Most isolates of human rhinovirus, the common cold virus, replicate more robustly at the cool temperatures found in the nasal cavity (33-35°C) than at core body temperature (37°C). To gain insight into the mechanism of temperature-dependent growth, we compared the transcriptional response of primary mouse airway epithelial cells infected with rhinovirus at 33°C vs. 37°C. Mouse airway cells infected with mouse-adapted rhinovirus 1B exhibited a striking enrichment in expression of antiviral defense response genes at 37°C relative to 33°C, which correlated with significantly higher expression levels of type I and type III IFN genes and IFNstimulated genes (ISGs) at 37°C. Temperature-dependent IFN induction in response to rhinovirus was dependent on the MAVS protein, a key signaling adaptor of the RIG-I-like receptors (RLRs). Stimulation of primary airway cells with the synthetic RLR ligand poly I:C led to greater IFN induction at 37°C relative to 33°C at early time points poststimulation and to a sustained increase in the induction of ISGs at 37°C relative to 33°C. Recombinant type I IFN also stimulated more robust induction of ISGs at 37°C than at 33°C. Genetic deficiency of MAVS or the type I IFN receptor in infected airway cells permitted higher levels of viral replication, particularly at 37°C, and partially rescued the temperature-dependent growth phenotype. These findings demonstrate that in mouse airway cells, rhinovirus replicates preferentially at nasal cavity temperature due, in part, to a less efficient antiviral defense response of infected cells at cool temperature.is the most frequent cause of the common cold and has recently been recognized as the most frequent cause of exacerbations of asthma, a disease affecting ∼10% of the US population (1, 2). RV is also increasingly recognized to be a major cause of lung symptoms in patients with other chronic respiratory diseases and in young children (3). Previously, RV was thought to cause disease primarily in the nasal cavity, consistent with the observation that most RV strains replicate more robustly at the cooler temperatures found in the nasal cavity (33-35°C) than at lung temperature (37°C) (4, 5). However, the recent recognition that RV is an important cause of disease in the lung (2, 3) compels further investigation of the mechanisms that control the optimal replication temperature of this virus, which are unknown.Previous studies of the replication machinery of RV have not identified a virus-intrinsic reason for temperature-dependent growth, including studies of cell entry, uncoating, and polymerase activity (6, 7). Therefore, we considered the possibility that other factors, such as temperature-dependent host antiviral responses, might contribute to this phenotype. To investigate this possibility, we examined the effect of incubation temperature on the response to RV infection by the infected host cell. Using a mouse primary airway cell infection model, we observed that incubating cells at the lower temperature of the nasal cavity (33°C) greatly dim...
Some eyespots are thought to deflect attack away from the vulnerable body, yet there is limited empirical evidence for this function and its adaptive advantage. Here, we demonstrate the conspicuous ventral hindwing eyespots found on Bicyclus anynana butterflies protect against invertebrate predators, specifically praying mantids. Wet season (WS) butterflies with larger, brighter eyespots were easier for mantids to detect, but more difficult to capture compared to dry season (DS) butterflies with small, dull eyespots. Mantids attacked the wing eyespots of WS butterflies more frequently resulting in greater butterfly survival and reproductive success. With a reciprocal eyespot transplant, we demonstrated the fitness benefits of eyespots were independent of butterfly behaviour. Regardless of whether the butterfly was WS or DS, large marginal eyespots pasted on the hindwings increased butterfly survival and successful oviposition during predation encounters. In previous studies, DS B. anynana experienced delayed detection by vertebrate predators, but both forms suffered low survival once detected. Our results suggest predator abundance, identity and phenology may all be important selective forces for B. anynana. Thus, reciprocal selection between invertebrate and vertebrate predators across seasons may contribute to the evolution of the B. anynana polyphenism.
Bodies are often made of repeated units, or serial homologs, that develop using the same core gene regulatory network. Local inputs and modifications to this network allow serial homologs to evolve different morphologies, but currently we do not understand which modifications allow these repeated traits to evolve different levels of phenotypic plasticity. Here we describe variation in phenotypic plasticity across serial homologous eyespots of the butterfly Bicyclus anynana, hypothesized to be under selection for similar or different functions in the wet and dry seasonal forms. Specifically, we document the presence of eyespot size and scale brightness plasticity in hindwing eyespots hypothesized to vary in function across seasons, and reduced size plasticity and absence of brightness plasticity in forewing eyespots hypothesized to have the same function across seasons. By exploring the molecular and physiological causes of this variation in plasticity across fore and hindwing serial homologs we discover that: 1) temperature experienced during the wandering stages of larval development alters titers of an ecdysteroid hormone, 20-hydroxyecdysone (20E), in the hemolymph of wet and dry seasonal forms at that stage; 2) the 20E receptor (EcR) is differentially expressed in the forewing and hindwing eyespot centers of both seasonal forms during this critical developmental stage; and 3) manipulations of EcR signaling disproportionately affected hindwing eyespots relative to forewing eyespots. We propose that differential EcR expression across forewing and hindwing eyespots at a critical stage of development explains the variation in levels of phenotypic plasticity across these serial homologues. This finding provides a novel signaling pathway, 20E, and a novel molecular candidate, EcR, for the regulation of levels of phenotypic plasticity across body parts or serial homologs.
Discovering the mechanisms that underlie the origin of novel features represents a major frontier in developmental and evolutionary biology. Here we begin to characterize the role of the Hox gene Sex combs reduced (Scr) during the development and evolution of a morphologically novel trait: beetle horns. Beetle horns develop as epidermal outgrowths from the prothorax and/or head, and size and location vary dramatically across species and between sexes. Using both comparative gene expression and larval RNA interference in two species of the horned beetle genus Onthophagus, we show that Scr functions in patterning adult labial mouthpart identity and suppressing wing development in the prothorax. At the same time, however, our results illustrate that Scr has acquired, within its ancestral domain of expression, additional new functions including the regulation of prepupal growth and pupal remodeling of pronotal horn primordia. Furthermore, comparative analyses of our results across both Onthophagus species, which differ in location of horn development (thoracic horns vs. thoracic and head horns) as well as patterns of sexual dimorphism (traditional vs. reversed sexual dimorphism), reveal surprising differences in exactly when, where, and to what degree Scr regulates horn formation in different sexes. These observations suggest that the interactions between Scr and its targets in the regulation of horn development can diversify quickly over remarkably short phylogenetic distances. More generally, our results suggest that the Hox complex can play an integral role in the development and evolution of novel complex traits while maintaining traditional patterning responsibilities.
Brilliant animal colors often are produced from light interacting with intricate nano-morphologies present in biological materials such as butterfly wing scales. Surveys across widely divergent butterfly species have identified multiple mechanisms of structural color production; however, little is known about how these colors evolved. Here, we examine how closely related species and populations of Bicyclus butterflies have evolved violet structural color from brown-pigmented ancestors with UV structural color. We used artificial selection on a laboratory model butterfly, B. anynana, to evolve violet scales from UV brown scales and compared the mechanism of violet color production with that of two other Bicyclus species, Bicyclus sambulos and Bicyclus medontias, which have evolved violet/blue scales independently via natural selection. The UV reflectance peak of B. anynana brown scales shifted to violet over six generations of artificial selection (i.e., in less than 1 y) as the result of an increase in the thickness of the lower lamina in ground scales. Similar scale structures and the same mechanism for producing violet/blue structural colors were found in the other Bicyclus species. This work shows that populations harbor large amounts of standing genetic variation that can lead to rapid evolution of scales' structural color via slight modifications to the scales' physical dimensions.thin film | constructive interference | parallel evolution | photonics O rganisms produce colors in two basic ways: by synthesizing pigments that selectively absorb light of certain spectral bands so that only light outside the absorption bands is backscattered (chemical color) or by developing nanomorphologies that enhance the reflection of light of certain wavelengths by interference (physical color or structural color). Structural colors play major roles in natural and sexual selection in many species (1) and have a broad range of applications in color display, paint, cosmetics, and textile industries (2). Structural color surveys across widely divergent species have revealed a large diversity of color-producing mechanisms (3-9). However, there has been a lack of systematic study and comparison of how different colors from closely related species or within populations of a single species evolve, even though these colors can vary dramatically. By examining how these species/populations evolve different colors, it is possible to identify the minimal amount of morphological change that results in significant color variation. Furthermore, this research may serve as an inspiration for future application of similar evolutionary principles to the design of photonic devices for color tuning, light trapping, or beam steering (2,(10)(11)(12)(13)(14)(15)(16)(17)(18)(19)(20). From an evolutionary biology point of view, we are curious to examine how structural colors respond to selection pressure and whether there is sufficient standing genetic variation in natural populations to allow the rapid evolution of novel colors. Here we focus on d...
The mycalesine butterfly Bicyclus anynana, the “Squinting bush brown,” is a model organism in the study of lepidopteran ecology, development, and evolution. Here, we present a draft genome sequence for B. anynana to serve as a genomics resource for current and future studies of this important model species. Seven libraries with insert sizes ranging from 350 bp to 20 kb were constructed using DNA from an inbred female and sequenced using both Illumina and PacBio technology; 128 Gb of raw Illumina data was filtered to 124 Gb and assembled to a final size of 475 Mb (∼×260 assembly coverage). Contigs were scaffolded using mate-pair, transcriptome, and PacBio data into 10 800 sequences with an N50 of 638 kb (longest scaffold 5 Mb). The genome is comprised of 26% repetitive elements and encodes a total of 22 642 predicted protein-coding genes. Recovery of a BUSCO set of core metazoan genes was almost complete (98%). Overall, these metrics compare well with other recently published lepidopteran genomes. We report a high-quality draft genome sequence for Bicyclus anynana. The genome assembly and annotated gene models are available at LepBase (http://ensembl.lepbase.org/index.html).
Studies focusing on the development of morphological novelties suggest that patterning genes underlying traditional appendage development (i.e. mouthparts, legs, and wings) also play important roles in patterning novel morphological structures. In this study, we examine whether the expression and function of a member of the TGF-β signaling pathway, decapentaplegic (dpp), promotes development of a morphologically novel structure: beetle horns. Beetle horns are complex secondary sexual structures that develop in the head and/or prothorax, lack obvious homology to other insect outgrowths, and vary remarkably between species and sexes. We studied dpp expression through in situ hybridization, performed functional analyses with RNA interference, and gathered allometric measurements to determine the role of dpp during both pronotal and head horn development in both sexes of two morphologically dissimilar species in the Onthophagus genus, Onthophagus binodis and Onthophagus sagittarius. Our findings show that in addition to affecting growth and patterning of traditional appendages, dpp regulates beetle horn growth and remodeling.
In contrast to the important role of hormones in the development of sexual traits in vertebrates (Cox RM, Stenquist DS, Calsbeek R. 2009. Testosterone, growth and the evolution of sexual size dimorphism. J Evol Biol. 22(8):1586–1598.), the differentiation of these traits in insects is attributed almost exclusively to cell-autonomous mechanisms controlled by members of the sex determination pathway (Verhulst EC, van de Zande L. 2015. Double nexus – doublesex is the connecting element in sex determination. Brief Funct Genomics 14(6):396–406.), such as doublesex. Although hormones can shape the development of sexual traits in insects, variation in hormone levels are not conclusively known to cause dimorphism in these traits (Prakash A, Monteiro A. 2016. Molecular mechanisms of secondary sexual trait development in insects. Curr Opin Insect Sci. 17:40–48.). Here, we show that butterflies use sex-specific differences in 20-hydroxyecdysone hormone titers to create sexually dimorphic wing ornaments. Females of the dry season (DS) form of Bicyclus anynana display a larger sexual ornament on their wings than males, whereas in the wet season form both sexes have similarly sized ornaments (Prudic KL, Jeon C, Cao H, Monteiro A. 2011. Developmental plasticity in sexual roles of butterfly species drives mutual sexual ornamentation. Science 331(6013):73–75.). High levels of circulating 20-hydroxyecdysone during larval development in DS females and wet season forms cause proliferation of the cells fated to give rise to this wing ornament, and results in sexual dimorphism in the DS forms. This study advances our understanding of how the environment regulates sex-specific patterns of plasticity of sexual ornaments and conclusively shows that hormones can play a role in the development of secondary sexual traits in insects, just like they do in vertebrates.
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