When microbial communities form, their composition is shaped by selective pressures imposed by the environment. Can we predict which communities will assemble under different environmental conditions? Here, we hypothesize that quantitative similarities in metabolic traits across metabolically similar environments lead to predictable similarities in community composition. To that end, we measured the growth rate and by-product profile of a library of proteobacterial strains in a large number of single nutrient environments. We found that growth rates and secretion profiles were positively correlated across environments when the supplied substrate was metabolically similar. By analyzing hundreds of in-vitro communities experimentally assembled in an array of different synthetic environments, we then show that metabolically similar substrates select for taxonomically similar communities. These findings lead us to propose and then validate a comparative approach for quantitatively predicting the effects of novel substrates on the composition of complex microbial consortia.

Evolutionary causes and consequences of ungulate migration.

Ungulate migrations are crucial for maintaining abundant populations and functional ecosystems. However, little is known about how or why migratory behaviour evolved in ungulates. To investigate the evolutionary origins of ungulate migration, we employed phylogenetic path analysis using a comprehensive species-level phylogeny of mammals. We found that 95 of 207 extant ungulate species are at least partially migratory, with migratory behaviour originating independently in 17 lineages. The evolution of migratory behaviour is associated with reliance on grass forage and living at higher latitudes wherein seasonal resource waves are most prevalent. Indeed, originations coincide with mid-Miocene cooling and the subsequent rise of C4 grasslands. Also, evolving migratory behaviour supported the evolution of larger bodies, allowing ungulates to exploit new ecological space. Reconstructions of migratory behaviour further revealed that seven of ten recently extinct species were probably migratory, suggesting that contemporary migrations are important models for understanding the ecology of the past.

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

Siphonophores (Cnidaria: Hydrozoa) are abundant and diverse gelatinous predators in open-ocean ecosystems. Due to limited access to the midwater, little is known about the diets of most deep-dwelling gelatinous species, which constrains our understanding of food-web structure and nutrient flow in these vast ecosystems. Visual gut-content methods can rarely identify soft-bodied rapidly-digested prey, while observations from submersibles often overlook small prey items. These methods have been differentially applied to shallow and deep siphonophore taxa, confounding habitat and methodological biases. DNA metabarcoding can be used to assess both shallow and deep species' diets under a common methodological framework, since it can detect both small and gelatinous prey. We (1) further characterized the diets of open-ocean siphonophores using DNA metabarcoding, (2) compared the prey detected by visual and molecular methods to evaluate their technical biases, and (3) evaluated tentacle-based predictions of diet. To do this, we performed DNA metabarcoding analyses on the gut contents of 39 siphonophore species across depths to describe their diets, using six barcode regions along the 18S gene. Taxonomic identifications were assigned using public databases combined with local zooplankton sequences. We identified 55 unique prey items, including crustaceans, gelatinous animals, and fish across 47 siphonophore specimens in 24 species. We reported 29 novel predator-prey interactions, among them the first insights into the diets of nine siphonophore species, many of which were congruent with the dietary predictions based on tentilla morphology. Our analyses detected both small and gelatinous prey taxa underrepresented by visual methods in species from both shallow and deep habitats, indicating that siphonophores play similar trophic roles across depth habitats. We also reveal hidden links between siphonophores and filter-feeders near the base of the food web. This study expands our understanding of the ecological roles of siphonophores in the open ocean, their trophic roles within the 'jelly-web', and the importance of their diversity for nutrient flow and ecosystem functioning. Understanding these inconspicuous yet ubiquitous predator-prey interactions is critical to predict the impacts of climate change, overfishing, and conservation policies on oceanic ecosystems.

Erythromycin sensitivity across different taxa of marine phytoplankton. A novel approach to sensitivity of microalgae and the evolutionary history of the 23S gene.

Erythromycin has been recorded in coastal waters and could pose a severe threat to marine microbial life. Macrolides such as erythromycin may affect microalgae by inhibiting the pathways involved in protein synthesis. Toxicological testing of microalgae has proven to be a useful tool for the risk assessment of a substance affecting phytoplankton. Due to the controversial results concerning the sensitivity of microalgal species to erythromycin found in the literature, the goals of this work were, initially, to assess the erythromycin sensitivity of different species of marine microalgae from different and representative taxonomic groups; and, secondly, to examine whether the sensitivity to erythromycin could be explained by the differences in the phylogenetic evolution. We chose eight species: two green algae, four heterokonts, one haptophyte and one dinoflagellate, which were then exposed to erythromycin (0.1 to 10 mg L-1). Our results showed a wide range of sensitivities indicating that the biology of each species was primarily responsible for the variation observed. To test the second objective, we contrasted different ecotoxicological endpoints (growth, cellular properties and status of the photosynthetic apparatus) with the phylogenetic distribution [eukaryotic host (concatenated nuclear tree), evolutionary history of the chloroplast (16S tree), efficiency and repair of photosystem II (psbA tree), and the binding site of erythromycin (23S tree)] of the species. We found that the growth inhibition of microalgae as a toxicological endpoint was the endpoint best explained by the topology of the 23S rRNA gene tree when it was modelled following a non-stationary evolutionary process.