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.

The repeated evolutionary specialization of distantly related insects to cardenolide-containing host plants provides a stunning example of parallel adaptation. Hundreds of herbivorous insect species have independently evolved insensitivity to cardenolides, which are potent inhibitors of the alpha-subunit of Na + ,K + -ATPase (ATPα). Previous studies investigating ATPα-mediated cardenolide insensitivity in five insect orders have revealed remarkably high levels of parallelism in the evolution of this trait, including the frequent occurrence of parallel amino acid substitutions at two sites and recurrent episodes of duplication followed by neo-functionalization. Here we add data for a sixth insect order, Orthoptera, which includes an ancient group of highly aposematic cardenolide-sequestering grasshoppers in the family Pyrgomorphidae. We find that Orthopterans exhibit largely predictable patterns of evolution of insensitivity established by sampling other insect orders. Taken together the data lend further support to the proposal that negative pleiotropic constraints are a key determinant in the evolution of cardenolide insensitivity in insects. Furthermore, analysis of our expanded taxonomic survey implicates positive selection acting on site 111 of cardenolide-sequestering species with a single-copy of ATPα, and sites 115, 118 and 122 in lineages with neo-functionalized duplicate copies, all of which are sites of frequent parallel amino acid substitution. This article is part of the theme issue ‘Convergent evolution in the genomics era: new insights and directions’.

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.

1The repeated evolutionary specialisation of distantly related insects to cardenolide-containing 2 host plants provides a stunning example of parallel adaptation. Hundreds of herbivorous insect 3 species have independently evolved insensitivity to cardenolides, which are potent inhibitors of 4 the alpha-subunit of Na + , K + -ATPase (ATPα). Previous studies investigating ATPα-mediated 5 cardenolide insensitivity in five insect orders have revealed remarkably high levels of parallelism 6 in the evolution of this trait, including the frequent occurrence of parallel amino acid 7 substitutions at two sites and recurrent episodes of duplication followed by neo-functionalisation. 8Here we add data for a sixth insect order, Orthoptera, which includes an ancient group of highly 9 aposematic cardenolide-sequestering grasshoppers in the family Pyrgomorphidae. We find that 10

The family Pyrgomorphidae (Orthoptera: Caelifera) is considered one of the most colourful grasshopper families, which contains about 500 species distributed worldwide. Commonly referred to as gaudy or bush grasshoppers, many pyrgomorphs are known to be aposematic and capable of sequestering plant secondary compounds. Several species are considered important agricultural pests, while some species are culturally important. Nevertheless, the phylogeny of this family has never been proposed using modern cladistic methods. In this study, we present a phylogenetic analysis of Pyrgomorphidae, based on 119 morphological characters with 269 character states, covering 28 out of 31 current recognized tribes. We recovered the monophyly of the family and one of the two currently recognized subfamilies, Orthacridinae. Pyrgomorphinae was recovered as paraphyletic. Based on the most parsimonious tree, we propose four main clades and discuss the biology and biogeography of members of these clades. This is the first step towards building a natural classification for Pyrgomorphidae, which is an excellent model system for studying the evolution of interesting traits such as wing development, warning coloration and chemical defence.