Biology subjects

Kawahara, A. Y.

Publications and source records attributed to Kawahara, A. Y..

34 records · Page 2Linked to original sources

bioRxiv2022

Effect of Behavioral Conditions on Silk Characteristics in the Indian Meal Moth (Plodia interpunctella)

Lepidopteran silks are produced during the larval stage and are used for mobility and protection from predators, parasitoids, and pathogens. Our knowledge of silk structure and production in Lepidoptera is based largely on the biology of the domestic silk moth (Bombyx mori), but recent comparative evidence suggests that silk production and structure vary widely across moth taxa. Some species like the Indian meal moth (Plodia interpunctella) are becoming important biological models to study silk for its potential application to materials science and medicine, but many aspects of silk production in this species remain unknown. Here we characterize the silk of P. interpunctella by measuring the width of wandering and pupal silk strands and find that pupal silk is significantly thicker than the latter. We then report individual variation in pupal silk production in our lab-reared colony with a very small number of individuals forgoing pupal silk (< 4%) and find that overcrowding had no effect on this, whereas exposure to elevated temperatures reduced rates of pupal silk production.

zoology↗

bioRxiv2022

Diversification is correlated with temperature in white and sulfur butterflies

Temperature is thought to be a key variable explaining global patterns of species richness. However, to investigate this relationship carefully, it is necessary to study clades with broad geographic ranges that are comprised of species inhabiting diverse biomes with well- characterized species ranges. In the present study, we investigate the link between temperature and diversification in the butterfly family Pieridae (sulfurs and whites) by combining Next Generation sequences and published molecular data with fine-grained distribution information. After building the most comprehensive phylogeny of the group, with almost 600 species and all higher taxa (subfamilies, tribes and subtribes), we found strong support for the following relationships within the family: Dismorphiinae + (Coliadinae + (Pseudopontiinae + Pierinae)). With a curated distribution dataset of over 800,000 occurrences, we conducted multiple comparative phylogenetic analyses that provided strong evidence that species in environments with more stable daily temperatures or with cooler maximum temperatures in the warm seasons have higher diversification rates. We also found a positive correlation between speciation and extinction with paleotemperature: as global temperature decreased through geological time, so did diversification rates. Although many studies demonstrate higher diversity in the tropics, we have been able to identify specific climate variables associated with changes in diversification, while also inferring the most robust and well sampled phylogenomic framework for Pieridae to date.

evolutionary biology↗

bioRxiv2022

Long-read HiFi Sequencing Correctly Assembles Repetitive heavy fibroin Silk Genes in New Moth and Caddisfly Genomes

Insect silk is an incredibly versatile biomaterial. Lepidoptera and their sister lineage, Trichoptera, display some of the most diverse uses of silk with varying strength, adhesive qualities and elastic properties. It is well known that silk fibroin genes are long (> 20 kb) and have many repetitive motifs. These features make these genes challenging to sequence. Most research thus far has focused on conserved N- and C-terminal regions of fibroin genes because a full comparison of repetitive regions across taxa has not been possible. Using the PacBio Sequel II system and SMRT sequencing, we generated high fidelity (HiFi) long-read genomic and transcriptomic sequences for the Indianmeal moth (Plodia interpunctella) and genomic sequences for the caddisfly, Eubasilissa regina. Both genomes were highly contiguous (N50 = 9.7 Mbp/32.4 Mbp, L50 = 13/11) and complete (BUSCO Complete = 99.3%/95.2%), with complete and contiguous recovery of silk heavy fibroin gene sequences. This study demonstrates that HiFi long-read sequencing can significantly help our understanding of genes with highly contiguous, repetitive regions.

genomics↗

bioRxiv2022

Evolution and diversification dynamics of butterflies

Butterflies are a diverse and charismatic insect group that are thought to have diversified via coevolution with plants and in response to dispersals following key geological events. These hypotheses have been poorly tested at the macroevolutionary scale because a comprehensive phylogenetic framework and datasets on global distributions and larval hosts of butterflies are lacking. We sequenced 391 genes from nearly 2,000 butterfly species to construct a new, phylogenomic tree of butterflies representing 92% of all genera and aggregated global distribution records and larval host datasets. We found that butterflies likely originated in what is now the Americas, [~]100 Ma, shortly before the Cretaceous Thermal Maximum, then crossed Beringia and diversified in the Paleotropics. The ancestor of modern butterflies likely fed on Fabaceae, and most extant families were present before the K/Pg extinction. The majority of butterfly dispersals occurred from the tropics (especially the Neotropics) to temperate zones, largely supporting a "cradle" pattern of diversification. Surprisingly, host breadth changes and shifts to novel host plants had only modest impacts.

evolutionary biology↗

bioRxiv2021

Anti-Bat Ultrasound Production in Moths is Globally and Phylogenetically Widespread

Warning signals are well known in the visual system, but rare in other modalities. Some moths produce ultrasonic sounds to warn bats of noxious taste or to mimic unpalatable models. Here we report results from a long-term study across the globe, assaying moth response to playback of bat echolocation. We tested 252 genera, spanning most families of large-bodied moths, and outline anti-bat ultrasound production in 52 genera, with eight new subfamily origins described. Based on acoustic analysis of ultrasonic emissions and palatability experiments with bats, it seems that acoustic warning and mimicry are the raison detre for sound production in most moths. However, some moths use high-density ultrasound capable of jamming bat sonar. In fact, we find preliminary evidence of independent origins of sonar jamming in at least six subfamilies. Palatability data indicates that jamming and warning are not mutually exclusive strategies. To explore the possible organization of anti-bat warning sounds into acoustic mimicry rings, we intensively studied a community of moths in Ecuador and found five distinct acoustic clusters using machine learning algorithms. While these data represent an early understanding of acoustic aposematism and mimicry across this megadiverse insect order, it is likely that ultrasonically-signaling moths comprise one of the largest mimicry complexes on earth.

evolutionary biology↗

bioRxiv2021

An inexpensive setup for robust activity tracking in small animals: Portable Locomotion Activity Monitor (pLAM)

O_LIAdvances in computer vision and deep learning have automated animal behaviour studies that previously required tedious manual input. However, tracking activity of small and fast flying animals remains a hurdle, especially in a field setting with variable light conditions. Commercial locomotor activity monitors (LAMs) can be expensive, closed source, and generally limited to laboratory settings. C_LIO_LIHere, we present a portable locomotion activity monitor (pLAM), a mobile activity detector to quantify small animal circadian activity. Our setup uses inexpensive components, is based on open-source motion tracking software, and is easy to assemble and use in the field. It runs off-grid, supports low-light tracking with infrared lights, and can implement arbitrary light cycle colours and brightnesses with programmable LEDs. We provide a user-friendly guide to assembling pLAM hardware and accessing its pre-configured software and guidelines for using it in other systems. C_LIO_LIWe benchmarked pLAM for insects under various lab and field conditions, then compared results to a commercial activity detector. They offer broadly similar activity measures, but our setup captures flight and bouts of motion that are often missed by beam-breaking activity detection. C_LIO_LIpLAM will enable high-throughput quantification of small animal location and activity in a low-cost and accessible manner, crucial to studying behaviour that can help inform conservation and management decisions. C_LI

animal behavior and cognition↗

bioRxiv2021

Adaptive shifts underlie the divergence in wing morphology in bombycoid moths

The evolution of flapping flight is linked to the prolific success of insects. Across Insecta, wing morphology diversified, strongly impacting aerodynamic performance. In the presence of ecological opportunity, discrete adaptive shifts and early bursts are two processes hypothesized to give rise to exceptional morphological diversification. Here, we use the sister-families Sphingidae and Saturniidae to answer how the evolution of aerodynamically important traits is linked to clade divergence and through what process(es) these traits evolve. Many agile Sphingidae evolved hover-feeding behaviors, while adult Saturniidae lack functional mouth parts and rely on a fixed energy budget as adults. We find that Sphingidae underwent an adaptive shift in wing morphology coincident with life history and behavior divergence, evolving small high aspect-ratio wings advantageous for power reduction that can be moved at high frequencies, beneficial for flight control. In contrast, Saturniidae, which do not feed as adults, evolved large wings and morphology which surprisingly does not reduce aerodynamic power, but could contribute to their erratic flight behavior, aiding in predator avoidance. We suggest that after the evolution of flapping flight, diversification of wing morphology can be potentiated by adaptative shifts, shaping the diversity of wing morphology across insects.

evolutionary biology↗

bioRxiv2020

Measuring Compound Eye Optics with Microscope and MicroCT Images

With a great variety of shapes and sizes, compound eye morphologies give insight into visual ecology, development, and evolution, and inspire novel engineering. In contrast to our own camera-type eyes, compound eyes reveal their resolution, sensitivity, and field of view externally, provided they have spherical curvature and orthogonal ommatidia. Non-spherical compound eyes with skewed ommatidia require measuring internal structures, such as with MicroCT (CT). Thus far, there is no efficient tool to characterize compound eye optics, from either 2D or 3D data, automatically. Here we present two open-source programs: (1) the ommatidia detecting algorithm (ODA), which measures ommatidia count and diameter in 2D images, and (2) a CT pipeline (ODA-3D), which calculates anatomical acuity, sensitivity, and field of view across the eye by applying the ODA to 3D data. We validate these algorithms on images, images of replicas, and CT eye scans from ants, fruit flies, moths, and a bee.

neuroscience↗

bioRxiv2020

Population differentiation and structural variation in the genome of Manduca sexta across the United States

Many species that are extensively studied in the laboratory are less well characterized in their natural habitat, and laboratory strains represent only a small fraction of the variation in a species genome. Here we investigate genomic variation in three natural North American populations of an agricultural pest and a model insect for many scientific disciplines, the tobacco hornworm (Manduca sexta). We show that hornworms from Arizona, Kansas, and North Carolina are genetically distinct, with Arizona being particularly differentiated from the other two populations using Illumina whole-genome resequencing. Peaks of differentiation exist across the genome, but here we focus in on the most striking regions. In particular, we identify two likely segregating inversions found in the Arizona population. One inversion on the Z chromosome may enhance adaptive evolution of the sex chromosome. The larger, autosomal inversion contains a pseudogene may be involved in the exploitation of a novel hostplant in Arizona, but functional genetic assays will be required to support this hypothesis. Nevertheless, our results reveal undiscovered natural variation and provide useful genomic data for both pest management and evolutionary genetics of this insect species.

evolutionary biology↗

bioRxiv2020

Wing shape evolution in bombycoid moths reveals two distinct strategies for maneuverable flight

Across insects, wing shape and size have undergone dramatic divergence even in closely related sister groups, but we do not yet know morphology changes in tandem with kinematics to support body weight within available aerodynamic power and how the specific force production patterns are linked to changes in behavior. Hawkmoths and wild silkmoths are two such diverse sister families with divergent wing morphology. Using 3d kinematics and quasi-steady aerodynamic modeling, we compare the aerodynamics and the contributions of wing shape, size, and kinematics in 10 moth species. We find that wing movement also diverges between the clades and underlies two distinct strategies for flight. Hawkmoths use wing kinematics, especially high frequencies, to enhance force, but wing morphologies that reduces power. Silkmoths use wing morphology to enhance force, and high amplitude wingstrokes to reduce power. Both strategies converge on similar aerodynamic power and can support similar body mass ranges, but their within-wingstroke force profiles are quite different and linked to the hovering flight of hawkmoths and the bobbing flight of silkmoths. These two groups of moths each fly more like other, distantly related insects than they do each other, demonstrating the convergence and diversity of flapping flight evolution.

physiology↗

bioRxiv2020

Spatial phylogenetics of butterflies in relation to environmental drivers and angiosperm diversity across North America

Broad-scale quantitative assessments of biodiversity and the factors shaping it remain particularly poorly explored in insects. Here, we undertook a spatial phylogenetic analysis of North American butterflies via assembly of a time-calibrated phylogeny of the region coupled with a unique, complete range assessment for ~75% of the known species. We utilized a suite of phylodiversity metrics and associated environmental data to test whether climate stability and temperature gradients have shaped North American butterfly phylogenetic diversity and endemism. We also undertook the first direct, quantitative comparisons of spatial phylogenetic patterns between butterflies and flowering plants in North America. We expected concordance between butterflies and angiosperms based on both shared historical environmental drivers and presumed strong butterfly-host plant specializations. We instead found that biodiversity patterns in butterflies are strikingly different from flowering plants in some regions of the continent. In particular, the warm desert regions of the southwestern United States and Mexico showed surprisingly high butterfly phylogenetic diversity and endemism, in contrast to much lower values for angiosperms. Butterflies did not show patterns of phylogenetic clustering as found in flowering plants, suggesting differences in habitat conservation between the two groups. Finally, we found weak relationships and spatially structured biases in relative branching timing between angiosperms and butterflies. These results suggest that shared biogeographic histories and trophic associations do not necessarily assure similar diversity outcomes. The work has applied value in conservation planning, documenting warm deserts as an important North American butterfly biodiversity hotspot.

ecology↗

bioRxiv2020

Evolution of body size and wing shape trade-offs in arsenurine silkmoths

AO_SCPLOWBSTRACTC_SCPLOWOne of the key objectives in biological research is understanding how evolutionary processes have produced Earths biodiversity. These processes have led to a vast diversity of wing shapes in insects; an unanswered question especially pronounced in moths. As one of the major predators of nocturnal moths, bats are thought to have been involved in a long evolutionary arms race with their prey. In response, moths are thought to have evolved many counter strategies, such as diverse wing shapes and large body sizes. However, the tradeoffs between body size and wing shape are not well understood. Here we examined the evolution of wing shape in the wild silkmoth subfamily Arsenurinae (Saturniidae). By using phylogenomics and geometric morphometrics, we established the framework to evaluate potential evolutionary relationships between body size and wing shape. The phylogeny was inferred based on 781 loci from target capture data of 42 arsenurine species representing all 10 recognized genera. We found there are evolutionary trade-offs between body size, wing shape, and the interaction of fore- and hindwing shape. Namely, body size decreases with increasing hindwing length, but increases as forewing shape becomes more complex. Additionally, hindwing shape has a significant effect on forewing shape complexity. The complex wing shapes that make Arsenurinae, and silkmoths as a whole, so charismatic are likely driven by the strong forces of natural selection and genomic constraints. One other important outcome was discovering within our data one of the most vexing problems in phylogenetic inference - a region of a tree that possesses short branches and no "support" for relationships (i.e., a polytomy). These parts of the Tree of Life are often some of the most interesting from an evolutionary standpoint. To investigate this problem, we used reciprocal illumination to determine the most probable generic relationships within the Arsenurinae by inspecting differing phylogenetic inferences, alternative support values, quartets, and phylogenetic networks to reveal hidden phylogenetic signal.

evolutionary biology↗

bioRxiv2020

The latitudinal diversity gradient in brush-footed butterflies (Nymphalidae): conserved ancestral tropical niche but different continental histories.

The latitudinal diversity gradient (LDG) is arguably one of the most striking patterns in nature. The global increase in species richness toward the tropics across continents and taxonomic groups stimulated the formulation of many hypotheses to explain the underlying mechanisms of this pattern. We evaluated several of these hypotheses to explain spatial diversity patterns in the butterfly family, Nymphalidae, by assessing the contributions of speciation, extinction, and dispersal to the LDG, and also the extent to which these processes differ among regions at the same latitude. We generated a new, time-calibrated phylogeny of Nymphalidae based on 10 gene fragments and containing ca. 2,800 species ([~]45% of extant diversity). Neither speciation nor extinction rate variations consistently explain the LDG among regions because temporal diversification dynamics differ greatly across longitude. For example, we found that Neotropical nymphalid diversity results from low extinction rates, not high speciation rates, and that biotic interchanges with other regions were rare. Southeast Asia was also characterized by a low speciation rate but, unlike the Neotropics, was the main source of dispersal events through time. Our results suggest that global climate change throughout the Cenozoic, particularly during the Eocene-Oligocene transition, combined with the conserved ancestral tropical niches, played a major role in generating the modern LDG of butterflies.

ecology↗

bioRxiv2020

Light environment drives evolution of color vision genes in butterflies and moths.

Opsins are the primary light-sensing molecules in animals. Opsins have peak sensitivities to specific wavelengths which allows for color discrimination. The opsin protein family has undergone duplications and losses, dynamically expanding and contracting the number of opsins, throughout invertebrate evolution, but it is unclear what drives this diversity. Light availability, however, appears to play a significant role. Dim environments are associated with low opsin diversity in deep-sea fishes and cave-dwelling animals. Correlations between high opsin diversity and bright environments, however, are tenuous. Insects are a good system to test whether opsin expansion is associated with greater light availability because they are enormously diverse and consequently display large variation in diel activity. To test this, we used 200 insect transcriptomes and examined the patterns of opsin diversity associated with diel-niche. We focused on the butterflies and moths (Lepidoptera) because this group has significant variation in diel-niche, substantial opsin recovery (n=100), and particularly well-curated transcriptomes. We identified opsin duplications using ancestral state reconstruction and examined rates of opsin evolution, and compared them across diel-niches. We find Lepidoptera species active in high light environments have independently expanded their opsins at least 10 times. Opsins from diurnal taxa also evolve faster; 13 amino acids were identified across different opsins that were under diversifying selection. Structural models reveal that four of these amino acids overlap with opsin color-tuning regions. By parsing nocturnal and diurnal switches, we show that light environment can influence gene diversity, selection, and protein structure of opsins in Lepidoptera.

evolutionary biology↗

bioRxiv2019

Phylogenetic synecdoche demonstrates optimality of subsampling and improves recovery of the Blaberoidea phylogeny

Phylogenomics seeks to use next-generation data to robustly infer an organisms evolutionary history. Yet, the practical caveats of phylogenomics motivates investigation of improved efficiency, particularly when quality of phylogenies are questionable. To achieve improvements, one goal is to maintain or enhance the quality of phylogenetic inference while severely reducing dataset size. We approach this goal by designing an optimized subsample of data with an experimental design whose results are determined on the basis of phylogenetic synecdoche - a comparison of phylogenies inferred from a subsample to phylogenies inferred from the entire dataset. We examine locus mutation rate, saturation, evolutionary divergence, rate heterogeneity, selection, and a priori information content as traits that may determine optimality. Our controlled experimental design is based on 265 loci for 102 blaberoidean cockroaches and 22 outgroup species. High phylogenetic utility is demonstrated by loci with high mutation rate, low saturation, low sequence distance, low rate heterogeneity, and low selection. We found that some phylogenetic information content estimators may not be meaningful for assessing information content a priori. We use these findings to design concatenated datasets with an optimized subsample of 100 loci. The tree inferred from the optimized subsample alignment was largely identical to that inferred from all 265 loci but with less evidence of long branch attraction and improved statistical support. In sum, optimized subsampling can improve tree quality while reducing data collection costs and yielding 4-6x improvements to computation time in tree inference and bootstrapping.

evolutionary biology↗

bioRxiv2019

Phylogenomics reveals major diversification rate shifts in the evolution of silk moths and relatives

The silkmoths and their relatives (Bombycoidea) are an ecologically and taxonomically diverse superfamily that includes some of the most charismatic species of all the Lepidoptera. Despite displaying some of the most spectacular forms and ecological traits among insects, relatively little attention has been given to understanding their evolution and the drivers of their diversity. We heavily sampled (both in taxa and loci) all major lineages of the Bombycoidea, producing a well-supported phylogeny that identified important evolutionary patterns (e.g., morphology, biogeography, and differences in speciation and extinction). Importantly, analysis of diversification rates highlights the stark increases that exist within the Sphingidae (hawkmoths) and Saturniidae (wild silkmoths). We postulate that these rate shifts are due to differences in the intense selective pressures from insectivorous bats. The study also introduces a new Bombycoidea-specific Anchored Hybrid Enrichment (AHE) probe set, a modified DNA extraction protocol for Lepidoptera specimens from natural history collections, and additional information on the existing AHE bioinformatics pipeline. Our research highlights the flexibility of AHE to generate genomic data from a wide range of museum specimens, both age and preservation method, and will allow researchers to tap into the wealth of biological data residing in natural history collections around the globe.

evolutionary biology↗