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This phylogenomic study shows that core muscle proteins were already present in unicellular organisms before the origin of multicellular animals, and supports a convergent evolutionary model for striated muscles in which new proteins are added to ancient contractile apparatus during independent evolution of bilaterians and some non-bilaterians, resulting in very similar ultrastructures. Muscles stretch back a long way The ultrastructural similarity between striated skeletal muscles in higher bilaterian animals, such as humans and insects, and non-bilaterian animals, such as jellyfish, suggests a common evolutionary origin of this important contractile cell type. However, the precise evolution of striated muscles has not been confirmed. In this phylogenomic study, Ulrich Technau and colleagues show that core muscle proteins are present in unicellular organisms, such as sponges, that do not have true muscles. Their analysis supports a convergent-evolution model for striated muscles. According to this model, novel proteins were added to the ancient contractile apparatus during the independent evolution of the cnidarians and bilaterians, resulting in strikingly similar ultrastructures. Striated muscles are present in bilaterian animals (for example, vertebrates, insects and annelids) and some non-bilaterian eumetazoans (that is, cnidarians and ctenophores). The considerable ultrastructural similarity of striated muscles between these animal groups is thought to reflect a common evolutionary origin 1 , 2 . Here we show that a muscle protein core set, including a type II myosin heavy chain (MyHC) motor protein characteristic of striated muscles in vertebrates, was already present in unicellular organisms before the origin of multicellular animals. Furthermore, ‘ striated muscle ’ and ‘ non-muscle ’ myhc orthologues are expressed differentially in two sponges, compatible with a functional diversification before the origin of true muscles and the subsequent use of striated muscle MyHC in fast-contracting smooth and striated muscle. Cnidarians and ctenophores possess striated muscle myhc orthologues but lack crucial components of bilaterian striated muscles, such as genes that code for titin and the troponin complex, suggesting the convergent evolution of striated muscles. Consistently, jellyfish orthologues of a shared set of bilaterian Z-disc proteins are not associated with striated muscles, but are instead expressed elsewhere or ubiquitously. The independent evolution of eumetazoan striated muscles through the addition of new proteins to a pre-existing, ancestral contractile apparatus may serve as a model for the evolution of complex animal cell types.

Organisms that move across ecosystem boundaries connect food webs in apparently disparate locations. As part of their life cycle, aquatic insects transition from aquatic larvae to terrestrial adults, thereby linking freshwater ecosystem processes and terrestrial insectivore dynamics. These linkages are strongly affected by contamination of freshwater ecosystems, which can reduce production of adult aquatic insects (i.e., emergence), increase contaminant concentrations in adult insect tissues, and alter contaminant flux to terrestrial ecosystems. Despite the potential impact of contaminants on adult aquatic insects, little is known about predicting these effects. Here, I develop a heuristic model based on contaminant properties and ecotoxicological principles to predict the effects of various classes of aquatic contaminants on adult aquatic insects and discuss implications for terrestrial insectivores living near contaminated freshwaters. The main finding is that contaminant classes vary greatly in how their biologically-mediated effects on aquatic insects affect terrestrial insectivores. Highly bioaccumulative contaminants that are well retained during metamorphosis, like polychlorinated biphenyls (PCBs), are often non-toxic to aquatic insect larvae at concentrations commonly found in the environment. Such contaminants flux from aquatic ecosystems in large quantities in the bodies of emerging adult aquatic insects and expose terrestrial insectivores to toxic levels of pollution. On the other hand, contaminants that are less bioaccumulative, excreted during metamorphosis, and more toxic to insects, like trace metals, tend to affect terrestrial insectivores by reducing production of adult aquatic insects on which they prey. Management applications of this model illustrate type and severity of risk of aquatic contaminants to consumers of adult aquatic insects.

Cnidarians (for example, sea anemones and jellyfish) develop from an outer ectodermal and inner endodermal germ layer, whereas bilaterians (for example, vertebrates and flies) additionally have a mesodermal layer as intermediate germ layer. Currently, cnidarian endoderm (that is, ‘mesendoderm’) is considered homologous to both bilaterian endoderm and mesoderm. Here we test this hypothesis by studying the fate of germ layers, the localization of gut cell types, and the expression of numerous ‘endodermal’ and ‘mesodermal’ transcription factor orthologues in the anthozoan sea anemone Nematostella vectensis . Surprisingly, we find that the developing pharyngeal ectoderm and its derivatives display a transcription-factor expression profile ( foxA , hhex , islet , soxB1 , hlxB9 , tbx2/3 , nkx6 and nkx2.2 ) and cell-type combination (exocrine and insulinergic) reminiscent of the developing bilaterian midgut, and, in particular, vertebrate pancreatic tissue. Endodermal derivatives, instead, display cell functions and transcription-factor profiles similar to bilaterian mesoderm derivatives (for example, somatic gonad and heart). Thus, our data supports an alternative model of germ layer homologies, where cnidarian pharyngeal ectoderm corresponds to bilaterian endoderm, and the cnidarian endoderm is homologous to bilaterian mesoderm. The cnidarian endoderm has been considered homologous to the bilaterian endoderm and mesoderm. Here, a gut-like ectoderm is revealed in a sea anemone, corresponding to the bilaterian endoderm, supporting an alternative model of germ layer homology.

The complex morphology of neurons requires precise control of their microtubule cytoskeleton. This is achieved by microtubule-associated proteins (MAPs) that regulate the assembly and stability of microtubules, and transport of molecules and vesicles along them. While many of these MAPs function in all cells, some are specifically or predominantly involved in regulating microtubules in neurons. Here we use the sea anemone Nematostella vectensis as a model organism to provide new insights into the early evolution of neural microtubule regulation. As a cnidarian, Nematostella belongs to an outgroup to all bilaterians and thus occupies an informative phylogenetic position for reconstructing the evolution of nervous system development. We identified an ortholog of the microtubule-binding protein doublecortin-like kinase (NvDclk1) as a gene that is predominantly expressed in neurons and cnidocytes (stinging cells), two classes of cells belonging to the neural lineage in cnidarians. A transgenic NvDclk1 reporter line revealed an elaborate network of neurite-like processes emerging from cnidocytes in the tentacles and the body column. A transgene expressing NvDclk1 under the control of the NvDclk1 promoter suggests that NvDclk1 localizes to microtubules and therefore likely functions as a microtubule-binding protein. Further, we generated a mutant for NvDclk1 using CRISPR/Cas9 and show that the mutants fail to generate mature cnidocytes. Our results support the hypothesis that the elaboration of programs for microtubule regulation occurred early in the evolution of nervous systems.

With the decline of bee populations worldwide, studies determining current wild bee distributions and diversity are increasingly important. Wild bee identification is often completed by experienced taxonomists or by genetic analysis. The current study was designed to compare two methods of identification including: (1) morphological identification by experienced taxonomists using images of field-collected wild bees and (2) genetic analysis of composite bee legs (multiple taxa) using metabarcoding. Bees were collected from conservation grasslands in eastern Iowa in summer 2019 and identified to the lowest taxonomic unit using both methods. Sanger sequencing of individual wild bee legs was used as a positive control for metabarcoding. Morphological identification of bees using images resulted in 36 unique taxa among 22 genera, and >80% of Bombus specimens were identified to species. Metabarcoding was limited to genus-level assignments among 18 genera but resolved some morphologically similar genera. Metabarcoding did not consistently detect all genera in the composite samples, including kleptoparasitic bees. Sanger sequencing showed similar presence or absence detection results as metabarcoding but provided species-level identifications for cryptic species (i.e., Lasioglossum ). Genus-specific detections were more frequent with morphological identification than metabarcoding, but certain genera such as Ceratina and Halictus were identified equally well with metabarcoding and morphology. Genera with proportionately less tissue in a composite sample were less likely to be detected using metabarcoding. Image-based methods were limited by image quality and visible morphological features, while genetic methods were limited by databases, primers, and amplification at target loci. This study shows how an image-based identification method compares with genetic techniques, and how in combination, the methods provide valuable genus- and species-level information for wild bees while preserving tissue for other analyses. These methods could be improved and transferred to a field setting to advance our understanding of wild bee distributions and to expedite conservation research.

Studies of aquatic–terrestrial ecosystem linkages explore the mechanisms by which components of one ecosystem, such as the aquatic insect community in a stream, directly affect components of an adjacent ecosystem, such as the density and diversity of riparian predators. On a human level, research into these linkages allows freshwater ecologists to form novel collaborations with stakeholders and other interest groups by emphasizing shared interests. To highlight this point, we use 3 case studies as examples of how aquatic–terrestrial linkages research can be leveraged to achieve multifaceted goals of improving riparian and freshwater management, engaging stakeholders, and advancing ecological understanding. In the 1st case study, we describe a project in which consideration of the complex life histories of aquatic insects could have led to more effective outcomes for riparian bird restoration. The 2nd case study provides an example of how studying contaminant transport through ecological subsidies has been incorporated into programs for contaminant management. In the 3rd case, we use a study of terrestrial vertebrates feeding on adult aquatic insects to show how research into aquatic–terrestrial subsidies connects freshwater ecologists, youth groups, and commercial river guides. By focusing on how in-stream processes propagate onto land through ecological subsidies, we argue that freshwater ecologists also gain a platform for communicating their science to riparian managers and the public, which can improve the potential for stream and riparian co-management and restoration success.

The effects of aquatic contaminants are propagated across ecosystem boundaries by aquatic insects that export resources and contaminants to terrestrial food webs; however, the mechanisms driving these effects are poorly understood. We examined how emergence, contaminant concentration, and total contaminant flux by adult aquatic insects changed over a gradient of bioavailable metals in streams and how these changes affected riparian web-building spiders. Insect emergence decreased 97% over the metal gradient, whereas metal concentrations in adult insects changed relatively little. As a result, total metal exported by insects (flux) was lowest at the most contaminated streams, declining 96% among sites. Spiders were affected by the decrease in prey biomass, but not by metal exposure or metal flux to land in aquatic prey. Aquatic insects are increasingly thought to increase exposure of terrestrial consumers to aquatic contaminants, but stream metals reduce contaminant flux to riparian consumers by strongly impacting the resource linkage. Our results demonstrate the importance of understanding the contaminant-specific effects of aquatic pollutants on adult insect emergence and contaminant accumulation in adults to predict impacts on terrestrial food webs.

Adult aquatic insects are a common resource for many terrestrial predators, often considered to subsidize terrestrial food webs. However, larval aquatic insects themselves consume both aquatic primary producers and allochthonous terrestrial detritus, suggesting that adults could provide aquatic subsidy and/or recycled terrestrial energy to terrestrial consumers. Understanding the source of carbon (aquatic vs. terrestrial) driving aquatic insect emergence is important for predicting magnitude of emergence and effects on recipient food web dynamics; yet direct experimental tests of factors determining source are lacking. Here, we use Culex mosquitoes in experimental pools as an exemplar to test how variation in general factors common to aquatic systems (terrestrial plant inputs and light) may alter the source and amount of energy exported to terrestrial ecosystems in adult aquatic insects that rely on terrestrial resources as larvae. We found strong sequential effects of terrestrial plant inputs and light on aquatic insect oviposition, diet, and emergence of Culex mosquitoes. Ovipositing mosquitoes laid ~3 times more egg masses in high terrestrial input pools under low light conditions. This behavior increased adult emergence from pools under low light conditions; however, high input pools (which had the highest mosquito densities) showed low emergence rates due to density-dependent mortality. Mosquito diets consisted mainly of terrestrial resources (~ 70-90 %). As a result, the amount of aquatic carbon exported from pools by mosquitoes during the experiment was ~ 18 times higher from low versus high light pools, while exports of terrestrial carbon peaked from pools receiving intermediate levels of inputs (3-6 times higher) and low light (~ 6 times higher). Our results suggest that understanding the interplay among terrestrial plant inputs, light availability and biotic responses of aquatic insects may be key in predicting source and magnitude of emergence, and thus the strength and effects of aquatic-terrestrial linkages in freshwater systems.

Background The metagenesis of sessile polyps into pelagic medusae in cnidarians represents one of the most ancient complex life cycles in animals. Interestingly, scyphozoans and hydrozoans generate medusae by apparently fundamentally different processes. It is therefore unclear whether medusa formation has evolved independently in different medusozoans. To this end, a thorough understanding of the correspondence of polyp and medusa is required. Results We monitored the expression patterns of conserved developmental genes in developing medusae of Clytia hemisphaerica (Hydrozoa) and Aurelia aurita (Scyphozoa) and found that developing medusae and polyps share similarities in their morphology and developmental gene expression. Unexpectedly, however, polyp tentacle marker genes were consistently expressed in the developing medusa bell, suggesting that the bell of medusae corresponds to modified and fused polyp tentacle anlagen. Conclusions Our data represent the first comparative gene expression analysis of developing medusae in two representatives of Scyphozoa and Hydrozoa. The results challenge prevailing views about polyp medusa body plan homology. We propose that the evolution of a new life stage may be facilitated by the adoption of existing developmental genes.