Insect outbreaks are expected to increase in frequency and intensity with projected changes in global climate through direct effects of climate change on insect populations and through disruption of community interactions. Although there is much concern about mean changes in global climate, the impact of climatic variability itself on species interactions has been little explored. Here, we compare caterpillar-parasitoid interactions across a broad gradient of climatic variability and find that the combined data in 15 geographically dispersed databases show a decrease in levels of parasitism as climatic variability increases. The dominant contribution to this pattern by relatively specialized parasitoid wasps suggests that climatic variability impairs the ability of parasitoids to track host populations. Given the important role of parasitoids in regulating insect herbivore populations in natural and managed systems, we predict an increase in the frequency and intensity of herbivore outbreaks through a disruption of enemy-herbivore dynamics as climates become more variable.climate change ͉ herbivore ͉ outbreak ͉ parasitoid ͉ top-down
Eyespots on the wings of nymphalid butterflies represent colorful examples of pattern formation, yet the developmental origins and mechanisms underlying eyespot center differentiation are still poorly understood. Using CRISPR-Cas9 we re-examine the function of Distal-less (Dll) as an activator or repressor of eyespots, a topic that remains controversial. We show that the phenotypic outcome of CRISPR mutations depends upon which specific exon is targeted. In Bicyclus anynana , exon 2 mutations are associated with both missing and ectopic eyespots, and also exon skipping. Exon 3 mutations, which do not lead to exon skipping, produce only null phenotypes, including missing eyespots, lighter wing coloration and loss of scales. Reaction-diffusion modeling of Dll function, using Wnt and Dpp as candidate morphogens, accurately replicates these complex crispant phenotypes. These results provide new insight into the function of Dll as a potential activator of eyespot development, scale growth and melanization, and suggest that the tuning of Dll expression levels can generate a diversity of eyespot phenotypes, including their appearance on the wing.
Ecologists debate whether tropical insect diversity is better explained by higher plant diversity or by host plant species specialization. However, plant-herbivore studies are primarily based in lowland rainforests (RF) thus excluding topographical effects on biodiversity. We examined turnover in Eois (Geometridae) communities across elevation by studying elevational transects in Costa Rica and Ecuador. We found four distinct Eois communities existing across the elevational gradients. Herbivore diversity was highest in montane forests (MF), whereas host plant diversity was highest in lowland RF. This was correlated with higher specialization and species richness of Eois/host plant species we found in MF. Based on these relationships, Neotropical Eois richness was estimated to range from 313 (only lowland RF considered) to 2034 (considering variation with elevation). We conclude that tropical herbivore diversity and diet breadth covary significantly with elevation and urge the inclusion of montane ecosystems in host specialization and arthropod diversity estimates.
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).
Butterfly eyespots are beautiful novel traits with an unknown developmental origin. Here we show that eyespots likely originated via cooption of parts of an ancestral appendage gene-regulatory network (GRN) to novel locations on the wing. Using comparative transcriptome analysis, we show that eyespots cluster most closely with antennae, relative to multiple other tissues. Furthermore, three genes essential for eyespot development, Distal-less (Dll), spalt (sal), and Antennapedia (Antp), share similar regulatory connections as those observed in the antennal GRN. CRISPR knockout of cis-regulatory elements (CREs) for Dll and sal led to the loss of eyespots, antennae, legs, and also wings, demonstrating that these CREs are highly pleiotropic. We conclude that eyespots likely reused an ancient GRN for their development, a network also previously implicated in the development of antennae, legs, and wings.
The extraordinary diversity of tropical herbivores may be linked to hostplant specialization driven in part by variation in pressure from natural enemies. We quantified levels of host-specificity and parasitoid attack for the specialist herbivore, Eois (Geometridae). The goals of this research were to examine: 1) whether Eois are specialized on the genus Piper (Piperaceae) and if hostplant specialization varies geographically; 2) whether Eois are equally vulnerable to parasitoid attack across different geographic regions and by the same parasitoid families; and 3) whether parasitism levels vary with precipitation and elevation. Based on over 15,000 rearings, we found Eois caterpillars feeding exclusively on Piper. However, we did not detect geographic differences in host-specificity; each Eois species fed on an average of two Piper species. Parasitism levels of Eois varied significantly with climate and topography; Eois were most vulnerable to parasitoid attack in moist versus dry and wet forests and at low versus high elevations. The diversity of parasitoid families reared from Eois was greater in Ecuador and Costa Rica than in Panama, where parasitoids were primarily in the family Braconidae. The quantitative evidence for host-specificity provides support for the hypothesis that Eois are specialized on Piper. Our results also reveal that Eois are exposed to a mosaic of potential selective pressures due to variation in parasitoid attack over a large spatial scale.
BackgroundButterfly wing color patterns are an important model system for understanding the evolution and development of morphological diversity and animal pigmentation. Wing color patterns develop from a complex network composed of highly conserved patterning genes and pigmentation pathways. Patterning genes are involved in regulating pigment synthesis however the temporal expression dynamics of these interacting networks is poorly understood. Here, we employ next generation sequencing to examine expression patterns of the gene network underlying wing development in the nymphalid butterfly, Vanessa cardui.ResultsWe identified 9, 376 differentially expressed transcripts during wing color pattern development, including genes involved in patterning, pigmentation and gene regulation. Differential expression of these genes was highest at the pre-ommochrome stage compared to early pupal and late melanin stages. Overall, an increasing number of genes were down-regulated during the progression of wing development. We observed dynamic expression patterns of a large number of pigment genes from the ommochrome, melanin and also pteridine pathways, including contrasting patterns of expression for paralogs of the yellow gene family. Surprisingly, many patterning genes previously associated with butterfly pattern elements were not significantly up-regulated at any time during pupation, although many other transcription factors were differentially expressed. Several genes involved in Notch signaling were significantly up-regulated during the pre-ommochrome stage including slow border cells, bunched and pebbles; the function of these genes in the development of butterfly wings is currently unknown. Many genes involved in ecdysone signaling were also significantly up-regulated during early pupal and late melanin stages and exhibited opposing patterns of expression relative to the ecdysone receptor. Finally, a comparison across four butterfly transcriptomes revealed 28 transcripts common to all four species that have no known homologs in other metazoans.ConclusionsThis study provides a comprehensive list of differentially expressed transcripts during wing development, revealing potential candidate genes that may be involved in regulating butterfly wing patterns. Some differentially expressed genes have no known homologs possibly representing genes unique to butterflies. Results from this study also indicate that development of nymphalid wing patterns may arise not only from melanin and ommochrome pigments but also the pteridine pigment pathway.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2586-5) contains supplementary material, which is available to authorized users.
Abstract:Rainfall seasonality can strongly influence biotic interactions by affecting host plant quality, and thus potentially regulating herbivore exposure to natural enemies. Plant defences are predicted to increase from dry to wet forests, rendering wet-forest caterpillars more vulnerable to parasitoids due to the slow-growth-high-mortality hypothesis. We collected and reared caterpillars from the understorey and trail edges of a wet forest and a seasonally dry forest to determine whether wet-forest caterpillars suffered a higher prevalence of parasitism and were less abundant than dry-forest caterpillars. In the two forests, caterpillar abundances (on average 8 h −1 ) and prevalence of parasitism (18%) were very similar regardless of feeding niche for both parasitism (27% versus 29% in shelter builders, and 16% versus 11% in external feeders) and caterpillar abundances (shelter builders: 1.42 versus 2.39, and external feeders: 8.27 versus 5.49 caterpillars h −1 ) in the dry and wet forests, respectively. A similar comparative analysis conducted in the canopy and understorey of the dry forest revealed a higher prevalence of parasitism in the canopy (43%) despite caterpillar densities similar to those in the understorey. Overall, shelter builders suffered higher parasitism than external feeders (32% versus 14.9%), and were attacked primarily by flies, whereas external feeders were more vulnerable to attack by parasitoid wasps.
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