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Seasonal animal movement among disparate habitats is a fundamental mechanism by which energy, nutrients, and biomass are transported across ecotones. A dramatic example of such exchange is the annual emergence of mayfly swarms from freshwater benthic habitats, but their characterization at macroscales has remained impossible. We analyzed radar observations of mayfly emergence flights to quantify long-term changes in annual biomass transport along the Upper Mississippi River and Western Lake Erie Basin. A single emergence event can produce 87.9 billion mayflies, releasing 3,078.6 tons of biomass into the airspace over several hours, but in recent years, production across both waterways has declined by over 50%. As a primary prey source in aquatic and terrestrial ecosystems, these declines will impact higher trophic levels and environmental nutrient cycling.

The evolution of winged insects revolutionized terrestrial ecosystems and led to the largest animal radiation on Earth. However, we still have an incomplete picture of the genomic changes that underlay this diversification. Mayflies, as one of the sister groups of all other winged insects, are key to understanding this radiation. Here, we describe the genome of the mayfly Cloeon dipterum and its gene expression throughout its aquatic and aerial life cycle and specific organs. We discover an expansion of odorant-binding-protein genes, some expressed specifically in breathing gills of aquatic nymphs, suggesting a novel sensory role for this organ. In contrast, flying adults use an enlarged opsin set in a sexually dimorphic manner, with some expressed only in males. Finally, we identify a set of wing-associated genes deeply conserved in the pterygote insects and find transcriptomic similarities between gills and wings, suggesting a common genetic program. Globally, this comprehensive genomic and transcriptomic study uncovers the genetic basis of key evolutionary adaptations in mayflies and winged insects. Genomic studies of paleopteran insects, such as mayflies, are needed to reconstruct early insect evolution. Here, Almudi and colleagues present the genome of the mayfly Cloeon dipterum and use transcriptomics to characterize its adaptations to distinct habitats and the origin of insect wings.

In the Paleozoic era, more than 400 Ma, a number of insect groups continued molting after forming functional wings. Today, however, flying insects stop molting after metamorphosis when they become fully winged. The only exception is the mayflies (Paleoptera, Ephemeroptera), which molt in the subimago, a flying stage between the nymph and the adult. However, the identity and homology of the subimago still is underexplored. Debate remains regarding whether this stage represents a modified nymph, an adult, or a pupa like that of butterflies. Another relevant question is why mayflies have the subimago stage despite the risk of molting fragile membranous wings. These questions have intrigued numerous authors, but nonetheless, clear answers have not yet been found. By combining morphological studies, hormonal treatments, and molecular analysis in the mayfly Cloeon dipterum, we found answers to these old questions. We observed that treatment with a juvenile hormone analog in the last nymphal instar stimulated the expression of the Kr-h1 gene and reduced that of E93, which suppress and trigger metamorphosis, respectively. The regulation of metamorphosis thus follows the MEKRE93 pathway, as in neopteran insects. Moreover, the treatment prevented the formation of the subimago. These findings suggest that the subimago must be considered an instar of the adult mayfly. We also observed that the forelegs dramatically grow between the last nymphal instar, the subimago, and the adult. This necessary growth spread over the last two stages could explain, at least in part, the adaptive sense of the subimago.

The Crato Formation (Aptian, Lower Cretaceous) is a fossiliferous deposit of global significance, representing a lacustrine palaeoenvironment which offers insights into aquatic insect taphonomy. Despite its importance, prior studies lacked an actualistic approach. Here, we analyze the preservation of mayflies (Ephemeroptera) and dragonflies (Odonata) from this formation using experimental taphonomy on 253 extant Ephemeroptera and 236 Odonata, alongside 306 fossil specimens. Disarticulation experiments showed that the thorax of modern mayfly larvae disarticulated first, yet Crato Hexagenitidae larvae retained intact thoraces, indicating minimal disturbance and autochthonous deposition. Fossil alate specimens rarely exhibited decay-related wing damage, aligning with short decay times. Dragonfly carcasses exhibited a characteristic leg posture in death, also preserved in Crato fossils, further suggesting minimal transport. Additionally, fossil dragonflies retained labial masks, the first structure to disarticulate experimentally, consistent with parautochthonous assemblages. Mayfly larvae exposed to low salinity during experiments exhibited excessive defecation before death, hinting at possible low salinity conditions in the Crato palaeoenvironment, though preservational challenges obscure confirmation. During experimentation, we also noticed that all carcasses immediately floated under hypersaline conditions, while carcasses immersed in non-hypersaline conditions went through slower decomposition. Thus, we can safely propose with experimental data that microbial biofilms on the surface of the water were acting during carcass sinking in this deposit.

Elevated major ion concentrations in streams are commonly observed as a consequence of resource extraction, de-icing and other anthropogenic activities. Ecologists report biodiversity losses associated with increasing salinity, with mayflies typically being highly responsive to increases of different major ions. In this study, we evaluated the performance of the mayfly Neocloeon triangulifer reared for its entire larval phase in a gradient of sulfate concentrations. Two natural waters were amended with SO 4 as a blend of CaSO 4 and MgSO 4 and exposures ranged from 5 to 1500 mg l –1 SO 4. Survival (per cent successful emergence to the subimago stage) was significantly reduced at the highest SO 4 concentration in both waters, while development was significantly delayed at 667 mg l −1 SO 4 . Final sub-adult body weights were consistent across treatments, except at the highest treatment concentration. Despite evidence for sulfate uptake rates increasing with exposure concentrations and not being saturated at even extremely high SO 4 concentrations, total body sulfur changed little in subimagos. Together, these results suggest that elevated SO 4 imposes an energetic demand associated with maintaining homeostasis that is manifested primarily as reduced growth rates and associated developmental delays. We identified two genes related to sulfate transport in N. triangulifer . This article is part of the theme issue ‘Salt in freshwaters: causes, ecological consequences and future prospects’.

The genus Cymbalcloeon gen. nov. (Ephemeroptera: Baetidae) is established for a new species Cymbalcloeon sartorii sp. nov. from Thailand, based on larval stage. This genus is unique among all of the Baetidae by the presence of three pairs of single gills on segments V-VII, ventrally oriented to cover the sterna VI-IX. Cymbalcloeon sartorii gen. nov. et sp. nov. presents unique or rare morphological characters such as a deeply concave margin between the prostheca and mola, without setae; a very large subtriangular process of the left mandible; a maxillary palp segment II with scarce and very long setae; almost completely fused labial palp segments II and III with numerous very long setae; elongate tarsal claw with two rows of teeth; a shagreen surface of the terga and paraproct; and a very reduced body size. The gills of the new genus move very quickly during respiration and present a near-synchronous protraction. Due to the very derived larval morphological character and the unknown imaginal stage, the exact phylogenetic position of the genus remains unclear; it most certainly belongs to the concept of Anteropatellata and is possibly closely related to the genus Baetopus.

The salinity of many freshwaters is increasing globally as a result of human activities. Associated with this increase in salinity are losses of Ephemeroptera (mayfly) abundance and richness. The salinity concentrations at which Ephemeroptera decline in nature are lower than their internal salinity or haemolymph osmolality. Many species also suffer substantial mortality in single species laboratory toxicity tests at salinities lower than their internal salinity. These findings are problematic as conventional osmoregulation theory suggests that freshwater animals should not experience stress where external osmolality is greater than haemolymph osmolality. Here I explore three hypotheses to explain salt sensitivity in Ephemeroptera. These conceptual hypotheses are based on the observations that as the external sodium ion (Na + ) concentration increases so does the Na + turnover rate (both uptake and elimination rates increase). Sulphate ( ) uptake in mayflies also increases with increasing external although, unlike Na + , its rate of increase decreases with increasing external . The first hypothesis is premised on ion turnover being energetically costly. The first hypothesis proposes that individuals must devote a greater proportion of their energy to ion homeostasis at the expense of other uses including growth and development. Lethal levels of salinity presumably result from individuals not being able to devote enough energy to maintain ion homeostasis without critical loss of other vital functions. The second hypothesis is premised on the uptake of Na + exchanged for (an outgoing) H + , leading to (localized) loss of pH regulation. The third hypothesis is premised on localized Na + toxicity or poisoning with increased Na turnover as salinity increases. None of the proposed hypotheses is without potential problems, yet all are testable, and research effort should be focused at attempting to falsify them. This article is part of the theme issue ‘Salt in freshwaters: causes, ecological consequences and future prospects’.

, a micro-endemic species reported from several streams within the Aurès Mountains (north-eastern Algeria), is described and illustrated at nymphal, subimaginal and imaginal stages of both sexes. Critical morphological diagnostic characters distinguishing the new species are presented, together with molecular affinities as well as notes on the biology and distribution of the species.

Ecological photopollution created by artificial night lighting can alter animal behavior and lead to population declines and biodiversity loss. Polarized light pollution is a second type of photopollution that triggers water-seeking insects to ovisposit on smooth and dark man-made objects, because they simulate the polarization signatures of natural water bodies. We document a case study of the interaction of these two forms of photopollution by conducting observations and experiments near a lamp-lit bridge over the river Danube that attracts mass swarms of the mayfly Ephoron virgo away from the river to oviposit on the asphalt road of the bridge. Millions of mayflies swarmed near bridge-lights for two weeks. We found these swarms to be composed of 99% adult females performing their upstream compensatory flight and were attracted upward toward unpolarized bridge-lamp light, and away from the horizontally polarized light trail of the river. Imaging polarimetry confirmed that the asphalt surface of the bridge was strongly and horizontally polarized, providing a supernormal ovipositional cue to Ephoron virgo, while other parts of the bridge were poor polarizers of lamplight. Collectively, we confirm that Ephoron virgo is independently attracted to both unpolarized and polarized light sources, that both types of photopollution are being produced at the bridge, and that spatial patterns of swarming and oviposition are consistent with evolved behaviors being triggered maladaptively by these two types of light pollution. We suggest solutions to bridge and lighting design that should prevent or mitigate the impacts of such scenarios in the future. The detrimental impacts of such scenarios may extend beyond Ephoron virgo.

The origin of the insect odorant receptor (OR) gene family has been hypothesized to have coincided with the evolution of terrestriality in insects. Missbach et al. (2014) suggested that ORs instead evolved with an ancestral OR co-receptor (Orco) after the origin of terrestriality and the OR/Orco system is an adaptation to winged flight in insects. We investigated genomes of the Collembola, Diplura, Archaeognatha, Zygentoma, Odonata, and Ephemeroptera, and find ORs present in all insect genomes but absent from lineages predating the evolution of insects. Orco is absent only in the ancestrally wingless insect lineage Archaeognatha. Our new genome sequence of the zygentoman firebrat Thermobia domestica reveals a full OR/Orco system. We conclude that ORs evolved before winged flight, perhaps as an adaptation to terrestriality, representing a key evolutionary novelty in the ancestor of all insects, and hence a molecular synapomorphy for the Class Insecta.