Adaptive Introgression across Semipermeable Species Boundaries between Local Helicoverpa zea and Invasive Helicoverpa armigera Moths.

Hybridization between invasive and native species has raised global concern, given the dramatic increase in species range shifts and pest outbreaks due to anthropogenic dispersal. Nevertheless, secondary contact between sister lineages of local and invasive species provides a natural laboratory to understand the factors that determine introgression and the maintenance or loss of species barriers. Here, we characterize the early evolutionary outcomes following secondary contact between invasive Helicoverpa armigera and native H. zea in Brazil. We carried out whole-genome resequencing of Helicoverpa moths from Brazil in two temporal samples: during the outbreak of H. armigera in 2013 and 2017. There is evidence for a burst of hybridization and widespread introgression from local H. zea into invasive H. armigera coinciding with H. armigera expansion in 2013. However, in H. armigera, the admixture proportion and the length of introgressed blocks were significantly reduced between 2013 and 2017, suggesting selection against admixture. In contrast to the genome-wide pattern, there was striking evidence for adaptive introgression of a single region from the invasive H. armigera into local H. zea, including an insecticide resistance allele that increased in frequency over time. In summary, despite extensive gene flow after secondary contact, the species boundaries are largely maintained except for the single introgressed region containing the insecticide-resistant locus. We document the worst-case scenario for an invasive species, in which there are now two pest species instead of one, and the native species has acquired resistance to pyrethroid insecticides through introgression

A global phylogeny of butterflies reveals their evolutionary history, ancestral hosts and biogeographic origins

Butterflies are a diverse and charismatic insect group that are thought to have evolved with plants and dispersed throughout the world in response to key geological events. However, these hypotheses have not been extensively tested because a comprehensive phylogenetic framework and datasets for butterfly larval hosts and global distributions are lacking. We sequenced 391 genes from nearly 2,300 butterfly species, sampled from 90 countries and 28 specimen collections, to reconstruct a new phylogenomic tree of butterflies representing 92% of all genera. Our phylogeny has strong support for nearly all nodes and demonstrates that at least 36 butterfly tribes require reclassification. Divergence time analyses imply an origin similar to 100 million years ago for butterflies and indicate that all but one family were present before the K/Pg extinction event. We aggregated larval host datasets and global distribution records and found that butterflies are likely to have first fed on Fabaceae and originated in what is now the Americas. Soon after the Cretaceous Thermal Maximum, butterflies crossed Beringia and diversified in the Palaeotropics. Our results also reveal that most butterfly species are specialists that feed on only one larval host plant family. However, generalist butterflies that consume two or more plant families usually feed on closely related plants

Molecular advances to study the function, evolution and spectral tuning of arthropod visual opsins

Visual opsins of vertebrates and invertebrates diversified independently and converged to detect ultraviolet to long wavelengths (LW) of green or red light. In both groups, colour vision largely derives from opsin number, expression patterns and changes in amino acids interacting with the chromophore. Functional insights regarding invertebrate opsin evolution have lagged behind those for vertebrates because of the disparity in genomic resources and the lack of robust in vitro systems to characterize spectral sensitivities. Here, we review bioinformatic approaches to identify and model functional variation in opsins as well as recently developed assays to measure spectral phenotypes. In particular, we discuss how transgenic lines, cAMP-spectroscopy and sensitive heterologous expression platforms are starting to decouple genotype-phenotype relationships of LW opsins to complement the classical physiological-behavioural-phylogenetic toolbox of invertebrate visual sensory studies. We illustrate the use of one heterologous method by characterizing novel LW Gq opsins from 10 species, including diurnal and nocturnal Lepidoptera, a terrestrial dragonfly and an aquatic crustacean, expressing them in HEK293T cells, and showing that their maximum absorbance spectra (λmax) range from 518 to 611 nm. We discuss the advantages of molecular approaches for arthropods with complications such as restricted availability, lateral filters, specialized photochemistry and/or electrophysiological constraints. This article is part of the theme issue 'Understanding colour vision: molecular, physiological, neuronal and behavioural studies in arthropods'

Adaptive Introgression across Semipermeable Species Boundaries between Local Helicoverpa zea and Invasive Helicoverpa armigera Moths.

Hybridization between invasive and native species has raised global concern, given the dramatic increase in species range shifts and pest outbreaks due to anthropogenic dispersal. Nevertheless, secondary contact between sister lineages of local and invasive species provides a natural laboratory to understand the factors that determine introgression and the maintenance or loss of species barriers. Here, we characterize the early evolutionary outcomes following secondary contact between invasive Helicoverpa armigera and native H. zea in Brazil. We carried out whole-genome resequencing of Helicoverpa moths from Brazil in two temporal samples: during the outbreak of H. armigera in 2013 and 2017. There is evidence for a burst of hybridization and widespread introgression from local H. zea into invasive H. armigera coinciding with H. armigera expansion in 2013. However, in H. armigera, the admixture proportion and the length of introgressed blocks were significantly reduced between 2013 and 2017, suggesting selection against admixture. In contrast to the genome-wide pattern, there was striking evidence for adaptive introgression of a single region from the invasive H. armigera into local H. zea, including an insecticide resistance allele that increased in frequency over time. In summary, despite extensive gene flow after secondary contact, the species boundaries are largely maintained except for the single introgressed region containing the insecticide-resistant locus. We document the worst-case scenario for an invasive species, in which there are now two pest species instead of one, and the native species has acquired resistance to pyrethroid insecticides through introgression

Geogenomics of montane palms points to Miocene–Pliocene Andean segmentation related to strike‐slip tectonics

Aim: In geographically and ecologically heterogeneous landscapes, such as tropical mountains, widely distributed species may be informative proxies for studying landscape and climatic evolution. We explore historical vicariant and dispersal processes that may have determined the genetic structure and variation of a palm species complex living in cloud forests. We hypothesize that the genomic groupings reflect uplift-based isolation by vicariance, divergence via dispersal events driven by faulted montane segments or recent divergence due to climate fluctuations. Location: Colombian Andes. Taxon: Geonoma undata–G. orbignyana species complex (Arecaceae). Methods: We sampled 195 individuals of the species complex plus the outgroup (G. interrupta) across the three cordilleras of Colombia, the Colombian Massif and the Sierra Nevada de Santa Marta. We used target capture sequencing to generate a dataset of 12,750 quality-filtered genome-wide SNPs. We conducted phylogenetic, multivariate and population genomics and structure analyses to infer demographical history. Results: We found four genetically distinct groups within the species complex. The geographical distributions of the genetic groups, and their inferred phylogenetic and population divergence are consistent with a history of colonization of mountain segments that were disconnected until the late Pliocene. These breaks coincide with the distribution of Pliocene strike-slip faulting events. Main conclusions: The faulting and resultant topographic disruption of the northernmostAndean cordillera prior to the onset of the Pleistocene is implied by the presence of phylogeographic breaks in areas that are topographically continuous today. These cordilleras were formed by connecting segments that were previously uplifted but historically detached in areas where dense fault systems occur. Large-scale strike-slip faulting can generate topographic gaps, features that likely caused the divergence by dispersal with gene flow of the Geonoma undata–G. orbignyana complex

Convergent evolution of noxious heat sensing by TRPA5, a novel class of heat sensor in<i>Rhodnius prolixus</i>

Insects are ectotherms, and as such, rely on a diverse repertoire of thermoreceptors to monitor environmental temperature and control behavioral thermoregulation. Here, we use structural, phylogenetic, genetic, and functional analyses to show that TRPA5 genes, widespread across numerous insect orders, encode a novel class of noxious heat receptors. We show that in the triatomine bug Rhodnius prolixus, the primary vector of Chagas disease, Rp-TRPA5_2 differs biophysically and structurally from noxious thermoTRPAs previously described in insects. This includes key changes in the ankyrin repeat domain and the selectivity filter of the channel.In vitro, we find evidence that the homo-tetrameric channel is not activated by voltage, but displays high thermosensitivity with an enthalpy change (ΔH) of 72 kcal/mol associated with the channel activation, with a Q10= 25 and T°half= 58.6°C. Structural analyses reveal parallels in the overall ion channel architecture between fruit fly TRPA1 and Rp-TRPA5_2; however, functional properties and expression patterns indicate that the role of Rp-TRPA5_2 is more similar to that of Pyrexia noxious heat receptors found in fruit flies. Pyrexia genes have been lost in true bugs, and our findings suggest that the rapidly evolving insect TRPA gene family has given rise to an independent evolutionary origin of a molecular transducer that is responsive to noxious thermal stimuli

The evolution of red color vision is linked to coordinated rhodopsin tuning in lycaenid butterflies.

Color vision has evolved multiple times in both vertebrates and invertebrates and is largely determined by the number and variation in spectral sensitivities of distinct opsin subclasses. However, because of the difficulty of expressing long-wavelength (LW) invertebrate opsins in vitro, our understanding of the molecular basis of functional shifts in opsin spectral sensitivities has been biased toward research primarily in vertebrates. This has restricted our ability to address whether invertebrate Gq protein-coupled opsins function in a novel or convergent way compared to vertebrate Gt opsins. Here we develop a robust heterologous expression system to purify invertebrate rhodopsins, identify specific amino acid changes responsible for adaptive spectral tuning, and pinpoint how molecular variation in invertebrate opsins underlie wavelength sensitivity shifts that enhance visual perception. By combining functional and optophysiological approaches, we disentangle the relative contributions of lateral filtering pigments from red-shifted LW and blue short-wavelength opsins expressed in distinct photoreceptor cells of individual ommatidia. We use in situ hybridization to visualize six ommatidial classes in the compound eye of a lycaenid butterfly with a four-opsin visual system. We show experimentally that certain key tuning residues underlying green spectral shifts in blue opsin paralogs have evolved repeatedly among short-wavelength opsin lineages. Taken together, our results demonstrate the interplay between regulatory and adaptive evolution at multiple Gq opsin loci, as well as how coordinated spectral shifts in LW and blue opsins can act together to enhance insect spectral sensitivity at blue and red wavelengths for visual performance adaptation