Acoustic communication is enabled by the evolution of specialised hearing and sound producing organs. In this study, we performed a large-scale macroevolutionary study to understand how both hearing and sound production evolved and affected diversification in the insect order Orthoptera, which includes many familiar singing insects, such as crickets, katydids, and grasshoppers. Using phylogenomic data, we firmly establish phylogenetic relationships among the major lineages and divergence time estimates within Orthoptera, as well as the lineage-specific and dynamic patterns of evolution for hearing and sound producing organs. In the suborder Ensifera, we infer that forewing-based stridulation and tibial tympanal ears co-evolved, but in the suborder Caelifera, abdominal tympanal ears first evolved in a non-sexual context, and later co-opted for sexual signalling when sound producing organs evolved. However, we find little evidence that the evolution of hearing and sound producing organs increased diversification rates in those lineages with known acoustic communication.

Locusts are grasshoppers that can form dense migrating swarms through an extreme form of density-dependent phenotypic plasticity, known as locust phase polyphenism. We present a comprehensive phylogeny of the genus Schistocerca, which contains both non-swarming grasshoppers and swarming locusts. We find that the desert locust, S. gregaria, which is the only Old World representative of the genus, is the earliest diverging lineage. This suggests that the common ancestor of Schistocerca must have been a swarming locust that crossed the Atlantic Ocean from Africa to America approximately 6 million years ago, giving rise to the current diversity in the New World. This also implies that density-dependent phenotypic plasticity is an ancestral trait for the genus. Through ancestral character reconstruction of reaction norms, we show that colour plasticity has been largely retained in most species in the genus, but behavioural plasticity was lost and regained at least twice. Furthermore, we show that swarming species do not form a monophyletic group and non-swarming species that are closely related to locusts often express locust-like plastic reaction norms. Thus, we conclude that individual reaction norms have followed different evolutionary trajectories, which have led to the evolutionary transition between grasshoppers and locusts - and vice versa.

The grasshopper family Acrididae is one of the most diverse lineages within Orthoptera, including more than 6,700 valid species distributed worldwide. Grasshoppers are dominant herbivores, which have diversified into grassland, desert, semi-aquatic, alpine, and tropical forest habitats, and exhibit a wide array of morphological, ecological, and behavioral diversity. Nevertheless, the phylogeny of Acrididae as a whole has never been proposed. In this study, we present the first comprehensive phylogeny of Acrididae based on mitochondrial genomes and nuclear genes to test monophyly of the family and different subfamilies as well as to understand the evolutionary relationships among them. We recovered the monophyletic Acrididae and identified four major clades as well as several well-characterized subfamilies, but we also found that paraphyly is rampant across many subfamilies, highlighting the need for a taxonomic revision of the family. We found that Acrididae originated in the Paleocene of the Cenozoic period (59.3 million years ago) and, because the separation of South America and Africa predates the origin of the family, we hypothesize that the current cosmopolitan distribution of Acrididae was largely achieved by dispersal. We also inferred that the common ancestor of modern grasshoppers originated in South America, contrary to a popular belief that they originated in Africa, based on a biogeographical analysis. We estimate that there have been a number of colonization and recolonization events between the New World and the Old World throughout the diversification of Acrididae, and, thus, the current diversity in any given region is a reflection of this complex history.

Background: At the time of publication, the most devastating desert locust crisis in decades is affecting East Africa, the Arabian Peninsula and South-West Asia. The situation is extremely alarming in East Africa, where Kenya, Ethiopia and Somalia face an unprecedented threat to food security and livelihoods. Most of the time, however, locusts do not occur in swarms, but live as relatively harmless solitary insects. The phenotypically distinct solitarious and gregarious locust phases differ markedly in many aspects of behaviour, physiology and morphology, making them an excellent model to study how environmental factors shape behaviour and development. A better understanding of the extreme phenotypic plasticity in desert locusts will offer new, more environmentally sustainable ways of fighting devastating swarms. Methods: High molecular weight DNA derived from two adult males was used for Mate Pair and Paired End Illumina sequencing and PacBio sequencing. A reliable reference genome of Schistocerca gregaria was assembled using the ABySS pipeline, scaffolding was improved using LINKS. Results: In total, 1,316 Gb Illumina reads and 112 Gb PacBio reads were produced and assembled. The resulting draft genome consists of 8,817,834,205 bp organised in 955,015 scaffolds with an N50 of 157,705 bp, making the desert locust genome the largest insect genome sequenced and assembled to date. In total, 18,815 protein-encoding genes are predicted in the desert locust genome, of which 13,646 (72.53%) obtained at least one functional assignment based on similarity to known proteins. Conclusions: The desert locust genome data will contribute greatly to studies of phenotypic plasticity, physiology, neurobiology, molecular ecology, evolutionary genetics and comparative genomics, and will promote the desert locust’s use as a model system. The data will also facilitate the development of novel, more sustainable strategies for preventing or combating swarms of these infamous insects.

Locusts exhibit one of nature’s most spectacular examples of complex phenotypic plasticity, in which changes in density cause solitary and cryptic individuals to transform into gregarious and conspicuous locusts forming large migrating swarms. We investigated how these coordinated alternative phenotypes might have evolved by studying the Central American locust and three closely related non-swarming grasshoppers in a comparative framework. By experimentally isolating and crowding during nymphal development, we induced density-dependent phenotypic plasticity and quantified the resulting behavioural, morphological, and molecular reaction norms. All four species exhibited clear plasticity, but the individual reaction norms varied among species and showed different magnitudes. Transcriptomic responses were species-specific, but density-responsive genes were functionally similar across species. There were modules of co-expressed genes that were highly correlated with plastic reaction norms, revealing a potential molecular basis of density-dependent phenotypic plasticity. These findings collectively highlight the importance of studying multiple reaction norms from a comparative perspective.