The evolutionary process of invasion in the fall armyworm (Spodoptera frugiperda).

The fall armyworm (FAW; Spodoptera frugiperda) is one of the major agricultural pest insects. FAW is native to the Americas, and its invasion was first reported in West Africa in 2016. Then it quickly spread through Africa, Asia, and Oceania, becoming one of the main threats to corn production. We analyzed whole genome sequences of 177 FAW individuals from 12 locations on four continents to infer evolutionary processes of invasion. Principal component analysis from the TPI gene and whole genome sequences shows that invasive FAW populations originated from the corn strain. Ancestry coefficient and phylogenetic analyses from the nuclear genome indicate that invasive populations are derived from a single ancestry, distinct from native populations, while the mitochondrial phylogenetic tree supports the hypothesis of multiple introductions. Adaptive evolution specific to invasive populations was observed in detoxification, chemosensory, and digestion genes. We concluded that extant invasive FAW populations originated from the corn strain with potential contributions of adaptive evolution.

Host-plant adaptation as a driver of incipient speciation in the fall armyworm (Spodoptera frugiperda).

BACKGROUND: Divergent selection on host-plants is one of the main evolutionary forces driving ecological speciation in phytophagous insects. The ecological speciation might be challenging in the presence of gene flow and assortative mating because the direction of divergence is not necessarily the same between ecological selection (through host-plant adaptation) and assortative mating. The fall armyworm (FAW), a major lepidopteran pest species, is composed of two sympatric strains, corn and rice strains, named after two of their preferred host-plants. These two strains have been hypothesized to undergo incipient speciation, based on (i) several lines of evidence encompassing both pre- and post-zygotic reproductive isolation, and (ii) the presence of a substantial level of genetic differentiation. Even though the status of these two strains has been established a long time ago, it is still yet to be found whether these two strains indeed exhibit a marked level of genetic differentiation from a large number of genomic loci. Here, we analyzed whole genome sequences from 56 FAW individuals either collected from pasture grasses (a part of the favored host range of the rice strain) or corn to assess the role of host-plant adaptation in incipient speciation. RESULTS: Principal component analysis of whole genome data shows that the pattern of divergence in the fall armyworm is predominantly explained by the genetic differentiation associated with host-plants. The level of genetic differentiation between corn and rice strains is particularly marked in the Z chromosome. We identified one autosomal locus and two Z chromosome loci targeted by selective sweeps specific to rice strain and corn strain, respectively. The autosomal locus has both increased DXY and FST while the Z chromosome loci had decreased DXY and increased FST. CONCLUSION: These results show that the FAW population structure is dominated by the genetic differentiation between corn and rice strains. This differentiation involves divergent selection targeting at least three loci, which include a locus potentially causing reproductive isolation. Taken together, these results suggest the evolutionary scenario that host-plant speciation is a driver of incipient speciation in the fall armyworm.

Genetic data from the extinct giant rat from Tenerife (Canary Islands) points to a recent divergence from mainland relatives.

Evolution of vertebrate endemics in oceanic islands follows a predictable pattern, known as the island rule, according to which gigantism arises in originally small-sized species and dwarfism in large ones. Species of extinct insular giant rodents are known from all over the world. In the Canary Islands, two examples of giant rats, †Canariomys bravoi and †Canariomys tamarani, endemic to Tenerife and Gran Canaria, respectively, disappeared soon after human settlement. The highly derived morphological features of these insular endemic rodents hamper the reconstruction of their evolutionary histories. We have retrieved partial nuclear and mitochondrial data from †C. bravoi and used this information to explore its evolutionary affinities. The resulting dated phylogeny confidently places †C. bravoi within the African grass rat clade (Arvicanthis niloticus). The estimated divergence time, 650 000 years ago (95% higher posterior densities: 373 000-944 000), points toward an island colonization during the Günz-Mindel interglacial stage. †Canariomys bravoi ancestors would have reached the island via passive rafting and then underwent a yearly increase of mean body mass calculated between 0.0015 g and 0.0023 g; this corresponds to fast evolutionary rates (in darwins (d), ranging from 7.09 d to 2.78 d) that are well above those observed for non-insular mammals.

A novel reference dated phylogeny for the genus Spodoptera Guenée (Lepidoptera: Noctuidae: Noctuinae): new insights into the evolution of a pest-rich genus.

The noctuid genus Spodoptera currently consists of 31 species with varied host plant breadths, ranging from monophagous and oligophagous non-pest species to polyphagous pests of economic importance. Several of these pest species have become major invaders, colonizing multiple continents outside their native range. Such is the case of the infamous fall armyworm, Spodoptera frugiperda (J.E. Smith), which includes two recognized host strains that have not been treated as separate species. Following its accidental introduction to Africa in 2016, it quickly spread through Africa and Asia to Australia. Given that half the described Spodoptera species cause major crop losses, comparative genomics studies of several Spodoptera species have highlighted major adaptive changes in genetic architecture, possibly relating to their pest status. Several recent population genomics studies conducted on two species enable a more refined understanding of their population structures, migration patterns and invasion processes. Despite growing interest in the genus, the taxonomic status of several Spodoptera species remains unstable and evolutionary studies suffer from the absence of a robust and comprehensive dated phylogenetic framework. We generated mitogenomic data for 14 Spodoptera taxa, which are combined with data from 15 noctuoid outgroups to generate a resolved mitogenomic backbone phylogeny using both concatenation and multi-species coalescent approaches. We combine this backbone with additional mitochondrial and nuclear data to improve our understanding of the evolutionary history of the genus. We also carry out comprehensive dating analyses, which implement three distinct calibration strategies based on either primary or secondary fossil calibrations. Our results provide an updated phylogenetic framework for 28 Spodoptera species, identifying two well-supported ecologically diverse clades that are recovered for the first time. Well-studied larvae in each of these clades are characterized by differences in mandibular shape, with one clade's being more specialized on silica-rich C4 grasses. Interestingly, the inferred timeframe for the genus suggests an earlier origin than previously thought for the genus: about 17-18 million years ago.

Genome-wide macroevolutionary signatures of key innovations in butterflies colonizing new host plants.

The mega-diversity of herbivorous insects is attributed to their co-evolutionary associations with plants. Despite abundant studies on insect-plant interactions, we do not know whether host-plant shifts have impacted both genomic adaptation and species diversification over geological times. We show that the antagonistic insect-plant interaction between swallowtail butterflies and the highly toxic birthworts began 55 million years ago in Beringia, followed by several major ancient host-plant shifts. This evolutionary framework provides a valuable opportunity for repeated tests of genomic signatures of macroevolutionary changes and estimation of diversification rates across their phylogeny. We find that host-plant shifts in butterflies are associated with both genome-wide adaptive molecular evolution (more genes under positive selection) and repeated bursts of speciation rates, contributing to an increase in global diversification through time. Our study links ecological changes, genome-wide adaptations and macroevolutionary consequences, lending support to the importance of ecological interactions as evolutionary drivers over long time periods.

Complete mitogenome data from a European specimen of Ostrinia scapulalis (Walker, 1859) (Lepidoptera, Pyraloidea, Crambidae, Pyraustinae).

We present an assembly and annotation of the mitogenome of a European specimen of the Adzuki bean borer, Ostrinia scapulalis (Walker, 1859). The data were obtained by combining WGS data issue of a de novo and a previously published sequence library (Gschloessl et al., 2018). We also provide the phylogenetic positioning of the mitogenome within the Ostrinia genus, the Crambidae family and with more distant Lepidoptera species.

Opposite macroevolutionary responses to environmental changes in grasses and insects during the Neogene grassland expansion.

The rise of Neogene C4 grasslands is one of the most drastic changes recently experienced by the biosphere. A central - and widely debated - hypothesis posits that Neogene grasslands acted as a major adaptive zone for herbivore lineages. We test this hypothesis with a novel model system, the Sesamiina stemborer moths and their associated host-grasses. Using a comparative phylogenetic framework integrating paleoenvironmental proxies we recover a negative correlation between the evolutionary trajectories of insects and plants. Our results show that paleoenvironmental changes generated opposing macroevolutionary dynamics in this insect-plant system and call into question the role of grasslands as a universal adaptive cradle. This study illustrates the importance of implementing environmental proxies in diversification analyses to disentangle the relative impacts of biotic and abiotic drivers of macroevolutionary dynamics.

Fossils know it best: Using a new set of fossil calibrations to improve the temporal phylogenetic framework of murid rodents (Rodentia: Muridae).

Murid rodents (Rodentia: Muridae) represent the most diverse and abundant mammalian family. In this study, we provide a refined set of fossil calibrations which is used to reconstruct a dated phylogeny of the family using a multilocus dataset (six nuclear and nine mitochondrial gene fragments) encompassing 161 species representing 82 murid genera from four extant subfamilies (Deomyinae, Gerbillinae, Lophiomyinae and Murinae). In comparison with previous studies on murid or muroid rodents, our work stands out for the implementation of nine robust fossil constraints within the Muridae thanks to a thorough review of the fossil record. Before being assigned to specific nodes of the phylogeny, all potential fossil constraints were carefully assessed; they were also subjected to several cross-validation analyses. The resulting phylogeny is consistent with previous phylogenetic studies on murids, and recovers the monophyly of all sampled murid subfamilies and tribes. Based on nine controlled fossil calibrations, our inferred temporal timeframe indicates that the murid family likely originated in the course of the Early Miocene, 22.0-17.0 million years ago (Ma), and that most major lineages (i.e. tribes) started diversifying ca. 10 Ma. Historical biogeography analyses support the tropical origin for the family, with an initial internal split (vicariance event) between Afrotropical and Oriental (Indomalaya and Philippines) lineages. During the course of their diversification, the biogeographic pattern of murids is marked by several dispersal events toward the Australasian and the Palearctic regions. The Afrotropical region was also secondarily colonized at least three times from the Indomalaya, indicating that the latter region has acted as a major centre of diversification for the family.

Biogeographic patterns and diversification dynamics of the genus Cardiodactylus Saussure (Orthoptera, Grylloidea, Eneopterinae) in Southeast Asia.

Southeast Asia harbors an extraordinary species richness and endemism. While only covering 4% of the Earth's landmass, this region includes four of the planet's 34 biodiversity hotspots. Its complex geological history generated a megadiverse and highly endemic biota, attracting a lot of attention, especially in the field of island biogeography. Here we used the cricket genus Cardiodactylus as a model system to study biogeographic patterns in Southeast Asia. We carried out molecular analyses to: (1) infer phylogenetic relationships based on five mitochondrial and four nuclear markers, (2) estimate divergence times and infer biogeographical ancestral areas, (3) depict colonization routes, and summarize emigration and immigration events, as well as in situ diversification, and (4) determine whether shifts in species diversification occurred during the course of Cardiodactylus evolution. Our results support the monophyly of the genus and of one of its species groups. Dating and biogeographical analyses suggest that Cardiodactylus originated in the Southwest Pacific during the Middle Eocene. Our reconstructions indicate that Southeast Asia was independently colonized twice during the Early Miocene (ca. 19-16 Million years ago), and once during the Middle Miocene (ca. 13 Million years ago), with New Guinea acting as a corridor allowing westward dispersal through four different passageways: Sulawesi, the Philippines, Java and the Lesser Sunda Islands. Sulawesi also served as a diversification hub for Cardiodactylus through a combination of high immigration and in situ diversification events, which can be accounted for by the complex geological history of the Wallacea region.

A first higher-level time-calibrated phylogeny of antlions (Neuroptera: Myrmeleontidae).

In this study, we reconstruct the first time-calibrated phylogeny of the iconic antlion family, the Myrmeleontidae (Neuroptera: Myrmeleontiformia). We use maximum likelihood and Bayesian inference to analyse a molecular dataset based on seven mitochondrial and nuclear gene markers. The dataset encompasses 106 species of Neuroptera, including 94 antlion species. The resulting phylogenetic framework provides support for a myrmeleontid classification distinguishing four subfamilies: Acanthaclisinae, Myrmeleontinae, Palparinae, and Stilbopteryginae. Within Myrmeleontinae, Myrmecaelurini and Nemoleontini are recovered as monophyletic clades; Gepini also appears as a valid tribe, distinct from Myrmecaelurini whereas Myrmecaelurini and Nesoleontini on one hand and Brachynemurini and Dendroleontini on the other hand, appear closely related. Some preliminary information related to generic and specific levels are also implied from our results, such as the paraphyly of several genera. Dating analyses based on thoroughly evaluated fossil calibrations indicate that the antlion family likely originated in the Cretaceous, between 135 and 138 million years ago (depending on the set of fossil calibrations), and that all higher-level lineages appeared during the Early Cretaceous. This first phylogenetic hypothesis will provide a valuable basis to further expand the taxonomic coverage and molecular sampling, and to lay the foundations of future systematic revisions.

Global patterns of insect diversification: towards a reconciliation of fossil and molecular evidence?

Macroevolutionary studies of insects at diverse taxonomic scales often reveal dynamic evolutionary patterns, with multiple inferred diversification rate shifts. Responses to major past environmental changes, such as the Cretaceous Terrestrial Revolution, or the development of major key innovations, such as wings or complete metamorphosis are usually invoked as potential evolutionary triggers. However this view is partially contradicted by studies on the family-level fossil record showing that insect diversification was relatively constant through time. In an attempt to reconcile both views, we investigate large-scale insect diversification dynamics at family level using two distinct types of diversification analyses on a molecular timetree representing ca. 82% of the extant families, and reassess the insect fossil diversity using up-to-date records. Analyses focusing on the fossil record recovered an early burst of diversification, declining to low and steady rates through time, interrupted by extinction events. Phylogenetic analyses showed that major shifts of diversification rates only occurred in the four richest holometabolous orders. Both suggest that neither the development of flight or complete metamorphosis nor the Cretaceous Terrestrial Revolution environmental changes induced immediate changes in diversification regimes; instead clade-specific innovations likely promoted the diversification of major insect orders.

Deciphering the evolution of birdwing butterflies 150 years after Alfred Russel Wallace.

One hundred and fifty years after Alfred Wallace studied the geographical variation and species diversity of butterflies in the Indomalayan-Australasian Archipelago, the processes responsible for their biogeographical pattern remain equivocal. We analysed the macroevolutionary mechanisms accounting for the temporal and geographical diversification of the charismatic birdwing butterflies (Papilionidae), a major focus of Wallace's pioneering work. Bayesian phylogenetics and dating analyses of the birdwings were conducted using mitochondrial and nuclear genes. The combination of maximum likelihood analyses to estimate biogeographical history and diversification rates reveals that diversity-dependence processes drove the radiation of birdwings, and that speciation was often associated with founder-events colonizing new islands, especially in Wallacea. Palaeo-environment diversification models also suggest that high extinction rates occurred during periods of elevated sea level and global warming. We demonstrated a pattern of spatio-temporal habitat dynamics that continuously created or erased habitats suitable for birdwing biodiversity. Since birdwings were extinction-prone during the Miocene (warmer temperatures and elevated sea levels), the cooling period after the mid-Miocene climatic optimum fostered birdwing diversification due to the release of extinction. This also suggests that current global changes may represent a serious conservation threat to this flagship group.

Phylogenetic molecular species delimitations unravel potential new species in the pest genus Spodoptera Guenée, 1852 (Lepidoptera, Noctuidae).

Nowadays molecular species delimitation methods promote the identification of species boundaries within complex taxonomic groups by adopting innovative species concepts and theories (e.g. branching patterns, coalescence). As some of them can efficiently deal with large single-locus datasets, they could speed up the process of species discovery compared to more time consuming molecular methods, and benefit from the existence of large public datasets; these methods can also particularly favour scientific research and actions dealing with threatened or economically important taxa. In this study we aim to investigate and clarify the status of economically important moths species belonging to the genus Spodoptera (Lepidoptera, Noctuidae), a complex group in which previous phylogenetic analyses and integrative approaches already suggested the possible occurrence of cryptic species and taxonomic ambiguities. In this work, the effectiveness of innovative (and faster) species delimitation approaches to infer putative species boundaries has been successfully tested in Spodoptera, by processing the most comprehensive dataset (in terms of number of species and specimens) ever achieved; results are congruent and reliable, irrespective of the set of parameters and phylogenetic models applied. Our analyses confirm the existence of three potential new species clusters (for S. exigua (Hübner, 1808), S. frugiperda (J.E. Smith, 1797) and S. mauritia (Boisduval, 1833)) and support the synonymy of S. marima (Schaus, 1904) with S. ornithogalli (Guenée, 1852). They also highlight the ambiguity of the status of S. cosmiodes (Walker, 1858) and S. descoinsi Lalanne-Cassou & Silvain, 1994. This case study highlights the interest of molecular species delimitation methods as valuable tools for species discovery and to emphasize taxonomic ambiguities.

Evolution of Spermophagus seed beetles (Coleoptera, Bruchinae, Amblycerini) indicates both synchronous and delayed colonizations of host plants.

Seed beetles are a group of specialized chrysomelid beetles, which are mostly associated with plants of the legume family (Fabaceae). In the legume-feeding species, a marked trend of phylogenetic conservatism of host use has been highlighted by several molecular phylogenetics studies. Yet, little is known about the evolutionary patterns of association of species feeding outside the legume family. Here, we investigate the evolution of host use in Spermophagus, a species-rich seed beetle genus that is specialized on two non-legume host-plant groups: morning glories (Convolvulaceae) and mallows (Malvaceae: Malvoideae). Spermophagus species are widespread in the Old World, especially in the Afrotropical, Indomalaya and Palearctic regions. In this study we rely on eight gene regions to provide the first phylogenetic framework for the genus, along with reconstructions of host use evolution, estimates of divergence times and historical biogeography analyses. Like the legume-feeding species, a marked trend toward conservatism of host use is revealed, with one clade specializing on Convolvulaceae and the other on Malvoideae. Comparisons of plants' and insects' estimates of divergence times yield a contrasted pattern: on one hand a quite congruent temporal framework was recovered for morning-glories and their seed-predators; on the other hand the diversification of Spermophagus species associated with mallows apparently lagged far behind the diversification of their hosts. We hypothesize that this delayed colonization of Malvoideae can be accounted for by the respective biogeographic histories of the two groups.

A revision of the genus Conicofrontia Hampson (Lepidoptera, Noctuidae, Apameini, Sesamiina), with description of a new species: new insights from morphological, ecological and molecular data.

The aim of this study was to review the species of Conicofrontia Hampson, a small genus of noctuid stem borers (Noctuidae, Apameini) that is distributed in East and Southeastern Africa. We review the morphology of species in this group and provide new diagnoses and ecological data for five species. The following taxonomic changes are proposed: Hygrostola dallolmoi (Berio, 1973) (= Conicofrontia dallolmoi Berio, 1973) comb. n. and Conicofrontia bipartita (Hampson, 1910) (= Phragmatiphila bipartita Hampson, 1910) comb. n., stat. rev. One new species is also described: C. lilomwa, sp. n. from Tanzania. Wing patterns as well as male and female genitalia of the five species are described and illustrated. Finally we carried out molecular phylogenetic and molecular species delimitation analyses on a multi-marker dataset of 31 specimens and 15 species, including the five mentioned species. The results of molecular analyses provide a clear support for the proposed taxonomical changes.

Molecular phylogenetics, systematics and host-plant associations of the Bruchidius albosparsus (Fåhraeus) species group (Coleoptera, Chrysomelidae, Bruchinae) with the description of four new species.

Bruchidius Schilsky is a large paraphyletic genus of seed beetles (Coleoptera: Chrysomelidae: Bruchinae) which consists of multiple lineages that are usually associated with narrow sets of host-plants. In this study we focus on a group that mostly develops on wattle trees (acacias) belonging to the genus Vachellia Wight & Arn. This group originally included nine species and was designated as the Bruchidius centromaculatus (Allard) species group, but recent phylogenetic analyses revealed that these species belong to a much wider group of species with similar morphologies. For reasons of anteriority we call this enlarged group Bruchidius albosparsus (Fåhraeus). Here we review the morphology of species in this group and provide new diagnoses and ecological data for 10 species. The following combinations and synonymies are proposed: Bruchidius tanaensis (Pic, 1921) (= Bruchus tanaensis Pic, 1921) comb. nov. and Bruchidius albosparsus (Fåhraeus, 1839) (= Bruchus spadiceus Fåhraeus, 1839) syn. nov. Four new species are also described: B. eminingensis sp. nov., B. gerrardiicola sp. nov., B. glomeratus sp. nov. and B. haladai sp. nov. Finally we carried out molecular phylogenetic analyses on a multi-marker dataset of 59 specimens and 35 species, including 14 species from the group. The resulting trees allow us to confirm the monophyly of the group of interest and provide a more detailed picture of their evolutionary relationships.

Spodoptera frugiperda (Lepidoptera: Noctuidae) host-plant variants: two host strains or two distinct species?

The moth Spodoptera frugiperda is a well-known pest of crops throughout the Americas, which consists of two strains adapted to different host-plants: the first feeds preferentially on corn, cotton and sorghum whereas the second is more associated with rice and several pasture grasses. Though morphologically indistinguishable, they exhibit differences in their mating behavior, pheromone compositions, and show development variability according to the host-plant. Though the latter suggest that both strains are different species, this issue is still highly controversial because hybrids naturally occur in the wild, not to mention the discrepancies among published results concerning mating success between the two strains. In order to clarify the status of the two host-plant strains of S. frugiperda, we analyze features that possibly reflect the level of post-zygotic isolation: (1) first generation (F1) hybrid lethality and sterility; (2) patterns of meiotic segregation of hybrids in reciprocal second generation (F2), as compared to the meiosis of the two parental strains. We found a significant reduction of mating success in F1 in one direction of the cross and a high level of microsatellite markers showing transmission ratio distortion in the F2 progeny. Our results support the existence of post-zygotic reproductive isolation between the two laboratory strains and are in accordance with the marked level of genetic differentiation that was recovered between individuals of the two strains collected from the field. Altogether these results provide additional evidence in favor of a sibling species status for the two strains.

Taxonomy, host-plant associations and phylogeny of African Crotalaria-feeding seed beetles (Coleoptera, Chrysomelidae, Bruchinae): the Conicobruchus strangulatus (Fåhraeus) species group.

A small group of six morphologically related seed beetles (Coleoptera: Chrysomelidae: Bruchinae) belonging to the Conicobruchus genus is reviewed. Species in this group for which host-plants are known feed on various species of Crotalaria (Fabaceae, Crotalarieae). Here we provide diagnoses and a dichotomous key for all six species. The following synonymies are proposed: Conicobruchus cicatricosus (Fåhraeus, 1839) (= Bruchus cicatricosus pallidioripennis Pic, 1941) syn. nov.; Conicobruchus strangulatus (Fåhraeus, 1839) (= Bruchus hargreavesi Pic, 1933) syn. nov. The corresponding Conicobruchus strangulatus species group is hereby designated. New host-plant data are also included, which correspond to the results of recent collections of legume pods in East Africa. In addition we carried out molecular phylogenetic analyses on a representative sampling of Conicobruchus species (including the six species of interest). The latter allow us to assess the monophyly of the group of interest and to unravel their evolutionary relationships. Molecular phylogenetic analyses also indicate that at least two lineages of Conicobruchus successfully shifted toward Crotalarieae during the course of their diversification. 

Cretaceous environmental changes led to high extinction rates in a hyperdiverse beetle family.

BACKGROUND: As attested by the fossil record, Cretaceous environmental changes have significantly impacted the diversification dynamics of several groups of organisms. A major biome turnover that occurred during this period was the rise of angiosperms starting ca. 125 million years ago. Though there is evidence that the latter promoted the diversification of phytophagous insects, the response of other insect groups to Cretaceous environmental changes is still largely unknown. To gain novel insights on this issue, we assess the diversification dynamics of a hyperdiverse family of detritivorous beetles (Tenebrionidae) using molecular dating and diversification analyses. RESULTS: Age estimates reveal an origin after the Triassic-Jurassic mass extinction (older than previously thought), followed by the diversification of major lineages during Pangaean and Gondwanan breakups. Dating analyses indicate that arid-adapted species diversified early, while most of the lineages that are adapted to more humid conditions diversified much later. Contrary to other insect groups, we found no support for a positive shift in diversification rates during the Cretaceous; instead there is evidence for an 8.5-fold increase in extinction rates that was not compensated by a joint increase in speciation rates. CONCLUSIONS: We hypothesize that this pattern is better explained by the concomitant reduction of arid environments starting in the mid-Cretaceous, which likely negatively impacted the diversification of arid-adapted species that were predominant at that time.