The most remarkable migrants-systematic analysis of the Western European insect flyway at a Pyrenean mountain pass.

In autumn 1950 David and Elizabeth Lack chanced upon a huge migration of insects and birds flying through the Pyrenean Pass of Bujaruelo, from France into Spain, later describing the spectacle as combining both grandeur and novelty. The intervening years have seen many changes to land use and climate, posing the question as to the current status of this migratory phenomenon. In addition, a lack of quantitative data has prevented insights into the ecological impact of this mass insect migration and the factors that may influence it. To address this, we revisited the site in autumn over a 4 year period and systematically monitored abundance and species composition of diurnal insect migrants. We estimate an annual mean of 17.1 million day-flying insect migrants from five orders (Diptera, Hymenoptera, Hemiptera, Lepidoptera and Odonata) moving south, with observations of southward 'mass migration' events associated with warmer temperatures, the presence of a headwind, sunlight, low windspeed and low rainfall. Diptera dominated the migratory assemblage, and annual numbers varied by more than fourfold. Numbers at this single site hint at the likely billions of insects crossing the entire Pyrenean mountain range each year, and we highlight the importance of this route for seasonal insect migrants.

Evolution of tissue-specific expression of ancestral genes across vertebrates and insects.

Regulation of gene expression is arguably the main mechanism underlying the phenotypic diversity of tissues within and between species. Here we assembled an extensive transcriptomic dataset covering 8 tissues across 20 bilaterian species and performed analyses using a symmetric phylogeny that allowed the combined and parallel investigation of gene expression evolution between vertebrates and insects. We specifically focused on widely conserved ancestral genes, identifying strong cores of pan-bilaterian tissue-specific genes and even larger groups that diverged to define vertebrate and insect tissues. Systematic inferences of tissue-specificity gains and losses show that nearly half of all ancestral genes have been recruited into tissue-specific transcriptomes. This occurred during both ancient and, especially, recent bilaterian evolution, with several gains being associated with the emergence of unique phenotypes (for example, novel cell types). Such pervasive evolution of tissue specificity was linked to gene duplication coupled with expression specialization of one of the copies, revealing an unappreciated prolonged effect of whole-genome duplications on recent vertebrate evolution.

The genome sequence of the Lesser Hornet Hoverfly, Volucella inanis (Linnaeus, 1758).

We present a genome assembly from an individual female Volucella inanis (the Lesser Hornet Hoverfly; Arthropoda; Insecta; Diptera; Syrphidae). The genome sequence is 961 megabases in span. Most of the assembly is scaffolded into six chromosomal pseudomolecules, including the assembled X sex chromosome. The mitochondrial genome has also been assembled and is 16.0 kilobases in length. Gene annotation of this assembly on Ensembl has identified 11,616 protein coding genes.

The efficiency of varying methods and degrees of time compensation for the solar azimuth.

Daytime migrants are known to orientate using the position of the sun, compensating for its changing position throughout the day with a 'time-compensated sun compass'. This compass has been demonstrated in many migratory species, with various degrees of accuracy for the actual movement of the sun. Here, we present a model for differing levels of compensation for the solar ephemeris that shows that a high degree of efficiency, in terms of distance travelled, can be achieved without full time compensation. In our model, compensating for the sun's position had a diminishing return with an accuracy of 80% leading to only a 2% reduction in distance travelled. We compare various modes of time compensation-full, partial, time averaged and step-revealing their directional efficiency in terms of distance travelled under an autumn migration scenario. We find that the benefit of time compensation varies with latitude, with time averaging performing very well, especially at all high latitudes, but step compensation performing better at very low latitudes. Importantly, even rudimentary adjustment can dramatically increase the efficiency of migration, which suggests an easy pathway for the independent evolution of time compensation.

The genome sequence of the Vagrant Hoverfly, Eupeodes corollae (Fabricius, 1794).

We present a genome assembly from an individual female Eupeodes corollae (the Vagrant Hoverfly; Arthropoda; Insecta; Diptera; Syrphidae). The genome sequence is 648.2 megabases in span. Most of the assembly is scaffolded into four chromosomal pseudomolecules, including with the X sex chromosome. The mitochondrial genome has also been assembled and is 18.3 kilobases in length.

Bat activity correlated with migratory insect bioflows in the Pyrenees.

High altitude mountain passes in the Pyrenees are known to be important migratory hotspots for autumn migrating insects originating from large swathes of northern Europe. In the Pyrenees, prior research has focused on diurnal migratory insects. In this study, we investigate the nocturnal component of the migratory assemblage and ask if this transient food source is also used by bat species. Three seasons of insect trapping revealed 66 species of four different orders, 90% of which were Noctuid moths, including the destructive pest Helicoverpa armigera, otherwise known as the cotton bollworm. Acoustic bat detectors revealed that high activity of Nyctalus spp. and Tadarida teniotis bats were closely synchronized with the arrival of the migratory moths, suggesting this food source is important for both resident and migratory bats to build or maintain energy reserves. Bats of the Nyctalus spp. are likely migrating through the study site using fly-and-forage strategies or stopping over in the area, while resident T. teniotis may be exploiting the abundant food source to build fat stores for hibernation. This study shows that nocturnal migratory insects are abundant in the Pyrenees during autumn and interact during migration, not only with their co-migrant bats but also with resident bat species.

The genome sequence of the slender grass hoverfly, Melanostoma scalare (Fabricius, 1794).

We present a genome assembly from an individual male Melanostoma scalare (the slender grass hoverfly; Arthropoda; Insecta; Diptera; Syrphidae). The genome sequence is 738.2 megabases in span. Most of the assembly is scaffolded into 5 chromosomal pseudomolecules, including the X and Y sex chromosomes. The mitochondrial genome has also been assembled and is 16.08 kilobases in length.

The genome sequence of the Common Spotted Hoverfly, Eupeodes luniger (Meigen, 1822).

We present a genome assembly from an individual female Eupeodes luniger (the Common Spotted Hoverfly; Arthropoda; Insecta; Diptera; Syrphidae). The genome sequence is 616.9 megabases in span. Most of the assembly is scaffolded into 4 chromosomal pseudomolecules. The mitochondrial genome has also been assembled and is 17.45 kilobases in length.

Migratory hoverflies orientate north during spring migration.

Migratory hoverflies are long-range migrants that, in the Northern Hemisphere, move seasonally to higher latitudes in the spring and lower latitudes in the autumn. The preferred migratory direction of hoverflies in the autumn has been the subject of radar and flight simulator studies, while spring migration has proved to be more difficult to characterize owing to a lack of ground observations. Consequently, the preferred migratory direction during spring has only been inferred from entomological radar studies and patterns of local abundance, and currently lacks ground confirmation. Here, during a springtime arrival of migratory insects onto the Isles of Scilly and mainland Cornwall, UK, we provide ground proof that spring hoverfly migrants have an innate northward preference. Captured migratory hoverflies displayed northward vanishing bearings when released under sunny conditions under both favourable wind and zero-wind conditions. In addition, and unlike autumn migrants, spring individuals were also able to orientate when the sun was obscured. Analysis of winds suggests an origin for insects arriving on the Isles of Scilly as being in western France. These findings of spring migration routes and preferred migration directions are likely to extend to the diverse set of insects found within the western European migratory assemblage.

Genome-wide transcriptomic changes reveal the genetic pathways involved in insect migration.

Insects are capable of extraordinary feats of long-distance movement that have profound impacts on the function of terrestrial ecosystems. The ability to undertake these movements arose multiple times through the evolution of a suite of traits that make up the migratory syndrome, however the underlying genetic pathways involved remain poorly understood. Migratory hoverflies (Diptera: Syrphidae) are an emerging model group for studies of migration. They undertake seasonal movements in huge numbers across large parts of the globe and are important pollinators, biological control agents and decomposers. Here, we assembled a high-quality draft genome of the marmalade hoverfly (Episyrphus balteatus). We leveraged this genomic resource to undertake a genome-wide transcriptomic comparison of actively migrating Episyrphus, captured from a high mountain pass as they flew south to overwinter, with the transcriptomes of summer forms which were non-migratory. We identified 1543 genes with very strong evidence for differential expression. Interrogation of this gene set reveals a remarkable range of roles in metabolism, muscle structure and function, hormonal regulation, immunity, stress resistance, flight and feeding behaviour, longevity, reproductive diapause and sensory perception. These features of the migrant phenotype have arisen by the integration and modification of pathways such as insulin signalling for diapause and longevity, JAK/SAT for immunity, and those leading to octopamine production and fuelling to boost flight capabilities. Our results provide a powerful genomic resource for future research, and paint a comprehensive picture of global expression changes in an actively migrating insect, identifying key genomic components involved in this important life-history strategy.

The genome sequence of the dumpy grass hoverfly, Melanostoma mellinum (Linnaeus, 1758).

We present a genome assembly from an individual male Melanostoma mellinum (the dumpy grass hoverfly; Arthropoda; Insecta; Diptera; Syriphidae). The genome sequence is 731 megabases in span. The majority of the assembly (99.67%) is scaffolded into five chromosomal pseudomolecules, with the X and Y sex chromosomes assembled. The complete mitochondrial genome was also assembled and is 16.1 kilobases in length.

The genome sequence of the plain-faced dronefly, Eristalis arbustorum (Linnaeus, 1758).

We present a genome assembly from an individual female Eristalis arbustorum (the plain-faced dronefly; Arthropoda; Insecta; Diptera; Syriphidae). The genome sequence is 451 megabases in span. The majority of the assembly (94.71%) is scaffolded into 6 chromosomal pseudomolecules, with the X sex chromosome assembled. The complete mitochondrial genome was also assembled and is 16.0 kilobases in length.

Hoverflies use a time-compensated sun compass to orientate during autumn migration.

The sun is the most reliable celestial cue for orientation available to daytime migrants. It is widely assumed that diurnal migratory insects use a 'time-compensated sun compass' to adjust for the changing position of the sun throughout the day, as demonstrated in some butterfly species. The mechanisms used by other groups of diurnal insect migrants remain to be elucidated. Migratory species of hoverflies (Diptera: Syrphidae) are one of the most abundant and beneficial groups of diurnal migrants, providing multiple ecosystem services and undergoing directed seasonal movements throughout much of the temperate zone. To identify the hoverfly navigational strategy, a flight simulator was used to measure orientation responses of the hoverflies Scaeva pyrastri and Scaeva selenitica to celestial cues during their autumn migration. Hoverflies oriented southwards when they could see the sun and shifted this orientation westward following a 6 h advance of their circadian clocks. Our results demonstrate the use of a time-compensated sun compass as the primary navigational mechanism, consistent with field observations that hoverfly migration occurs predominately under clear and sunny conditions.

The genome sequence of the clouded yellow, Colias crocea (Geoffroy, 1785).

We present a genome assembly from an individual female Colias crocea (also known as Colias croceus; the clouded yellow; Arthropoda; Insecta; Lepidoptera; Pieridae). The genome sequence is 325 megabases in span. The complete assembly is scaffolded into 32 chromosomal pseudomolecules, with the W and Z sex chromosome assembled. Gene annotation of this assembly on Ensembl has identified 13,803 protein coding genes.

The genome sequence of the two-banded wasp hoverfly, Chrysotoxum bicinctum (Linnaeus, 1758).

We present a genome assembly from an individual female Chrysotoxum bicinctum (the two-banded wasp hoverfly; Arthropoda; Insecta; Diptera; Syriphidae). The genome sequence is 913 megabases in span. The majority of the assembly (98.81%) is scaffolded into five chromosomal pseudomolecules, with the X sex chromosome assembled.

The genome sequence of the tapered dronefly, Eristalis pertinax (Scopoli, 1763).

We present a genome assembly from an individual male Eristalis tenax (the tapered dronefly; Arthropoda; Insecta; Diptera; Syriphidae). The genome sequence is 487 megabases in span. The majority of the assembly (95.23%) is scaffolded into seven chromosomal pseudomolecules, with the X and Y sex chromosomes assembled. The complete mitochondrial genome was also assembled and is 17.2 kilobases in length.

Adaptive strategies of high-flying migratory hoverflies in response to wind currents.

Large migrating insects, flying at high altitude, often exhibit complex behaviour. They frequently elect to fly on winds with directions quite different from the prevailing direction, and they show a degree of common orientation, both of which facilitate transport in seasonally beneficial directions. Much less is known about the migration behaviour of smaller (10-70 mg) insects. To address this issue, we used radar to examine the high-altitude flight of hoverflies (Diptera: Syrphidae), a group of day-active, medium-sized insects commonly migrating over the UK. We found that autumn migrants, which must move south, did indeed show migration timings and orientation responses that would take them in this direction, despite the unfavourability of the prevailing winds. Evidently, these hoverfly migrants must have a compass (probably a time-compensated solar mechanism), and a means of sensing the wind direction (which may be determined with sufficient accuracy at ground level, before take-off). By contrast, hoverflies arriving in the UK in spring showed weaker orientation tendencies, and did not correct for wind drift away from their seasonally adaptive direction (northwards). However, the spring migrants necessarily come from the south (on warm southerly winds), so we surmise that complex orientation behaviour may not be so crucial for the spring movements.

Pollination by hoverflies in the Anthropocene.

Pollinator declines, changes in land use and climate-induced shifts in phenology have the potential to seriously affect ecosystem function and food security by disrupting pollination services provided by insects. Much of the current research focuses on bees, or groups other insects together as 'non-bee pollinators', obscuring the relative contribution of this diverse group of organisms. Prominent among the 'non-bee pollinators' are the hoverflies, known to visit at least 72% of global food crops, which we estimate to be worth around US$300 billion per year, together with over 70% of animal pollinated wildflowers. In addition, hoverflies provide ecosystem functions not seen in bees, such as crop protection from pests, recycling of organic matter and long-distance pollen transfer. Migratory species, in particular, can be hugely abundant and unlike many insect pollinators, do not yet appear to be in serious decline. In this review, we contrast the roles of hoverflies and bees as pollinators, discuss the need for research and monitoring of different pollinator responses to anthropogenic change and examine emerging research into large populations of migratory hoverflies, the threats they face and how they might be used to improve sustainable agriculture.

Quantification of migrant hoverfly movements (Diptera: Syrphidae) on the West Coast of North America.

The seasonal migration of huge numbers of hoverflies is frequently reported in Europe from mountain passes or spurs of land. The movement of such large numbers of beneficial insects is thought to provide significant ecosystem services in terms of pollination and pest control. Observations from the East Coast of the USA during the 1920s indicate the presence of migratory life histories among some hoverfly species there, but 90 years have now passed since the last reported observation of hoverfly migration in the USA. Here, we analyse video footage taken during a huge northward migration of hoverflies on 20 April 2017 on the West Coast of California. The quantification of migrant numbers from this footage allows us to estimate the passage of over 100 000 hoverflies in half an hour over a 200 m section of headland in Montaña de Oro State Park (San Luis Obispo County). Field collections and analysis of citizen science data indicate different species from the previously reported Eristalis tenax migrations on the East Coast of the USA and provide evidence for migration among North American hoverflies. We wish to raise awareness of this phenomenon and suggest approaches to advance the study of hoverfly migration in North America and elsewhere.

Mass Seasonal Migrations of Hoverflies Provide Extensive Pollination and Crop Protection Services.

Despite the fact that migratory insects dominate aerial bioflows in terms of diversity, abundance, and biomass [1-6], the migration patterns of most species, and the effects of their annual fluxes between high- and low-latitude regions, are poorly known. One important group of long-range migrants that remain understudied is a suite of highly beneficial species of hoverfly in the tribe Syrphini, which we collectively term "migrant hoverflies." Adults are key pollinators [7-10] and larvae are significant biocontrol agents of aphid crop pests [11], and thus, it is important to quantify the scale of their migrations and the crucial ecosystem services they provide with respect to energy, nutrient, and biomass transport; regulation of crop pests; and pollen transfer. Such assessments cannot be made by sporadic observations of mass arrivals at ground level, because hoverflies largely migrate unnoticed high above ground. We used insect-monitoring radars [12] to show that up to 4 billion hoverflies (80 tons of biomass) travel high above southern Britain each year in seasonally adaptive directions. The long-range migrations redistribute tons of essential nutrients (nitrogen [N] and phosphorus [P]) and transport billions of pollen grains between Britain and Europe, and locally produced populations consume 6 trillion aphids and make billions of flower visits. Migrant hoverfly abundance fluctuated greatly between years, but there was no evidence of a population trend during the 10-year study period. Considering that many beneficial insects are seriously declining [7, 10, 13-19], our results demonstrate that migrant hoverflies are key to maintaining essential ecosystem services.